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Park S, Kim H, Jung J, Lee S. Effects of Sacroiliac Joint Manipulation on Autonomic Nervous System and Lower Abdominal Pain in Women with Primary Dysmenorrhoea: A Randomized Controlled Trial. MEDICINA (KAUNAS, LITHUANIA) 2024; 60:2068. [PMID: 39768946 PMCID: PMC11677759 DOI: 10.3390/medicina60122068] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 11/21/2024] [Revised: 12/06/2024] [Accepted: 12/14/2024] [Indexed: 01/11/2025]
Abstract
Background and Objectives: Autonomic nervous system (ANS) disorders are responsible for primary dysmenorrhea and are closely linked to the spine. This study aims to evaluate the effects of sacroiliac joint manipulation on the ANS and lower abdominal pain in women with primary dysmenorrhea and proposes an alternative treatment method. Materials and Methods: A total of 40 participants were randomly assigned; however, 35 participants remained in the final analysis after 5 dropped out; they were assigned to either the sacroiliac joint manipulation group (n = 18) or the superficial heat therapy group (n = 17). Assessments included heart rate variability (HRV), visual analogue scale (VAS) scores for lower abdominal pain, the pressure pain threshold (PPT) of the sacroiliac joint, and the Moos Menstrual Distress Questionnaire (MMDQ) at baseline and after 4 weeks. Only the VAS and MMDQ scores were reassessed after 8 weeks to evaluate the sustained effects of the treatment. Results: Changes in HRV showed improvements in ANS balance only in the sacroiliac joint manipulation group (p < 0.05). It was found to be more effective than superficial heat therapy (p < 0.05). A significant decrease in lower abdominal pain following the intervention was observed in both groups (p < 0.05), along with the sustained effects of the treatment (p < 0.05). The MMDQ scores decreased after sacroiliac joint manipulation (p < 0.05), with greater improvements compared to the superficial heat therapy (p < 0.05). Conclusions: Sacroiliac joint manipulation positively affects ANS balance and is effective in alleviating lower abdominal pain and menstruation-related symptoms, with sustained effects observed over time. Therefore, sacroiliac joint manipulation can be an effective alternative treatment for women with primary dysmenorrhea.
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Affiliation(s)
- Sungeon Park
- Department of Physical Therapy, Graduate School, Sahmyook University, 815, Hwarang-ro, Seoul 01795, Republic of Korea;
| | - Hyunjoong Kim
- Department of Senior Exercise Prescription, Gwangju Health University, Bungmun-daero 419 beon-gil, Gwangju 62287, Republic of Korea;
| | - Jihye Jung
- Institute of SMART Rehabilitation, Sahmyook University, 815, Hwarang-ro, Seoul 01795, Republic of Korea;
| | - Seungwon Lee
- Institute of SMART Rehabilitation, Sahmyook University, 815, Hwarang-ro, Seoul 01795, Republic of Korea;
- Department of Physical Therapy, Sahmyook University, 815, Hwarang-ro, Seoul 01795, Republic of Korea
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Cawley DR, Seton B, Logullo D, Pandey R, Tickal A, Onyeke A, Jones C, Saliba N, Moralejo L, Pearson WG. Autonomic recalibration: A pilot study documenting mechanistic evidence for a trauma-informed manual therapy for chronic pain. J Bodyw Mov Ther 2024; 40:1985-1993. [PMID: 39593555 DOI: 10.1016/j.jbmt.2024.10.061] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2024] [Revised: 10/06/2024] [Accepted: 10/20/2024] [Indexed: 11/28/2024]
Affiliation(s)
- Daniel R Cawley
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Bob Seton
- Edward Via College of Osteopathic Medicine Auburn Campus, USA; Hope Institute for Human Performance, USA.
| | - Drew Logullo
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Rishika Pandey
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Adam Tickal
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Amanda Onyeke
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Cody Jones
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Natalie Saliba
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
| | - Laura Moralejo
- Edward Via College of Osteopathic Medicine Auburn Campus, USA.
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Fischbach AK, Satpute AB, Quigley K, Kragel PA, Chen D, Bianciardi M, Wald L, Wager TD, Choi JK, Zhang J, Barrett LF, Theriault JE. Seven Tesla Evidence for Columnar and Rostral-Caudal Organization of the Human Periaqueductal Gray Response in the Absence of Threat: A Working Memory Study. J Neurosci 2024; 44:e1757232024. [PMID: 38664013 PMCID: PMC11211719 DOI: 10.1523/jneurosci.1757-23.2024] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/12/2023] [Revised: 03/01/2024] [Accepted: 04/08/2024] [Indexed: 06/28/2024] Open
Abstract
The periaqueductal gray (PAG) is a small midbrain structure that surrounds the cerebral aqueduct, regulates brain-body communication, and is often studied for its role in "fight-or-flight" and "freezing" responses to threat. We used ultra-high-field 7 T fMRI to resolve the PAG in humans and distinguish it from the cerebral aqueduct, examining its in vivo function during a working memory task (N = 87). Both mild and moderate cognitive demands elicited spatially similar patterns of whole-brain blood oxygenation level-dependent (BOLD) response, and moderate cognitive demand elicited widespread BOLD increases above baseline in the brainstem. Notably, these brainstem increases were not significantly greater than those in the mild demand condition, suggesting that a subthreshold brainstem BOLD increase occurred for mild cognitive demand as well. Subject-specific masks were group aligned to examine PAG response. In PAG, both mild and moderate demands elicited a well-defined response in ventrolateral PAG, a region thought to be functionally related to anticipated painful threat in humans and nonhuman animals-yet, the present task posed only the most minimal (if any) "threat," with the cognitive tasks used being approximately as challenging as remembering a phone number. These findings suggest that the PAG may play a more general role in visceromotor regulation, even in the absence of threat.
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Affiliation(s)
| | - Ajay B Satpute
- Department of Psychology, Northeastern University, Boston, Massachusetts 02115
| | - Karen Quigley
- Department of Psychology, Northeastern University, Boston, Massachusetts 02115
| | - Philip A Kragel
- Department of Psychology, Emory University, Atlanta, Georgia 30322
| | - Danlei Chen
- Department of Psychology, Northeastern University, Boston, Massachusetts 02115
| | - Marta Bianciardi
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129
| | - Larry Wald
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129
| | - Tor D Wager
- Department of Psychological and Brain Sciences, Dartmouth College, Hanover, New Hampshire 03755
| | - Ji-Kyung Choi
- Department of Surgery, University of California, San Francisco, California 94143
| | - Jiahe Zhang
- Department of Psychology, Northeastern University, Boston, Massachusetts 02115
| | | | - Jordan E Theriault
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129
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Weizman L, Sharon H, Dayan L, Espaniol J, Brill S, Nahman-Averbuch H, Hendler T, Jacob G. Oral Delta-9-Tetrahydrocannabinol (THC) Increases Parasympathetic Activity and Supraspinal Conditioned Pain Modulation in Chronic Neuropathic Pain Male Patients: A Crossover, Double-Blind, Placebo-Controlled Trial. CNS Drugs 2024; 38:375-385. [PMID: 38597988 PMCID: PMC11026292 DOI: 10.1007/s40263-024-01085-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 03/11/2024] [Indexed: 04/11/2024]
Abstract
BACKGROUND Disordered autonomic nervous system regulation and supraspinal pain inhibition have been repeatedly described in chronic pain. We aimed to explore the effects of δ-9-tetrahydrocannabinol (THC), an emerging treatment option, on autonomic nervous system and central pain modulation measures in patients with chronic pain. METHODS Twelve male patients with chronic radicular neuropathic pain participated in a randomized, double-blind, crossover, placebo-controlled, single-administration trial. Low/high frequency (LF/HF) heart rate variability (HRV) ratio and conditioned pain modulation (CPM) response were measured and resting-state functional magnetic resonance imaging (MRI) was performed at baseline and after sublingual administration of either 0.2 mg/kg oral THC or placebo. RESULTS THC significantly reduced the LF/HF ratio compared with placebo (interaction effect F(1,11) = 20.5; p < 0.005) and significantly improved CPM responses (interaction effect F(1,9) = 5.2; p = 0.048). The THC-induced reduction in LF/HF ratio correlated with increased functional connectivity between the rostral ventrolateral medulla and the dorsolateral prefrontal cortex [T(10) = 6.4, cluster p-FDR < 0.005]. CONCLUSIONS THC shifts the autonomic balance towards increased parasympathetic tone and improves inhibitory pain mechanisms in chronic pain. The increase in vagal tone correlates with connectivity changes in higher-order regulatory brain regions, suggesting THC exerts top-down effects. These changes may reflect a normalizing effect of THC on multiple domains of supraspinal pain dysregulation. CLINICAL TRIAL REGISTRY NUMBER NCT02560545.
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Affiliation(s)
- Libat Weizman
- Sagol Brain Institute, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Haggai Sharon
- Sagol Brain Institute, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel
- Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
- School of Medicine, Tel Aviv University, Tel Aviv, Israel
- Department of Anesthesiology and Critical Care Medicine, Institute of Pain Medicine, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Lior Dayan
- Department of Anesthesiology and Critical Care Medicine, Institute of Pain Medicine, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Joumana Espaniol
- Department of Internal Medicine F, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
- Recanati Autonomic Dysfunction Center, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Silviu Brill
- Department of Anesthesiology and Critical Care Medicine, Institute of Pain Medicine, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Hadas Nahman-Averbuch
- Division of Clinical and Translational Research, Department of Anesthesiology, Washington University Pain Center, Washington University in St Louis School of Medicine, St Louis, MO, USA
| | - Talma Hendler
- Sagol Brain Institute, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel
- Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
- School of Medicine, Tel Aviv University, Tel Aviv, Israel
- School of Psychological Sciences, Tel Aviv University, Tel-Aviv, Israel
| | - Giris Jacob
- Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.
- School of Medicine, Tel Aviv University, Tel Aviv, Israel.
- Department of Internal Medicine F, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
- Recanati Autonomic Dysfunction Center, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel.
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Wegeberg AM, Sejersgaard-Jacobsen TH, Brock C, Drewes AM. Prediction of pain using electrocardiographic-derived autonomic measures: A systematic review. Eur J Pain 2024; 28:199-213. [PMID: 37655709 DOI: 10.1002/ejp.2175] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2023] [Revised: 08/08/2023] [Accepted: 08/18/2023] [Indexed: 09/02/2023]
Abstract
BACKGROUND AND OBJECTIVE Pain is a major clinical challenge, and understanding the pathophysiology is critical for optimal management. The autonomic nervous system reacts to pain stimuli, and autonomic dysfunction may predict pain sensation. The most used assessment of autonomic function is based on electrocardiographic measures, and the ability of such measures to predict pain was investigated. DATABASES AND DATA TREATMENT English articles indexed in PubMed and EMBASE were reviewed for eligibility and included when they reported electrocardiographic-derived measures' ability to predict pain response. The quality in prognostic studies (QUIPS) tool was used to assess the quality of the included articles. RESULTS The search revealed 15 publications, five on experimental pain, five on postoperative pain, and five on longitudinal clinical pain changes, investigating a total of 1069 patients. All studies used electrocardiographically derived parameters to predict pain assessed with pain thresholds using quantitative sensory testing or different scales. Across all study modalities, electrocardiographic measures were able to predict pain. Higher parasympathetic activity predicted decreased experimental, postoperative, and long-term pain in most cases while changes in sympathetic activity did not consistently predict pain. CONCLUSIONS Most studies demonstrated that parasympathetic activity could predict acute and chronic pain intensity. In the clinic, this may be used to identify which patients need more intensive care to prevent, for example postoperative pain and develop personalized chronic pain management. SIGNIFICANCE Pain is a debilitating problem, and the ability to predict occurrence and severity would be a useful clinical tool. Basal autonomic tone has been suggested to influence pain perception. This systematic review investigated electrocardiographic-derived autonomic tone and found that increased parasympathetic tone could predict pain reduction in different types of pain.
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Affiliation(s)
- Anne-Marie Wegeberg
- Thisted Research Unit, Aalborg University Hospital Thisted, Thisted, Denmark
- Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
- Mech-Sense, Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
| | | | - Christina Brock
- Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
- Mech-Sense, Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
- Steno Diabetes Center North Denmark, Aalborg, Denmark
| | - Asbjørn Mohr Drewes
- Thisted Research Unit, Aalborg University Hospital Thisted, Thisted, Denmark
- Mech-Sense, Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
- Steno Diabetes Center North Denmark, Aalborg, Denmark
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Kleber F, Reif A, de Greck M. The effect of social exclusion on pain perception and heart rate variability in healthy controls and somatoform pain patients. Scand J Pain 2024; 24:sjpain-2024-0042. [PMID: 39629686 DOI: 10.1515/sjpain-2024-0042] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/27/2024] [Accepted: 10/25/2024] [Indexed: 12/24/2024]
Abstract
OBJECTIVES The overlapping neural networks of social and physical pain have been investigated intensively in recent years. It was postulated that triggering social pain might result in greater physical pain. Nonetheless, how this affects somatoform pain disorder has not yet been considered. Since an increased pain processing activity is reported in these patients, the investigation of social exclusion and its effect on this group seems interesting. Hence, the aim of this study was to compare the influence of social exclusion on healthy controls and patients with somatoform pain disorder. METHODS Nineteen patients with somatoform pain disorder and 19 healthy controls were examined. Cyberball, a virtual ball-tossing paradigm, was used to experimentally induce social exclusion and inclusion. To measure effects on pain perception, pressure pain thresholds and heart rate variability (HRV) were recorded after each round of cyberball. Demographic data, pain medication, and potential psychosocial moderators were collected by questionnaires. RESULTS After social exclusion, pressure pain thresholds were significantly reduced in healthy controls (p < 0.01) as well as somatoform pain patients (p < 0.05), while HRV increased only in patients with somatoform pain disorder (p < 0.05) indicating increased parasympathetic activity. CONCLUSION This study is the first to analyse the effects of social exclusion on pain perception in somatoform pain disorder. While the reduction in pressure pain thresholds is in line with the social pain literature, the effects on HRV could be interpreted as a form of pain regulation mechanism. However, further research is needed to investigate the role of parasympathetic activity in socially excluded somatoform pain patients.
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Affiliation(s)
- Fabrice Kleber
- Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany
| | - Andreas Reif
- Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany
| | - Moritz de Greck
- Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany
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7
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Forte G, Troisi G, Favieri F, De Pascalis V, Langher V, Casagrande M. Inhibition and Heart Rate Variability in Experimentally Induced Pain. J Pain Res 2023; 16:3239-3249. [PMID: 37790193 PMCID: PMC10542212 DOI: 10.2147/jpr.s418238] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2023] [Accepted: 08/03/2023] [Indexed: 10/05/2023] Open
Abstract
Introduction Pain is a complex experience that requires executive functions (EFs) to be processed. The autonomic outcome of the neural networks involved in the cognitive evaluation of pain is reflected by heart rate variability (HRV), an index of self-regulation abilities. Although some results suggest a relationship between HRV, EFs, and pain, studies focusing on this three-way relationship are still scarce. Objective This study aims to investigate the relationship between pain, cognitive, and autonomic mechanisms, hypothesizing an association between resting HRV and both cognitive and motor inhibition as indices of executive functioning. This relationship was investigated after an experimental-induced pain. Methods Seventy-six young adults were exposed to the Cold Pressure Arm Warp to induce experimental pain. HRV was collected, and cognitive tasks were administered to assess executive performance. Results The results showed that (1) HRV indices significantly increased during pain stimulation, (2) cognitive inhibition was positively correlated with vagal indices and with pain parameters, (3) both inhibition tasks significantly predicted pain threshold while the performance on the Stroop Task predicted pain tolerance. Conclusion Results suggest a three-way relationship. Further research would focus on the role of HRV and cognitive strategies in pain management in chronic pain conditions.
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Affiliation(s)
- Giuseppe Forte
- Department of Dynamic and Clinical Psychology and Health Studies, Sapienza University of Rome, Roma, 00185, Italy
| | - Giovanna Troisi
- Department of Psychology, Sapienza University of Rome, Roma, 00185, Italy
| | - Francesca Favieri
- Department of Dynamic and Clinical Psychology and Health Studies, Sapienza University of Rome, Roma, 00185, Italy
| | | | - Viviana Langher
- Department of Dynamic and Clinical Psychology and Health Studies, Sapienza University of Rome, Roma, 00185, Italy
| | - Maria Casagrande
- Department of Dynamic and Clinical Psychology and Health Studies, Sapienza University of Rome, Roma, 00185, Italy
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Scheuren PS, Bösch S, Rosner J, Allmendinger F, Kramer JLK, Curt A, Hubli M. Priming of the autonomic nervous system after an experimental human pain model. J Neurophysiol 2023; 130:436-446. [PMID: 37405990 PMCID: PMC10625835 DOI: 10.1152/jn.00064.2023] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/07/2023] [Revised: 07/02/2023] [Accepted: 07/03/2023] [Indexed: 07/07/2023] Open
Abstract
Modulated autonomic responses to noxious stimulation have been reported in experimental and clinical pain. These effects are likely mediated by nociceptive sensitization, but may also, more simply reflect increased stimulus-associated arousal. To disentangle between sensitization- and arousal-mediated effects on autonomic responses to noxious input, we recorded sympathetic skin responses (SSRs) in response to 10 pinprick and heat stimuli before (PRE) and after (POST) an experimental heat pain model to induce secondary hyperalgesia (EXP) and a control model (CTRL) in 20 healthy females. Pinprick and heat stimuli were individually adapted for pain perception (4/10) across all assessments. Heart rate, heart rate variability, and skin conductance level (SCL) were assessed before, during, and after the experimental heat pain model. Both pinprick- and heat-induced SSRs habituated from PRE to POST in CTRL, but not EXP (P = 0.033). Background SCL (during stimuli application) was heightened in EXP compared with CTRL condition during pinprick and heat stimuli (P = 0.009). Our findings indicate that enhanced SSRs after an experimental pain model are neither fully related to subjective pain, as SSRs dissociated from perceptual responses, nor to nociceptive sensitization, as SSRs were enhanced for both modalities. Our findings can, however, be explained by priming of the autonomic nervous system during the experimental pain model, which makes the autonomic nervous system more susceptible to noxious input. Taken together, autonomic readouts have the potential to objectively assess not only nociceptive sensitization but also priming of the autonomic nervous system, which may be involved in the generation of distinct clinical pain phenotypes.NEW & NOTEWORTHY The facilitation of pain-induced sympathetic skin responses observed after experimentally induced central sensitization is unspecific to the stimulation modality and thereby unlikely solely driven by nociceptive sensitization. In addition, these enhanced pain-induced autonomic responses are also not related to higher stimulus-associated arousal, but rather a general priming of the autonomic nervous system. Hence, autonomic readouts may be able to detect generalized hyperexcitability in chronic pain, beyond the nociceptive system, which may contribute to clinical pain phenotypes.
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Affiliation(s)
- Paulina Simonne Scheuren
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
- Department of Neurology, University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
| | - Sofia Bösch
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Jan Rosner
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
- Department of Neurology, University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
- Danish Pain Research Centre, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
| | - Florin Allmendinger
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - John Lawrence Kipling Kramer
- International Collaboration on Repair Discoveries (ICORD), University of British Columbia, Vancouver, British Columbia, Canada
- Department of Anesthesiology, Pharmacology & Therapeutics, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada
| | - Armin Curt
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Michèle Hubli
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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Viti A, Panconi G, Guarducci S, Garfagnini S, Mondonico M, Bravi R, Minciacchi D. Modulation of Heart Rate Variability following PAP Ion Magnetic Induction Intervention in Subjects with Chronic Musculoskeletal Pain: A Pilot Randomized Controlled Study. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2023; 20:3934. [PMID: 36900946 PMCID: PMC10001461 DOI: 10.3390/ijerph20053934] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 01/12/2023] [Revised: 02/18/2023] [Accepted: 02/19/2023] [Indexed: 06/18/2023]
Abstract
Heart rate variability (HRV) analysis has emerged as a simple and non-invasive technique to indirectly evaluate the autonomic nervous system (ANS), and it is considered a sensible and advanced index of health status. Pulsed electromagnetic fields (PEMFs) are widely used in clinical settings for improving the health status of individuals with chronic musculoskeletal pain. The aim of the present single-blind, randomized, placebo-controlled parallel pilot study was to investigate the acute effect of a single session of PEMFs stimulation by a PAP ion magnetic induction (PAPIMI) device on ANS activity, as measured by HRV, in patients with chronic musculoskeletal pain, and compare such effect with that induced by a sham (control) PAPIMI inductor. Thirty-two patients were randomized into two groups: PAPIMI intervention (PAP) (n = 17) and sham PAPIMI intervention (SHAM-PAP) (n = 15). HRV was assessed before and following the interventions. The PAP group showed a significant increase in all values of the time-domain parameters (SDNN, RMSSD, NN50, and pNN50) and the HF component of HRV, suggesting a parasympathetic effect. In contrast, the SHAM-PAP group showed no significant differences in all HRV indices following the intervention. Preliminary findings suggested that PAPIMI inductor could influence ANS activity and provided initial evidence of the potential physiological response induced by the PAPIMI device.
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Affiliation(s)
- Antonio Viti
- Centro Fisioterapico Apuano, Via delle Contrade 242, 55047 Lucca, Italy
| | - Giulia Panconi
- Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, 50134 Florence, Italy
| | - Sara Guarducci
- Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, 50134 Florence, Italy
| | | | - Mosè Mondonico
- Centro Fisioterapico Apuano, Via delle Contrade 242, 55047 Lucca, Italy
| | - Riccardo Bravi
- Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, 50134 Florence, Italy
| | - Diego Minciacchi
- Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, 50134 Florence, Italy
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10
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Bonin EAC, Lejeune N, Szymkowicz E, Bonhomme V, Martial C, Gosseries O, Laureys S, Thibaut A. Assessment and management of pain/nociception in patients with disorders of consciousness or locked-in syndrome: A narrative review. Front Syst Neurosci 2023; 17:1112206. [PMID: 37021037 PMCID: PMC10067681 DOI: 10.3389/fnsys.2023.1112206] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2022] [Accepted: 03/06/2023] [Indexed: 04/07/2023] Open
Abstract
The assessment and management of pain and nociception is very challenging in patients unable to communicate functionally such as patients with disorders of consciousness (DoC) or in locked-in syndrome (LIS). In a clinical setting, the detection of signs of pain and nociception by the medical staff is therefore essential for the wellbeing and management of these patients. However, there is still a lot unknown and a lack of clear guidelines regarding the assessment, management and treatment of pain and nociception in these populations. The purpose of this narrative review is to examine the current knowledge regarding this issue by covering different topics such as: the neurophysiology of pain and nociception (in healthy subjects and patients), the source and impact of nociception and pain in DoC and LIS and, finally, the assessment and treatment of pain and nociception in these populations. In this review we will also give possible research directions that could help to improve the management of this specific population of severely brain damaged patients.
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Affiliation(s)
- Estelle A. C. Bonin
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
| | - Nicolas Lejeune
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre Hospitalier Neurologique (CHN) William Lennox, Saint-Luc Hospital Group, Ottignies-Louvain-la-Neuve, Belgium
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
| | - Emilie Szymkowicz
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
| | - Vincent Bonhomme
- Department of Anesthesia and Intensive Care Medicine, Liège University Hospital, Liège, Belgium
- Anesthesia and Perioperative Neuroscience Laboratory, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
| | - Charlotte Martial
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
| | - Olivia Gosseries
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
| | - Steven Laureys
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
- Joint International Research Unit on Consciousness, CERVO Brain Research Centre, Centre Intégré Universitaire de Santé et Services Sociaux (CIUSS), University Laval, Québec City, QC, Canada
| | - Aurore Thibaut
- Coma Science Group, GIGA-Consciousness Thematic Unit, GIGA-Research, Liège, Belgium
- Centre du Cerveau, Liège University Hospital, Liège, Belgium
- *Correspondence: Aurore Thibaut,
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11
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Scheuren PS, De Schoenmacker I, Rosner J, Brunner F, Curt A, Hubli M. Pain-autonomic measures reveal nociceptive sensitization in complex regional pain syndrome. Eur J Pain 2023; 27:72-85. [PMID: 36130736 PMCID: PMC10092513 DOI: 10.1002/ejp.2040] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2022] [Revised: 09/01/2022] [Accepted: 09/17/2022] [Indexed: 12/15/2022]
Abstract
BACKGROUND Allodynia and hyperalgesia are common signs in individuals with complex regional pain syndrome (CRPS), mainly attributed to sensitization of the nociceptive system. Appropriate diagnostic tools for the objective assessment of such hypersensitivities are still lacking, which are essential for the development of mechanism-based treatment strategies. OBJECTIVES This study investigated the use of pain-autonomic readouts to objectively detect sensitization processes in CRPS. METHODS Twenty individuals with chronic CRPS were recruited for the study alongside 16 age- and sex-matched healthy controls (HC). All individuals underwent quantitative sensory testing and neurophysiological assessments. Sympathetic skin responses (SSRs) were recorded in response to 15 pinprick and 15 noxious heat stimuli of the affected (CRPS hand/foot) and a control area (contralateral shoulder/hand). RESULTS Individuals with CRPS showed increased mechanical pain sensitivity and increased SSR amplitudes compared with HC in response to pinprick and heat stimulation of the affected (p < 0.001), but not in the control area (p > 0.05). Habituation of pinprick-induced SSRs was reduced in CRPS compared to HC in both the affected (p = 0.018) and slightly in the control area (p = 0.048). Habituation of heat-induced SSR was reduced in CRPS in the affected (p = 0.008), but not the control area (p = 0.053). CONCLUSIONS This is the first study demonstrating clinical evidence that pain-related autonomic responses may represent objective tools to quantify sensitization processes along the nociceptive neuraxis in CRPS (e.g. widespread hyperexcitability). Pain-autonomic readouts could help scrutinize mechanisms underlying the development and maintenance of chronic pain in CRPS and provide valuable metrics to detect mechanism-based treatment responses in clinical trials. SIGNIFICANCE This study provides clinical evidence that autonomic measures to noxious stimuli can objectively detect sensitization processes along the nociceptive neuraxis in complex regional pain syndrome (CRPS) (e.g. widespread hyperexcitability). Pain-autonomic readouts may represent valuable tools to explore pathophysiological mechanisms in a variety of pain patients and offer novel avenues to help guide mechanism-based therapeutic strategies.
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Affiliation(s)
- Paulina S Scheuren
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.,Department of Neurology, University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
| | - Iara De Schoenmacker
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Jan Rosner
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.,Department of Neurology, University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
| | - Florian Brunner
- Department of Physical Medicine and Rheumatology, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Armin Curt
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Michèle Hubli
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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12
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Wank I, Niedermair T, Kronenberg D, Stange R, Brochhausen C, Hess A, Grässel S. Influence of the Peripheral Nervous System on Murine Osteoporotic Fracture Healing and Fracture-Induced Hyperalgesia. Int J Mol Sci 2022; 24:510. [PMID: 36613952 PMCID: PMC9820334 DOI: 10.3390/ijms24010510] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/17/2022] [Revised: 12/16/2022] [Accepted: 12/20/2022] [Indexed: 12/29/2022] Open
Abstract
Osteoporotic fractures are often linked to persisting chronic pain and poor healing outcomes. Substance P (SP), α-calcitonin gene-related peptide (α-CGRP) and sympathetic neurotransmitters are involved in bone remodeling after trauma and nociceptive processes, e.g., fracture-induced hyperalgesia. We aimed to link sensory and sympathetic signaling to fracture healing and fracture-induced hyperalgesia under osteoporotic conditions. Externally stabilized femoral fractures were set 28 days after OVX in wild type (WT), α-CGRP- deficient (α-CGRP -/-), SP-deficient (Tac1-/-) and sympathectomized (SYX) mice. Functional MRI (fMRI) was performed two days before and five and 21 days post fracture, followed by µCT and biomechanical tests. Sympathectomy affected structural bone properties in the fracture callus whereas loss of sensory neurotransmitters affected trabecular structures in contralateral, non-fractured bones. Biomechanical properties were mostly similar in all groups. Both nociceptive and resting-state (RS) fMRI revealed significant baseline differences in functional connectivity (FC) between WT and neurotransmitter-deficient mice. The fracture-induced hyperalgesia modulated central nociception and had robust impact on RS FC in all groups. The changes demonstrated in RS FC in fMRI might potentially be used as a bone traumata-induced biomarker regarding fracture healing under pathophysiological musculoskeletal conditions. The findings are of clinical importance and relevance as they advance our understanding of pain during osteoporotic fracture healing and provide a potential imaging biomarker for fracture-related hyperalgesia and its temporal development. Overall, this may help to reduce the development of chronic pain after fracture thereby improving the treatment of osteoporotic fractures.
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Affiliation(s)
- Isabel Wank
- Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, Germany
| | - Tanja Niedermair
- Institute of Pathology, University of Regensburg, 93053 Regensburg, Germany
| | - Daniel Kronenberg
- Department of Regenerative Musculoskeletal Medicine, Institute of Musculoskeletal Medicine (IMM), University Hospital Münster, 48149 Münster, Germany
| | - Richard Stange
- Department of Regenerative Musculoskeletal Medicine, Institute of Musculoskeletal Medicine (IMM), University Hospital Münster, 48149 Münster, Germany
| | | | - Andreas Hess
- Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, Germany
| | - Susanne Grässel
- Centre for Medical Biotechnology (ZMB), Department of Orthopedic Surgery, Experimental Orthopedics, University of Regensburg, 93053 Regensburg, Germany
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13
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Chen H, Comnick C, Norman GJ, Caplan DJ, Jin XX, Fillingim RB. Triad Multisystem Phenotype with High-risk for Developing Temporomandibular Disorders- Characteristics and Potential Pathophysiology Results from the OPPERA Dataset. Pain 2022; 164:1027-1038. [PMID: 36661844 DOI: 10.1097/j.pain.0000000000002797] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2022] [Accepted: 09/20/2022] [Indexed: 01/21/2023]
Abstract
ABSTRACT A multisystem phenotype with the Triad of bodily pain, psychological distress, and sleep disturbance was found to have high risk for developing initial onset of painful temporomandibular disorders (TMDs) in the multicenter Orofacial Pain: Prospective Evaluation and Risk Assessment (OPPERA) dataset. In this study, we systemically examined phenotypic characteristics and explored potential pathophysiology in quantitative sensory testing (QST) and autonomic nervous system (ANS) domains in this multisystem Triad phenotype. Secondary analysis was performed on 1199 non-Triad and 154 Triad TMD-free OPPERA enrollees at baseline. Results indicate that prior to developing TMDs, the Triad phenotype demonstrated both orofacial and systemic signs and symptoms that can only be captured through multisystem assessment. In addition, we found significantly lower resting heart rate variability and higher resting heart rate in the Triad phenotype as compared to the non-Triad group. However, pain sensitivity measured by QST was not different between groups. These findings highlight the importance of whole-person multisystem assessment at the stage prior to developing complex pain conditions such as TMDs, and suggest that, in addition to a "tissue damage monitor", pain should be considered in a broader context, such as a component within a "distress monitoring system" at the whole-person level when multisystem issues co-present. Therefore, the presence or absence of multisystem issues may carry critical information when searching for disease mechanisms and developing mechanism-based intervention and prevention strategies for TMDs and related pain conditions. Cardiovascular autonomic function should be further researched when multisystem issues co-present prior to developing TMDs.
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Affiliation(s)
- Hong Chen
- the University of Iowa College of Dentistry, Department of Preventive and Community Dentistry
| | - Carissa Comnick
- University of Iowa College of Dentistry, Division of Biostatistics & Computational Biology and University of Iowa College of Public Health, Department of Biostatistics
| | | | - Daniel J Caplan
- the University of Iowa College of Dentistry, Department of Preventive and Community Dentistry
| | - Xie Xian Jin
- University of Iowa College of Dentistry, Division of Biostatistics & Computational Biology and University of Iowa College of Public Health, Department of Biostatistics
| | - Roger B Fillingim
- University of Florida College of Dentistry, Department of Community Dentistry and Behavioral Science
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14
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Sympathetic skin response as an objective tool to estimate stimulus-associated arousal in a human model of hyperalgesia. Neurophysiol Clin 2022; 52:436-445. [DOI: 10.1016/j.neucli.2022.10.002] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/18/2021] [Revised: 08/02/2022] [Accepted: 10/04/2022] [Indexed: 11/06/2022] Open
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15
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Chae Y, Park HJ, Lee IS. Pain modalities in the body and brain: Current knowledge and future perspectives. Neurosci Biobehav Rev 2022; 139:104744. [PMID: 35716877 DOI: 10.1016/j.neubiorev.2022.104744] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2022] [Revised: 05/29/2022] [Accepted: 06/11/2022] [Indexed: 11/16/2022]
Abstract
Development and validation of pain biomarkers has become a major issue in pain research. Recent advances in multimodal data acquisition have allowed researchers to gather multivariate and multilevel whole-body measurements in patients with pain conditions, and data analysis techniques such as machine learning have led to novel findings in neural biomarkers for pain. Most studies have focused on the development of a biomarker to predict the severity of pain with high precision and high specificity, however, a similar approach to discriminate different modalities of pain is lacking. Identification of more accurate and specific pain biomarkers will require an in-depth understanding of the modality specificity of pain. In this review, we summarize early and recent findings on the modality specificity of pain in the brain, with a focus on distinct neural activity patterns between chronic clinical and acute experimental pain, direct, social, and vicarious pain, and somatic and visceral pain. We also suggest future directions to improve our current strategy of pain management using our knowledge of modality-specific aspects of pain.
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Affiliation(s)
- Younbyoung Chae
- College of Korean Medicine, Kyung Hee University, Seoul, the Republic of Korea; Acupuncture & Meridian Science Research Center, Kyung Hee University, Seoul, the Republic of Korea
| | - Hi-Joon Park
- College of Korean Medicine, Kyung Hee University, Seoul, the Republic of Korea; Acupuncture & Meridian Science Research Center, Kyung Hee University, Seoul, the Republic of Korea
| | - In-Seon Lee
- College of Korean Medicine, Kyung Hee University, Seoul, the Republic of Korea; Acupuncture & Meridian Science Research Center, Kyung Hee University, Seoul, the Republic of Korea.
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16
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De Schoenmacker I, Leu C, Curt A, Hubli M. Pain‐autonomic interaction is a reliable measure of pain habituation in healthy subjects. Eur J Pain 2022; 26:1679-1690. [PMID: 35671124 PMCID: PMC9544564 DOI: 10.1002/ejp.1990] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2022] [Revised: 05/16/2022] [Accepted: 06/04/2022] [Indexed: 11/24/2022]
Abstract
Background Habituation is a response decrement resulting from repeated stimuli. Reduced habituation to noxious stimuli is considered to be a proxy for central sensitization in subjects with chronic pain. Despite numerous investigations of pain habituation in relation to central sensitization, there is no consensus on the most sensitive and reliable readout, as well as analysis approach. Therefore, this study compared the usability and reliability of different readouts and habituation analysis approaches to measure pain habituation in response to repetitive heat simulation. Methods Three blocks of 20 contact heat stimuli were applied on the volar forearm of 20 healthy subjects on two separate visits. Habituation was assessed by three different readouts: pain ratings, contact heat evoked potentials (CHEPs) and heat‐induced sympathetic skin responses (SSRs). In addition, two different habituation analysis approaches were used: between the three stimulation blocks (between‐block) and within the first stimulation block (within‐block). Results Significant between‐block habituation for SSRs (p < 0.001), but not for pain ratings (p = 1.000) and CHEPs (p = 0.078) was found. There was significant within‐block habituation for pain ratings (p = 0.012) and SSRs (p < 0.001), but not for CHEPs (p = 0.246). Only the between‐block habituation of heat‐induced SSR was reliable between the two visits (first to second block: intraclass correlation coefficient [ICC] = 0.58, p = 0.030; first to third block: ICC = 0.64, p = 0.015). Conclusion Heat‐induced SSR as a measure of pain‐autonomic interaction revealed the strongest pain habituation and showed the highest test–retest reliability.
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Affiliation(s)
- Iara De Schoenmacker
- Spinal Cord Injury CenterBalgrist University Hospital, University of ZurichZurichSwitzerland
| | - Chiara Leu
- Spinal Cord Injury CenterBalgrist University Hospital, University of ZurichZurichSwitzerland
- Institute of NeuroscienceUniversité Catholique de LouvainBrusselsBelgium
| | - Armin Curt
- Spinal Cord Injury CenterBalgrist University Hospital, University of ZurichZurichSwitzerland
| | - Michèle Hubli
- Spinal Cord Injury CenterBalgrist University Hospital, University of ZurichZurichSwitzerland
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17
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Acevedo AM, Leger KA, Jenkins BN, Pressman SD. Keep calm or get excited? Examining the effects of different types of positive affect on responses to acute pain. THE JOURNAL OF POSITIVE PSYCHOLOGY 2022. [DOI: 10.1080/17439760.2020.1858338] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 10/22/2022]
Affiliation(s)
- Amanda M. Acevedo
- Department of Psychological Science, University of California, Irvine, CA, USA
| | - Kate A. Leger
- Department of Psychology, University of Kentucky, Lexington, KY, USA
| | | | - Sarah D. Pressman
- Department of Psychological Science, University of California, Irvine, CA, USA
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18
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Forte G, Troisi G, Pazzaglia M, Pascalis VD, Casagrande M. Heart Rate Variability and Pain: A Systematic Review. Brain Sci 2022; 12:brainsci12020153. [PMID: 35203917 PMCID: PMC8870705 DOI: 10.3390/brainsci12020153] [Citation(s) in RCA: 87] [Impact Index Per Article: 29.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/27/2021] [Revised: 01/20/2022] [Accepted: 01/21/2022] [Indexed: 02/04/2023] Open
Abstract
Background and Objective: Heart rate variability (HRV) as an index of the autonomic nervous system appears to be related to reactivity to experimental pain stimuli. HRV could better explain the contributions of sympathetic and parasympathetic activity response to nociceptive stimulation. The aim of this study was to systematically review and synthesize the current evidence on HRV in relation to the experience of pain in experimental tasks. Databases and Data Treatment: Studies indexed in the PubMed, PsycINFO, MEDLINE, WebOfScience, and Scopus databases were reviewed for eligibility. Studies on the autonomic response (i.e., HRV) to experimentally induced pain in healthy adults were included. Different methods of pain induction were considered (e.g., thermal, pressure, and electrical). Data were synthesized considering the association between HRV and both pain induction and subjective measures of pain. Results: Seventy-one studies were included. The results underline significant change in both the sympathetic and parasympathetic autonomic nervous systems during the painful stimulation independent of the pain induction method. The autonomic reaction to pain could be affected by several factors, such as sex, age, body mass index, breathing patterns, the intensity of the stimulation, and the affective state. Moreover, an association between the autonomic nervous system and the subjective experience of pain was found. Higher parasympathetic activity was associated with better self-regulation capacities and, accordingly, a higher pain inhibition capacity. Conclusions: HRV appears to be a helpful marker to evaluate nociceptive response in experimentally induced pain. Future studies are also needed in clinical samples to understand better the interindividual changes of autonomic response due to pain stimuli.
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Affiliation(s)
- Giuseppe Forte
- Department of Psychology, “Sapienza” University of Rome, 00185 Rome, Italy; (M.P.); (V.D.P.)
- Body and Action Lab, IRCCS Fondazione Santa Lucia, Via Ardeatina 306, 00179 Rome, Italy
- Correspondence: (G.F.); (M.C.)
| | - Giovanna Troisi
- Department of Clinical and Dynamic Psychology and Health Studies, “Sapienza” University of Rome, 00185 Rome, Italy;
| | - Mariella Pazzaglia
- Department of Psychology, “Sapienza” University of Rome, 00185 Rome, Italy; (M.P.); (V.D.P.)
- Body and Action Lab, IRCCS Fondazione Santa Lucia, Via Ardeatina 306, 00179 Rome, Italy
| | - Vilfredo De Pascalis
- Department of Psychology, “Sapienza” University of Rome, 00185 Rome, Italy; (M.P.); (V.D.P.)
| | - Maria Casagrande
- Department of Clinical and Dynamic Psychology and Health Studies, “Sapienza” University of Rome, 00185 Rome, Italy;
- Correspondence: (G.F.); (M.C.)
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19
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Susam B, Riek N, Akcakaya M, Xu X, de Sa V, Nezamfar H, Diaz D, Craig K, Goodwin M, Huang J. Automated Pain Assessment in Children using Electrodermal Activity and Video Data Fusion via Machine Learning. IEEE Trans Biomed Eng 2021; 69:422-431. [PMID: 34242161 DOI: 10.1109/tbme.2021.3096137] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/07/2022]
Abstract
Pain assessment in children continues to challenge clinicians and researchers, as subjective experiences of pain require inference through observable behaviors, both involuntary and deliberate. The presented approach supplements the subjective self-report-based method by fusing electrodermal activity (EDA) recordings with video facial expressions to develop an objective pain assessment metric. Such an approach is specifically important for assessing pain in children who are not capable of providing accurate self-pain reports, requiring nonverbal pain assessment. We demonstrate the performance of our approach using data recorded from children in post-operative recovery following laparoscopic appendectomy. We examined separately and combined the usefulness of EDA and video facial expression data as predictors of childrens self-reports of pain following surgery through recovery. Findings indicate that EDA and facial expression data independently provide above chance sensitivities and specificities, but their fusion for classifying clinically significant pain vs. clinically nonsignificant pain achieved substantial improvement, yielding 90.91% accuracy, with 100% sensitivity and 81.82% specificity. The multimodal measures capitalize upon different features of the complex pain response. Thus, this paper presents both evidence for the utility of a weighted maximum likelihood algorithm as a novel feature selection method for EDA and video facial expression data and an accurate and objective automated classification algorithm capable of discriminating clinically significant pain from clinically nonsignificant pain in children.
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20
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Posada-Quintero HF, Kong Y, Chon KH. Objective pain stimulation intensity and pain sensation assessment using machine learning classification and regression based on electrodermal activity. Am J Physiol Regul Integr Comp Physiol 2021; 321:R186-R196. [PMID: 34133246 DOI: 10.1152/ajpregu.00094.2021] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
An objective measure of pain remains an unmet need of people with chronic pain, estimated to be 1/3 of the adult population in the United States. The current gold standard to quantify pain is highly subjective, based upon self-reporting with numerical or visual analog scale (VAS). This subjectivity complicates pain management and exacerbates the epidemic of opioid abuse. We have tested classification and regression machine learning models to objectively estimate pain sensation in healthy subjects using electrodermal activity (EDA). Twenty-three volunteers underwent pain stimulation using thermal grills. Three different "pain stimulation intensities" were induced for each subject, who reported the "pain sensation" right after each stimulus using a VAS (0-10). EDA data were collected throughout the experiment. For machine learning, we computed validated features of EDA based on time-domain decomposition, spectral analysis, and differential features. Models for estimation of pain stimulation intensity and pain sensation achieved maximum macroaveraged geometric mean scores of 69.7% and 69.2%, respectively, when three classes were considered ("No," "Low," and "High"). Regression of levels of stimulation intensity and pain sensation achieved R2 values of 0.357 and 0.47, respectively. Overall, the high variance and inconsistency of VAS scores led to lower performance of pain sensation classification, but regression was better for pain sensation than stimulation intensity. Our results provide that three levels of pain can be quantified with good accuracy and physiological evidence that sympathetic responses recorded by EDA are more correlated to the applied stimuli's intensity than to the pain sensation reported by the subject.
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Affiliation(s)
| | - Youngsun Kong
- Department of Biomedical Engineering, University of Connecticut, Storrs, Connecticut
| | - Ki H Chon
- Department of Biomedical Engineering, University of Connecticut, Storrs, Connecticut
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21
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Jaquess KJ, Allen N, Chun TJ, Crock L, Zajdel AA, Reinhard MJ, Costanzo ME. The relationship between Gulf War Illness symptom severity and heart rate variability: A pilot study. Life Sci 2021; 280:119663. [PMID: 34087286 DOI: 10.1016/j.lfs.2021.119663] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/06/2021] [Revised: 05/20/2021] [Accepted: 05/21/2021] [Indexed: 11/30/2022]
Abstract
INTRODUCTION Gulf War Illness (GWI) is a chronic multisymptom illness affecting 250,000+ veterans of the '90-'91 Gulf War which remains under-explored in terms of its physiological characteristics. We investigated whether subjective GWI symptom severity scores were related to objective measures of autonomic nervous system activity. METHODS We estimated activity in the two major branches of the autonomic nervous system (the parasympathetic nervous system [PNS] and the sympathetic nervous system [SNS]) via metrics of heart rate variability in a sample of Veterans who met established criteria for GWI with varying degrees of self-reported symptom severity. We hypothesized that subjective symptom severity scores would be inversely related to PNS activity and positively related to SNS activity. RESULTS Significant negative relationships were observed between the root mean square of successive differences of beat-to-beat intervals (a measure of PNS activity) and symptom severity, both overall and across specific GWI symptom categories (sp. fatigue [r = -0.574], gastrointestinal [r = -0.544]). Furthermore, significant positive relationships were observed between the cardiac sympathetic index and symptom severity, both overall and across specific symptom categories (sp. cognitive [r = 0.721], fatigue [r = 0.560], gastrointestinal [r = 0.694], skin [r = 0.686]). CONCLUSIONS Metrics of PNS activation revealed a negative relationship with self-reported symptom severity, while metrics of SNS activation revealed a positive relationship. The present results improve our understanding of the physiology of GWI and provide a new window from which to consider this medically unexplained illness.
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Affiliation(s)
- Kyle J Jaquess
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America; Department of Kinesiology, University of Maryland, College Park, MD, United States of America; Department of Psychology, Juniata College, Huntingdon, PA, United States of America.
| | - Nathaniel Allen
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America
| | - Timothy J Chun
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America
| | - Lucas Crock
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America
| | - Alexander A Zajdel
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America
| | - Matthew J Reinhard
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America; Department of Psychiatry, Georgetown University School of Medicine, Washington, DC, United States of America
| | - Michelle E Costanzo
- War Related Illness and Injury Study Center, Department of Veterans Affairs Washington, DC, United States of America
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22
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Kulthanan K, Ungprasert P, Tapechum S, Rujitharanawong C, Kiratiwongwan R, Munprom K, Terhorst-Molawi D, Maurer M. Vibratory Angioedema Subgroups, Features, and Treatment: Results of a Systematic Review. THE JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY-IN PRACTICE 2021; 9:971-984. [DOI: 10.1016/j.jaip.2020.09.009] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/06/2020] [Revised: 09/04/2020] [Accepted: 09/06/2020] [Indexed: 01/20/2023]
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23
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Feneberg AC, Kappert MB, Maidhof RM, Doering BK, Olbrich D, Nater UM. Efficacy, Treatment Characteristics, and Biopsychological Mechanisms of Music-Listening Interventions in Reducing Pain (MINTREP): Study Protocol of a Three-Armed Pilot Randomized Controlled Trial. Front Psychiatry 2020; 11:518316. [PMID: 33329075 PMCID: PMC7672017 DOI: 10.3389/fpsyt.2020.518316] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/07/2019] [Accepted: 09/22/2020] [Indexed: 11/24/2022] Open
Abstract
Background: Pain can severely compromise a person's overall health and well-being. Music-listening interventions have been shown to alleviate perceived pain and to modulate the body's stress-sensitive systems. Despite the growing evidence of pain- and stress-reducing effects of music-listening interventions from experimental and clinical research, current findings on music-induced analgesia are inconclusive regarding the role of specific treatment characteristics and the biopsychological mechanisms underlying these effects. Objective: The overall aim of this pilot randomized controlled trial is to test and compare the differential effects of frequency-modulated and unmodulated music (both researcher-selected) on experimentally induced perception of acute pain and to test the efficacy of the interventions in reducing biological and subjective stress levels. Moreover, these two interventions will be compared to a third condition, in which participants listen to self-selected unmodulated music. Methods and Analysis: A total of 90 healthy participants will be randomly allocated to one of the three music-listening intervention groups. Each intervention encompasses 10 sessions of music listening in our laboratory. Frequency-modulation will involve stepwise filtering of frequencies in the audible range of 50-4,000 Hz. Acute pain will be induced via the cold pressor test. Primary (i.e., pain tolerance, perceived pain intensity) and secondary (i.e., heart rate variability, electrodermal activity, hair cortisol, subjective stress) outcomes will be measured at baseline, post, and follow-up. In addition, intermittent measurements as well as a follow-up assessment and a range of tertiary measures (e.g., music-induced emotions) are included. Discussion: This is the first study to systematically test and compare the effects of music frequencies along with the control over music selection, both of which qualify as central treatment characteristics of music-listening interventions. Results will be highly informative for the design of subsequent large-scale clinical trials and provide valuable conclusions for the implementation of music-listening interventions for the reduction of perceived pain. Clinical Trial Registration: Clinical Trials Database of the U.S. National Library of Medicine: Identifier NCT02991014.
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Affiliation(s)
- Anja C. Feneberg
- Clinical Psychology of Adulthood, Department of Clinical and Health Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
| | - Mattes B. Kappert
- Clinical Biopsychology, Department of Psychology, University of Marburg, Marburg, Germany
| | - Rosa M. Maidhof
- Clinical Psychology of Adulthood, Department of Clinical and Health Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
| | - Bettina K. Doering
- Division of Clinical and Biological Psychology, Department of Psychology, Catholic University Eichstätt-Ingolstadt, Eichstätt, Germany
| | - Dieter Olbrich
- Center for Psychosomatic Rehabilitation, Klinik Lipperland, Bad Salzuflen, Germany
| | - Urs M. Nater
- Clinical Psychology of Adulthood, Department of Clinical and Health Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
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24
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Posada-Quintero HF, Kong Y, Nguyen K, Tran C, Beardslee L, Chen L, Guo T, Cong X, Feng B, Chon KH. Using electrodermal activity to validate multilevel pain stimulation in healthy volunteers evoked by thermal grills. Am J Physiol Regul Integr Comp Physiol 2020; 319:R366-R375. [PMID: 32726157 PMCID: PMC7509251 DOI: 10.1152/ajpregu.00102.2020] [Citation(s) in RCA: 22] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2020] [Revised: 06/29/2020] [Accepted: 07/26/2020] [Indexed: 11/22/2022]
Abstract
We have tested the feasibility of thermal grills, a harmless method to induce pain. The thermal grills consist of interlaced tubes that are set at cool or warm temperatures, creating a painful "illusion" (no tissue injury is caused) in the brain when the cool and warm stimuli are presented collectively. Advancement in objective pain assessment research is limited because the gold standard, the self-reporting pain scale, is highly subjective and only works for alert and cooperative patients. However, the main difficulty for pain studies is the potential harm caused to participants. We have recruited 23 subjects in whom we induced electric pulses and thermal grill (TG) stimulation. The TG effectively induced three different levels of pain, as evidenced by the visual analog scale (VAS) provided by the subjects after each stimulus. Furthermore, objective physiological measurements based on electrodermal activity showed a significant increase in levels as stimulation level increased. We found that VAS was highly correlated with the TG stimulation level. The TG stimulation safely elicited pain levels up to 9 out of 10. The TG stimulation allows for extending studies of pain to ranges of pain in which other stimuli are harmful.
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Affiliation(s)
| | | | | | - Cara Tran
- University of Connecticut, Storrs, Connecticut
| | - Luke Beardslee
- Emory University School of Medicine Department of Surgery, Atlanta, Georgia
| | - Longtu Chen
- University of Connecticut, Storrs, Connecticut
| | | | | | - Bin Feng
- University of Connecticut, Storrs, Connecticut
| | - Ki H Chon
- University of Connecticut, Storrs, Connecticut
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25
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Abstract
Cognitive self-regulation can shape pain experience, but its effects on autonomic responses to painful events are unclear. In this study, participants (N = 41) deployed a cognitive strategy based on reappraisal and imagination to regulate pain up or down on different trials while skin conductance responses (SCRs) and electrocardiogram activity were recorded. Using a machine learning approach, we first developed stimulus-locked SCR and electrocardiogram physiological markers predictive of pain ratings. The physiological markers demonstrated high sensitivity and moderate specificity in predicting pain across 2 data sets, including an independent test data set (N = 84). When we tested the markers on the cognitive self-regulation data, we found that cognitive self-regulation had significant impacts on both pain ratings and pain-related physiology in accordance with regulatory goals. These findings suggest that self-regulation can impact autonomic nervous system responses to painful stimuli and provide pain-related autonomic profiles for future studies.
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26
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Scheuren PS, Rosner J, Curt A, Hubli M. Pain-autonomic interaction: A surrogate marker of central sensitization. Eur J Pain 2020; 24:2015-2026. [PMID: 32794307 DOI: 10.1002/ejp.1645] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2020] [Revised: 08/05/2020] [Accepted: 08/06/2020] [Indexed: 11/07/2022]
Abstract
BACKGROUND Central sensitization represents a key pathophysiological mechanism underlying the development of neuropathic pain, often manifested clinically as mechanical allodynia and hyperalgesia. Adopting a mechanism-based treatment approach relies highly on the ability to assess the presence of central sensitization. The aim of the study was to investigate potential pain-autonomic readouts to operationalize experimentally induced central sensitization in the area of secondary hyperalgesia. METHODS Pinprick evoked potentials (PEPs) and sympathetic skin responses (SSRs) were recorded in 20 healthy individuals. Three blocks of PEP and SSR recordings were performed before and after heat-induced secondary hyperalgesia. All measurements were also performed before and after a control condition. Multivariate analyses were performed using linear mixed-effect regression models to examine the effect of experimentally induced central sensitization on PEP and SSR parameters (i.e. amplitudes, latencies and habituation) and on pinprick pain ratings. RESULTS The noxious heat stimulation induced robust mechanical hyperalgesia with a significant increase in PEP and SSR amplitudes (p < 0.001) in the area of secondary hyperalgesia. Furthermore, PEP and SSR habituation were reduced (p < 0.001) after experimentally induced central sensitization. CONCLUSIONS The findings demonstrate that combined recordings of PEPs and SSRs are sensitive to objectify experimentally induced central sensitization and may have a great potential to reveal its presence in clinical pain conditions. Corroborating current pain phenotyping with pain-autonomic markers has the potential to unravel central sensitization along the nociceptive neuraxis and might provide a framework for mechanistically founded therapies. SIGNIFICANCE Our findings provide evidence that combined recordings of sympathetic skin responses (SSRs) and pinprick evoked potentials (PEPs) might be able to unmask central sensitization induced through a well-established experimental pain model in healthy individuals. As such, these novel readouts of central sensitization might attain new insights towards complementing clinical pain phenotyping.
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Affiliation(s)
- Paulina S Scheuren
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Jan Rosner
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.,Department of Neurology, University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
| | - Armin Curt
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
| | - Michèle Hubli
- Spinal Cord Injury Center, Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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27
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Frisch S, Werner P, Al-Hamadi A, Traue HC, Gruss S, Walter S. [From external assessment of pain to automated multimodal measurement of pain intensity : Narrative review of state of research and clinical perspectives]. Schmerz 2020; 34:376-387. [PMID: 32382799 DOI: 10.1007/s00482-020-00473-x] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Abstract
BACKGROUND In patients with limited communication skills, the use of conventional scales or external assessment is only possible to a limited extent or not at all. Multimodal pain recognition based on artificial intelligence (AI) algorithms could be a solution. OBJECTIVE Overview of the methods of automated multimodal pain measurement and their recognition rates that were calculated with AI algorithms. METHODS In April 2018, 101 studies on automated pain recognition were found in the Web of Science database to illustrate the current state of research. A selective literature review with special consideration of recognition rates of automated multimodal pain measurement yielded 14 studies, which are the focus of this review. RESULTS The variance in recognition rates was 52.9-55.0% (pain threshold) and 66.8-85.7%; in nine studies the recognition rate was ≥80% (pain tolerance), while one study reported recognition rates of 79.3% (pain threshold) and 90.9% (pain tolerance). CONCLUSION Pain is generally recorded multimodally, based on external observation scales. With regard to automated pain recognition and on the basis of the 14 selected studies, there is to date no conclusive evidence that multimodal automated pain recognition is superior to unimodal pain recognition. In the clinical context, multimodal pain recognition could be advantageous, because this approach is more flexible. In the case of one modality not being available, e.g., electrodermal activity in hand burns, the algorithm could use other modalities (video) and thus compensate for missing information.
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Affiliation(s)
- S Frisch
- Sektion Medizinische Psychologie, Klinik für Psychosomatische Medizin und Psychotherapie, Universitätsklinikum Ulm, Frauensteige 6, 89075, Ulm, Deutschland
- Praxis für Neurologie und Psychiatrie Leutkirch, Leutkirch, Deutschland
| | - P Werner
- Neuro-Informationstechnik, Institut für Informations- und Kommunikationstechnik, Otto-von-Guericke-Universität Magdeburg, Magdeburg, Deutschland
| | - A Al-Hamadi
- Neuro-Informationstechnik, Institut für Informations- und Kommunikationstechnik, Otto-von-Guericke-Universität Magdeburg, Magdeburg, Deutschland
| | - H C Traue
- Sektion Medizinische Psychologie, Klinik für Psychosomatische Medizin und Psychotherapie, Universitätsklinikum Ulm, Frauensteige 6, 89075, Ulm, Deutschland
| | - S Gruss
- Sektion Medizinische Psychologie, Klinik für Psychosomatische Medizin und Psychotherapie, Universitätsklinikum Ulm, Frauensteige 6, 89075, Ulm, Deutschland
| | - S Walter
- Sektion Medizinische Psychologie, Klinik für Psychosomatische Medizin und Psychotherapie, Universitätsklinikum Ulm, Frauensteige 6, 89075, Ulm, Deutschland.
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28
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Acute Posttrauma Resting-State Functional Connectivity of Periaqueductal Gray Prospectively Predicts Posttraumatic Stress Disorder Symptoms. BIOLOGICAL PSYCHIATRY: COGNITIVE NEUROSCIENCE AND NEUROIMAGING 2020; 5:891-900. [PMID: 32389746 DOI: 10.1016/j.bpsc.2020.03.004] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/20/2019] [Revised: 03/04/2020] [Accepted: 03/08/2020] [Indexed: 12/30/2022]
Abstract
BACKGROUND Posttraumatic stress disorder (PTSD) is characterized by hyperarousal, avoidance, and intrusive/re-experiencing symptoms. The periaqueductal gray (PAG), which generates behavioral responses to physical and psychological stressors, is also implicated in threat processing. Distinct regions of the PAG elicit opposing responses to threatening or stressful stimuli; the ventrolateral PAG evokes passive coping strategies (e.g., analgesia), whereas the dorsolateral PAG (dlPAG) promotes active responses (e.g., fight or flight). We investigated whether altered PAG resting-state functional connectivity (RSFC) prospectively predicted PTSD symptoms. METHODS A total of 48 trauma-exposed individuals underwent an RSFC scan 2 weeks posttraumatic injury. Self-report measures, including the visual analog scale for pain and the Impact of Event Scale, were collected at 2 weeks and 6 months posttrauma. We analyzed whether acute bilateral PAG RSFC was a marker of risk for total 6-month symptom severity and specific symptom clusters. In an exploratory analysis, we investigated whether dlPAG RSFC predicted PTSD symptoms. RESULTS After adjusting for physical pain ratings, greater acute posttrauma PAG-frontal pole and PAG-posterior cingulate cortex connectivity was positively associated with 6-month total PTSD symptoms. Weaker dlPAG-superior/inferior parietal lobule connectivity predicted both higher hyperarousal and higher intrusive symptoms, while weaker dlPAG-supramarginal gyrus RSFC was associated with only hyperarousal symptoms. CONCLUSIONS Altered connectivity of the PAG 2 weeks posttrauma prospectively predicted PTSD symptoms. These findings suggest that aberrant PAG function may serve as a marker of risk for chronic PTSD symptoms, possibly by driving specific symptom clusters, and more broadly that connectivity of specific brain regions may underlie specific symptom profiles.
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Hohenschurz-Schmidt DJ, Calcagnini G, Dipasquale O, Jackson JB, Medina S, O'Daly O, O'Muircheartaigh J, de Lara Rubio A, Williams SCR, McMahon SB, Makovac E, Howard MA. Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks. Front Neurosci 2020; 14:147. [PMID: 33041747 PMCID: PMC7527240 DOI: 10.3389/fnins.2020.00147] [Citation(s) in RCA: 40] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/22/2019] [Accepted: 02/06/2020] [Indexed: 12/27/2022] Open
Abstract
There are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain areas of the central autonomic network and areas involved in pain processing and modulation. To date, however, relatively little is known about the neuronal substrates of the ANS-pain association. Here, we acquired resting state fMRI scans in 21 healthy subjects at rest and during tonic noxious cold stimulation. As indicators of autonomic function, we examined how heart rate variability (HRV) frequency measures were influenced by tonic noxious stimulation and how these variables related to participants’ pain perception and to brain functional connectivity in regions known to play a role in both ANS regulation and pain perception, namely the right dorsal anterior cingulate cortex (dACC) and periaqueductal gray (PAG). Our findings support a role of the cardiac ANS in brain connectivity during pain, linking functional connections of the dACC and PAG with measurements of low frequency (LF)-HRV. In particular, we identified a three-way relationship between the ANS, cortical brain networks known to underpin pain processing, and participants’ subjectively reported pain experiences. LF-HRV both at rest and during pain correlated with functional connectivity between the seed regions and other cortical areas including the right dorsolateral prefrontal cortex (dlPFC), left anterior insula (AI), and the precuneus. Our findings link cardiovascular autonomic parameters to brain activity changes involved in the elaboration of nociceptive information, thus beginning to elucidate underlying brain mechanisms associated with the reciprocal relationship between autonomic and pain-related systems.
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Affiliation(s)
- David Johannes Hohenschurz-Schmidt
- Department of Neuroimaging, King's College London, London, United Kingdom.,Department of Surgery and Cancer, Imperial College London, London, United Kingdom
| | - Giovanni Calcagnini
- Department of Technology and Health, Italian National Institute of Health, Rome, Italy
| | - Ottavia Dipasquale
- Department of Neuroimaging, King's College London, London, United Kingdom
| | - Jade B Jackson
- Department of Neuroimaging, King's College London, London, United Kingdom.,Wolfson Centre for Age Related Diseases, King's College London, London, United Kingdom
| | - Sonia Medina
- Department of Neuroimaging, King's College London, London, United Kingdom.,Wolfson Centre for Age Related Diseases, King's College London, London, United Kingdom
| | - Owen O'Daly
- Department of Neuroimaging, King's College London, London, United Kingdom
| | - Jonathan O'Muircheartaigh
- Department of Neuroimaging, King's College London, London, United Kingdom.,Sackler Institute for Translational Neurodevelopment, King's College London, London, United Kingdom.,Centre for the Developing Brain, King's College London, London, United Kingdom.,MRC Centre for Neurodevelopmental Disorders, King's College London, London, United Kingdom
| | | | | | - Stephen B McMahon
- Department of Technology and Health, Italian National Institute of Health, Rome, Italy
| | - Elena Makovac
- Department of Neuroimaging, King's College London, London, United Kingdom.,Department of Technology and Health, Italian National Institute of Health, Rome, Italy
| | - Matthew A Howard
- Department of Neuroimaging, King's College London, London, United Kingdom
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30
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Picchiottino M, Honoré M, Leboeuf-Yde C, Gagey O, Cottin F, Hallman DM. The effect of a single spinal manipulation on cardiovascular autonomic activity and the relationship to pressure pain threshold: a randomized, cross-over, sham-controlled trial. Chiropr Man Therap 2020; 28:7. [PMID: 31988711 PMCID: PMC6971986 DOI: 10.1186/s12998-019-0293-4] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2019] [Accepted: 12/23/2019] [Indexed: 02/06/2023] Open
Abstract
Background The autonomic nervous system interacts with the pain system. Knowledge on the effects of high velocity low amplitude spinal manipulations (SM) on autonomic activity and experimentally induced pain is limited. In particular, the effects of SM on autonomic activity and pain beyond the immediate post intervention period as well as the relationship between these two outcomes are understudied. Thus, new research is needed to provide further insight on this issue. Objectives The aim was to assess the effect of a single SM (i.e. SM vs. sham) on cardiovascular autonomic activity. Also, we assessed the relationship between cardiovascular autonomic activity and level of pain threshold after the interventions. Method We conducted a randomized, cross-over, sham-controlled trial on healthy first-year chiropractic students comprising two experimental sessions separated by 48 h. During each session, subjects received, in a random order, either a thoracic SM or a sham manipulation. Cardiovascular autonomic activity was assessed using heart rate and systolic blood pressure variabilities. Pain sensitivity was assessed using pressure pain threshold. Measurements were performed at baseline and repeated three times (every 12 min) during the post intervention period. Participants and outcome assessors were blinded. The effect of the SM was tested with linear mixed models. The relationship between autonomic outcomes and pressure pain threshold was tested with bivariate correlations. Results Fifty-one participants were included, forty-one were finally analyzed. We found no statistically significant difference between SM and sham in cardiovascular autonomic activity post intervention. Similarly, we found no post-intervention relationship between cardiovascular autonomic activity and pressure pain threshold. Conclusion Our results suggest that a single SM of the thoracic spine has no specific effect on cardiovascular autonomic activity. Also, we found no relationship between cardiovascular autonomic activity and pressure pain threshold after the SM. Further experimental research should consider the use of several markers of autonomic activity and a more comprehensive pain assessment. Trial registration N° NCT03273868. Registered September 6, 2017.
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Affiliation(s)
- Mathieu Picchiottino
- Université Paris-Saclay CIAMS, 91405 Orsay, France
- CIAMS, Université d’Orléans, 45067 Orléans, France
- Institut Franco-européen de Chiropraxie (IFEC), Ivry-sur-Seine, Toulouse, France
| | - Margaux Honoré
- Université Paris-Saclay CIAMS, 91405 Orsay, France
- CIAMS, Université d’Orléans, 45067 Orléans, France
- Institut Franco-européen de Chiropraxie (IFEC), Ivry-sur-Seine, Toulouse, France
| | - Charlotte Leboeuf-Yde
- Université Paris-Saclay CIAMS, 91405 Orsay, France
- CIAMS, Université d’Orléans, 45067 Orléans, France
- Institut Franco-européen de Chiropraxie (IFEC), Ivry-sur-Seine, Toulouse, France
- Institute for Regional Health Research, University of Southern Denmark, Odense, Denmark
| | - Olivier Gagey
- Université Paris-Saclay CIAMS, 91405 Orsay, France
- CIAMS, Université d’Orléans, 45067 Orléans, France
| | - François Cottin
- Université Paris-Saclay CIAMS, 91405 Orsay, France
- CIAMS, Université d’Orléans, 45067 Orléans, France
| | - David M. Hallman
- Centre for Musculoskeletal Research, Department of Occupational and Public Health Sciences, University of Gävle, Gävle, Sweden
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31
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Lyubashina OA, Mamontov OV, Volynsky MA, Zaytsev VV, Kamshilin AA. Contactless Assessment of Cerebral Autoregulation by Photoplethysmographic Imaging at Green Illumination. Front Neurosci 2019; 13:1235. [PMID: 31798408 PMCID: PMC6863769 DOI: 10.3389/fnins.2019.01235] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/17/2019] [Accepted: 10/31/2019] [Indexed: 12/15/2022] Open
Abstract
Accurate and practical assessment of the brain circulation is needed to adequately estimate the viability of cerebral blood flow regulatory mechanisms in various physiological conditions. The objective of our study was to examine feasibility of the contactless green-light imaging photoplethysmography (PPG) for assessing cerebral autoregulation by revealing the dynamic relationships between cortical microcirculation assessed by PPG and changes in systemic blood pressure caused by visceral and somatic peripheral stimuli. In anesthetized male Wistar rats, the PPG video images of the open parietal cortex (either with unimpaired or dissected dura mater), electrocardiogram, and systemic arterial blood pressure (ABP) in the femoral artery were continuously recorded before, during and after visceral (colorectal distension) or somatic (tail squeezing) stimulation. In the vast majority of experiments with intact and removed dura mater, both spontaneous and peripheral stimulation-evoked changes in ABP negatively correlated with the accompanying alterations in the amplitude of pulsatile PPG component (APC), i.e., an increase of ABP resulted in a decrease of APC and vice versa. The most pronounced ABP and APC alterations were induced by noxious stimuli. Visceral painful stimulation in all cases caused short-term hypotension with simultaneous increase in cortical APC, whereas somatic noxious stimuli in 8 of 21 trials produced hypertensive effect with decreased APC. Animals with pressure 50-70 mmHg possessed higher negative cerebrovascular response rate of ABP-APC gradients than rats with either lower or higher pressure. Severe hypotension reversed the negative ratio to positive one, which was especially evident under visceral pain stimulation. Amplitude of the pulsatile PPG component probably reflects the regulation of vascular tone of cerebral cortex in response to systemic blood pressure fluctuations. When combined with different kinds of peripheral stimuli, the technique is capable for evaluation of normal and elucidation of impaired cerebrovascular system reactivity to particular physiological events, for example pain. The reported contactless PPG monitoring of cortical circulatory dynamics during neurosurgical interventions in combination with recordings of changes in other physiological parameters, such as systemic blood pressure and ECG, has the appealing potential to monitor viability of the cortex vessels and determine the state of patient's cerebrovascular autoregulation.
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Affiliation(s)
- Olga A. Lyubashina
- Laboratory of Cortico-Visceral Physiology, Pavlov Institute of Physiology, Russian Academy of Sciences, Saint Petersburg, Russia
- Valdman Institute of Pharmacology, Pavlov First Saint Petersburg State Medical University, Saint Petersburg, Russia
| | - Oleg V. Mamontov
- Department of Circulation Physiology, Almazov National Medical Research Centre, Saint Petersburg, Russia
- Faculty of Applied Optics, ITMO University, Saint Petersburg, Russia
| | - Maxim A. Volynsky
- Faculty of Applied Optics, ITMO University, Saint Petersburg, Russia
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Lopez-Martinez D, Picard R. Continuous Pain Intensity Estimation from Autonomic Signals with Recurrent Neural Networks. ANNUAL INTERNATIONAL CONFERENCE OF THE IEEE ENGINEERING IN MEDICINE AND BIOLOGY SOCIETY. IEEE ENGINEERING IN MEDICINE AND BIOLOGY SOCIETY. ANNUAL INTERNATIONAL CONFERENCE 2019; 2018:5624-5627. [PMID: 30441611 DOI: 10.1109/embc.2018.8513575] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/09/2022]
Abstract
Pain is usually measured by patient's self-report, which requires patient collaboration. Hence, the development of an objective automatic pain detection method would be useful in many clinical applications and patient populations. Previous studies have explored the feasibility of using physiological autonomic signals to detect the presence of pain. In this study, we focused on continuously estimating experimental heat pain intensity with high temporal resolution from autonomic signals. Specifically, we employed skin conductance deconvolution and point process heart rate variability analysis to continuously evaluate time-varying autonomic parameters, and presented a regression algorithm based on recurrent neural networks.
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33
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Differential responses of neurons in the rat caudal ventrolateral medulla to visceral and somatic noxious stimuli and their alterations in colitis. Brain Res Bull 2019; 152:299-310. [PMID: 31377442 DOI: 10.1016/j.brainresbull.2019.07.030] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/29/2019] [Revised: 07/15/2019] [Accepted: 07/30/2019] [Indexed: 02/06/2023]
Abstract
Visceral and somatic types of pain have been reported to manifest crucial differences not only in the experience, but also in their peripheral and central processing. However, the precise neuronal mechanisms that responsible for the modality-specific transmission of pain signals, especially at the supraspinal level, remain unclear. Very little is known also about the potential involvement of such mechanisms in the development of viscero-somatic hyperalgesia. Therefore, in the present study performed on urethane-anesthetized adult male Wistar rats we examined responses of neurons in the caudal ventrolateral medulla (CVLM)-the first site for supraspinal processing of both internal and external pain signals-to visceral (colorectal distension, CRD) and somatic (squeezing of the tail) noxious stimulations and evaluated alterations in response properties of these cells after the induction of colitis. It has been found out that the CVLM of healthy control rats, along with harboring of cells excited by both stimulations (23.7%), contained neurons that were activated by either visceral (31.9%) or somatic noxious stimuli (44.4%). In inflamed animals, the percentages of the visceral and somatic nociceptive cells were decreased (to 18.3% and 34.3%, correspondingly) and the number of bimodal neurons was increased (up to 47.4%); these alterations were associated with substantially enhanced responses of both the modality-specific and convergent CVLM neurons not only to CRD, but also to squeezing of the tail. Under these conditions, visceral and somatic pain stimuli induced similar changes in arterial blood pressure and respiratory rate, whereas in the absence of intestinal inflammation noxious CRD and tail stimulation evoked predominantly divergent autonomic reactions. The data obtained can benefit to a deeper understanding of the neuronal mechanisms that underlie differential supraspinal processing of visceral and somatic noxious stimuli and can potentially contribute to the realization of specific cardiovascular and respiratory accompaniments inherent to a particular type of pain. Therewith, results of the study elucidate colitis-induced alterations in these mechanisms, which may be responsible for the combined development of visceral hypersensitivity and somatic hyperalgesia.
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34
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Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses - corrected and republished. Pain 2019; 160:1469-1481. [PMID: 31107415 DOI: 10.1097/j.pain.0000000000001573] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/25/2022]
Abstract
Nociception reliably elicits an autonomic nervous system (ANS) response. Because pain and ANS circuitry interact on multiple spinal, subcortical, and cortical levels, it remains unclear whether autonomic responses are simply a reflexive product of noxious stimulation regardless of how stimulation is consciously perceived or whether the experience of pain mediates ANS responses to noxious stimulation. To test these alternative predictions, we examined the relative contribution of noxious stimulation and individual pain experience to ANS responses in healthy volunteers who underwent 1 or 2 pain assessment tasks. Participants received 8 seconds of thermal stimulation of varied temperatures and judged pain intensity on every trial. Skin conductance responses and pupil dilation responses to stimulation served as measures of the heat-evoked autonomic response. We used multilevel modelling to examine trial-by-trial relationships between heat, pain, and ANS response. Although both pain and noxious heat stimulation predicted skin conductance response and pupil dilation response in separate analyses, the individual pain experience statistically mediated effects of noxious heat on both outcomes. Furthermore, moderated mediation revealed that evidence for this process was stronger when stimulation was perceived as painful compared with when stimulation was perceived as nonpainful, although this difference emerged late, in the 4-second period after thermal stimulation. These findings suggest that pain appraisal regulates the heat-evoked autonomic response to noxious stimulation, documenting the flexibility of the autonomic pain response to adjust to perceived or actual changes in environmental affordances above and beyond nociceptive input.
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Kano M, Yoshizawa M, Kono K, Muratsubaki T, Morishita J, Van Oudenhove L, Yagihashi M, Mugikura S, Dupont P, Takase K, Kanazawa M, Fukudo S. Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome. Sci Rep 2019; 9:7358. [PMID: 31089154 PMCID: PMC6517375 DOI: 10.1038/s41598-019-43455-5] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2018] [Accepted: 04/18/2019] [Indexed: 12/15/2022] Open
Abstract
The nociceptive and autonomic nervous systems (ANS) are significantly intertwined. Decoupling of these systems may occur in pathological pain conditions, including irritable bowel syndrome (IBS). We investigated ANS activity and its association with visceral perception and brain activity during rectal distention in 27 patients with non-constipated IBS and 33 controls by assessing heart rate variability (HRV) using electrocardiography at rest, before, and during colorectal distention. Brain responses to colorectal distention were measured using functional magnetic resonance imaging and correlated with individual ANS function parameters. The IBS group displayed blunted sympathovagal balance [low/high-frequency ratio (LF:HF) of HRV] in response to colorectal distention compared with controls (P = 0.003). In controls, basal parasympathetic tone (HF component of HRV) was significantly negatively correlated with toleration threshold to the rectal distention, but not in patients with IBS (group comparison P = 0.04). Further, a positive correlation between baseline HF values and neural responses to rectal distension was found in the right caudate, bilateral dorsolateral anterior cingulate cortex, and pregenual anterior cingulate cortex in the control group but not in the IBS group. The results indicate abnormal interactions between ANS activity and the brain mechanisms underlying visceral perception in patients with IBS.
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Affiliation(s)
- Michiko Kano
- Sukawa Clinic, Kirari Health Coop, Fukushima, Japan.
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan.
| | - Makoto Yoshizawa
- Research Division on Advanced Information Technology, Cyberscience Center, Tohoku University, Sendai, Japan
| | - Keiji Kono
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan
| | - Tomohiko Muratsubaki
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan
| | - Joe Morishita
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan
| | - Lukas Van Oudenhove
- Laboratory for Brain-Gut Axis Studies (LaBGAS), Translational Research Center for Gastrointestinal Disorders (TARGID), KU Leuven, Leuven, Belgium
| | - Mao Yagihashi
- Dept. Biodesign, Clinical Research, Innovation and Education Center (CRIETO), Tohoku University Hospital, Sendai, Japan
| | - Shunji Mugikura
- Diagnostic Radiology, Tohoku University Hospital, Sendai, Japan
| | - Patrick Dupont
- Laboratory for Cognitive Neurology, KU Leuven, Leuven, Belgium
| | - Kei Takase
- Diagnostic Radiology, Tohoku University Hospital, Sendai, Japan
| | - Motoyori Kanazawa
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan
| | - Shin Fukudo
- Behavioral Medicine, Graduate School of Medicine, Tohoku University, Sendai, Japan
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Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses. Pain 2019; 159:699-711. [PMID: 29251663 DOI: 10.1097/j.pain.0000000000001132] [Citation(s) in RCA: 38] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/05/2023]
Abstract
Nociception reliably elicits an autonomic nervous system (ANS) response. Because pain and ANS circuitry interact on multiple spinal, subcortical, and cortical levels, it remains unclear whether autonomic responses are simply a reflexive product of noxious stimulation regardless of how stimulation is consciously perceived or whether the experience of pain mediates ANS responses to noxious stimulation. To test these alternative predictions, we examined the relative contribution of noxious stimulation and individual pain experience to ANS responses in healthy volunteers who underwent 1 or 2 pain assessment tasks. Participants received 8 seconds of thermal stimulation of varied temperatures and judged pain intensity on every trial. Skin conductance responses and pupil dilation responses to stimulation served as measures of the heat-evoked autonomic response. We used multilevel modelling to examine trial-by-trial relationships between heat, pain, and ANS response. Although both pain and noxious heat stimulation predicted skin conductance response and pupil dilation response in separate analyses, the individual pain experience statistically mediated effects of noxious heat on both outcomes. Furthermore, moderated mediation revealed that evidence for this process was stronger when stimulation was perceived as painful compared with when stimulation was perceived as nonpainful. These findings suggest that pain appraisal regulates the heat-evoked autonomic response to noxious stimulation, documenting the flexibility of the autonomic pain response to adjust to perceived or actual changes in environmental affordances above and beyond nociceptive input.
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Picchiottino M, Leboeuf-Yde C, Gagey O, Hallman DM. The acute effects of joint manipulative techniques on markers of autonomic nervous system activity: a systematic review and meta-analysis of randomized sham-controlled trials. Chiropr Man Therap 2019; 27:17. [PMID: 30911373 PMCID: PMC6413458 DOI: 10.1186/s12998-019-0235-1] [Citation(s) in RCA: 25] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2018] [Accepted: 01/16/2019] [Indexed: 12/19/2022] Open
Abstract
Background The autonomic nervous system (ANS) interests many chiropractors and manual therapists, because joint manipulative techniques (JMT), e.g. high velocity low amplitude (HVLA) manipulations and mobilizations, appear to produce acute changes in ANS mediated physiology. The complexity of this issue justifies a systematic critical literature review. Objective To review the literature comparing the acute changes in markers of ANS activity between JMT applied on spinal or peripheral joints and a sham procedure in healthy or symptomatic subjects. Method We searched PsycINFO, PEDro, PubMed, Cochrane library, EMBASE, and Medline up to December 2017. We updated the search with PubMed, Cochrane library, EMBASE, and Medline including July 2018. Inclusion criteria were: randomized sham-controlled trials assessing the effect of JMT on markers of ANS activity; manually applied JMT, regardless of technique, applied on either healthy or symptomatic humans; outcome measurements recorded at baseline and repeated during and/or after interventions. Selection of articles and data extraction were performed independently by two reviewers. The quality of studies was assessed using the Cochrane ‘risk of bias’ tool and a technical check-list. Results were reported narratively with some meta-analyses. The Cochrane GRADE approach was used to assess the certainty of evidence. Results Twenty-nine of 2267 studies were included in the synthesis. Mobilizations (oscillatory technique) probably produce an immediate and short-term, bilateral increase in skin sympathetic nerve activity (reflected by an increase in skin conductance) regardless of the area treated (moderate-certainty evidence). It is uncertain whether the sympathetic arousal also explains an increase in respiratory rate (very low-certainty evidence). Our evaluation of the literature suggests that spinal sustained apophyseal glides (SNAGs) mobilization and HVLA manipulation of the spine may have no acute effect on the studied markers of ANS activity (very low- to low-certainty evidence). Conclusion Some types of mobilizations probably produce an immediate and short-term, statistically significant increase in skin sympathetic nerve activity when compared to a sham procedure, whereas spinal SNAGs and spinal HVLA techniques may have no acute effect on the studied markers of ANS activity. No region-specific results were noted. The literature suffers from several shortcomings, for which reason we strongly suggest further research. Electronic supplementary material The online version of this article (10.1186/s12998-019-0235-1) contains supplementary material, which is available to authorized users.
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Affiliation(s)
- Mathieu Picchiottino
- 1CIAMS, Université Paris-Sud, Université Paris-Saclay, Orsay Cedex, France.,2CIAMS, Université d'Orléans, Orléans, France.,Institut Franco-européen de Chiropraxie (IFEC), Ivry-sur-Seine, France
| | - Charlotte Leboeuf-Yde
- 1CIAMS, Université Paris-Sud, Université Paris-Saclay, Orsay Cedex, France.,2CIAMS, Université d'Orléans, Orléans, France.,Institut Franco-européen de Chiropraxie (IFEC), Ivry-sur-Seine, France.,4Institute for Regional Health Research, University of Southern Denmark, Odense, Denmark
| | - Olivier Gagey
- 1CIAMS, Université Paris-Sud, Université Paris-Saclay, Orsay Cedex, France.,2CIAMS, Université d'Orléans, Orléans, France
| | - David M Hallman
- 5Centre for Musculoskeletal Research, Department of Occupational and Public Health Sciences, University of Gävle, Gävle, Sweden
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Boedts MJO. The pharyngeal recess/Eustachian tube complex forms an acoustic passageway. Med Hypotheses 2018; 121:112-122. [PMID: 30396462 DOI: 10.1016/j.mehy.2018.09.032] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/01/2018] [Revised: 08/10/2018] [Accepted: 09/16/2018] [Indexed: 10/28/2022]
Abstract
We propose that the complex formed by the Pharyngeal Recess and Eustachian Tube, acts as an acoustic passageway for sounds originating inside the body: sounds made by one's voice, breathing, mastication, one's heartbeats. The antagonistic effect of two sets of muscles, one innervated by the trigeminal nerve, the other by the vagal nerve and cervical plexus, enables the body to modulate transmission of sound via this passageway and hence modulate the awareness of body sounds. Impairment of this system can be due to local factors, such as adhesions over the pharyngeal recess or inflammation inside the pharyngeal recess and/or Eustachian tube; or to tensions of the muscles involved, related to other causes. Dysfunction of the system can lead to symptoms related to increased or decreased awareness of body sounds, such as autophony, hearing of pulsating sounds and clicks in the ear; sensory symptoms related to increased activation of the nerves such as fullness feeling in the ear, facial pain, burning mouth syndrome, globus pharyngeus, pharyngeal pain; and symptoms related to inappropriate muscular contraction such as masticatory and cervical muscle tensions, bruxism, and tension type headache. The functioning of this acoustic passageway is related to the concept of the Trigeminocervical complex. The concept of Vagocervical complex is proposed.
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Affiliation(s)
- M J O Boedts
- Brai3n Neuromodulation Centre, Jemappesstraat 5, 9000 Gent, Belgium; AZ Maria Middelares, Buitenring 30, 9000 Gent, Belgium.
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Tracy LM, Koenig J, Georgiou-Karistianis N, Gibson SJ, Giummarra MJ. Heart rate variability is associated with thermal heat pain threshold in males, but not females. Int J Psychophysiol 2018; 131:37-43. [DOI: 10.1016/j.ijpsycho.2018.02.017] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2018] [Revised: 02/27/2018] [Accepted: 02/27/2018] [Indexed: 12/16/2022]
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Colitis-induced alterations in response properties of visceral nociceptive neurons in the rat caudal medulla oblongata and their modulation by 5-HT3 receptor blockade. Brain Res Bull 2018; 142:183-196. [PMID: 30031817 DOI: 10.1016/j.brainresbull.2018.07.013] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/05/2018] [Revised: 06/15/2018] [Accepted: 07/17/2018] [Indexed: 12/17/2022]
Abstract
There is considerable clinical and experimental evidence that intestinal inflammation is associated with altered visceral nociceptive processing in the spinal cord and brain, but the underlying neuronal mechanisms, especially acting at the supraspinal level, remain unclear. Considering that the caudal ventrolateral medulla (CVLM) and the nucleus tractus solitarius (NTS) are the first sites for supraspinal processing of visceral pain signals, in the present study we evaluated the experimental colitis-induced changes in response properties of CVLM and NTS medullary neurons to noxious colorectal distension (CRD) in urethane-anesthetized adult male Wistar rats. To determine if gut inflammation alters the 5-HT3 receptor-dependent modulation of visceral pain-related CVLM and NTS cells, we examined the effects of intravenously administered selective 5-HT3 antagonist granisetron on ongoing and CRD-evoked activity of CVLM and NTS neurons in healthy control and colitic animals. In the absence of colonic pathology, the CVLM neurons were more excited by noxious CRD that the NTS cells, which demonstrated a greater tendency to be inhibited by the stimulation. The difference was eliminated after the development of colitis due to the increase in the proportion of CRD-excited neurons in both medullary regions associated with enhanced magnitude of the neuronal nociceptive responses. Intravenous granisetron (1 or 2 mg/kg) produced the dose-dependent suppression of the ongoing and evoked firing of CRD-excited cells within both the CVLM and NTS in normal conditions as well as was able to substantially reduce excitability of the caudal medullary neurons in the presence of colonic inflammation, arguing for the potential efficacy of the 5-HT3 receptor blockade with granisetron against both acute and inflammatory abdominal pain. Taken together, the data obtained can contribute to a deeper understanding of supraspinal serotonergic mechanisms responsible for the persistence of visceral hypersensitivity and hyperalgesia triggered by colonic inflammation.
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Solcà M, Ronchi R, Bello-Ruiz J, Schmidlin T, Herbelin B, Luthi F, Konzelmann M, Beaulieu JY, Delaquaize F, Schnider A, Guggisberg AG, Serino A, Blanke O. Heartbeat-enhanced immersive virtual reality to treat complex regional pain syndrome. Neurology 2018; 91:e479-e489. [DOI: 10.1212/wnl.0000000000005905] [Citation(s) in RCA: 47] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2017] [Accepted: 04/24/2018] [Indexed: 11/15/2022] Open
Abstract
ObjectivesTo develop and test a new immersive digital technology for complex regional pain syndrome (CRPS) that combines principles from mirror therapy and immersive virtual reality and the latest research from multisensory body processing.MethodsIn this crossover double-blind study, 24 patients with CRPS and 24 age- and sex-matched healthy controls were immersed in a virtual environment and shown a virtual depiction of their affected limb that was flashing in synchrony (or in asynchrony in the control condition) with their own online detected heartbeat (heartbeat-enhanced virtual reality [HEVR]). The primary outcome measures for pain reduction were subjective pain ratings, force strength, and heart rate variability (HRV).ResultsHEVR reduced pain ratings, improved motor limb function, and modulated a physiologic pain marker (HRV). These significant improvements were reliable and highly selective, absent in control HEVR conditions, not observed in healthy controls, and obtained without the application of tactile stimulation (or movement) of the painful limb, using a readily available biological signal (the heartbeat) that is most often not consciously perceived (thus preventing placebo effects).ConclusionsNext to these specific and well-controlled analgesic effects, immersive HEVR allows the application of prolonged and repeated doses of digital therapy, enables the automatized integration with existing pain treatments, and avoids application of painful bodily cues while minimizing the active involvement of the patient and therapist.Classification of evidenceThis study provides Class III evidence that HEVR reduces pain and increases force strength in patients with CRPS.
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Pain processing in the human brainstem and spinal cord before, during, and after the application of noxious heat stimuli. Pain 2018; 159:2012-2020. [DOI: 10.1097/j.pain.0000000000001302] [Citation(s) in RCA: 22] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/04/2023]
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Intranasal oxytocin reduces heart rate variability during a mental arithmetic task: A randomised, double-blind, placebo-controlled cross-over study. Prog Neuropsychopharmacol Biol Psychiatry 2018; 81:408-415. [PMID: 28844717 DOI: 10.1016/j.pnpbp.2017.08.016] [Citation(s) in RCA: 18] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/28/2017] [Revised: 08/08/2017] [Accepted: 08/19/2017] [Indexed: 12/17/2022]
Abstract
Heart rate variability (HRV) refers to variation in the interval between successive heart beats. Low HRV is an indicator of potential autonomic nervous system dysfunction. People with chronic pain often display autonomic dysregulation, especially in the parasympathetic nervous system. The hormone oxytocin has been shown to increase HRV in non-clinical samples, but its potential impact on HRV in persons with chronic pain is unknown. This study investigated the impact of intranasal oxytocin on HRV in persons with chronic neck and shoulder pain. Participants included 24 individuals with chronic neck and shoulder pain lasting >12months and 24 age- and sex-matched pain-free controls. In a randomised double-blind, placebo-controlled, cross-over study, participants self-administered intranasal oxytocin (24IU) in one session, and placebo in another, before HRV was recorded at rest and during a mental arithmetic task. Intranasal oxytocin did not influence HRV at rest. However, compared to placebo, intranasal oxytocin elicited small decreases in low-frequency and high-frequency HRV in both groups during the mental arithmetic task. These results suggest that intranasal oxytocin may enhance the salience of the mental arithmetic task, leading to reduced engagement of the parasympathetic nervous system when completing the task. Further investigation and replication of these findings are required to improve our understanding of the effects of intranasal oxytocin on autonomic functioning both at rest and under cognitive stress.
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Tracy LM, Jarczok MN, Ellis RJ, Bach C, Hillecke TK, Thayer JF, Koenig J. Heart Rate Variability and Sensitivity to Experimentally Induced Pain: A Replication. Pain Pract 2017; 18:687-689. [DOI: 10.1111/papr.12652] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/02/2023]
Affiliation(s)
- Lincoln M. Tracy
- School of Psychological Sciences and Monash Institute of Cognitive and Clinical Neurosciences; Monash University; Melbourne Victoria Australia
- Pain Management & Research Centre; Caulfield Hospital; Caulfield Victoria Australia
| | - Marc N. Jarczok
- Clinic for Psychosomatic Medicine and Psychotherapy; University Hospital Ulm; Ulm
- Institute of Medical Psychology; Center for Psychosocial Medicine; Heidelberg University; Heidelberg Germany
| | - Robert J. Ellis
- School of Computing; National University of Singapore; Singapore Singapore
| | - Claudia Bach
- Department of General Psychiatry; University of Heidelberg; Heidelberg Germany
| | - Thomas K. Hillecke
- School of Therapeutic Sciences; SRH University of Applied Sciences; Heidelberg Germany
| | - Julian F. Thayer
- Department of Psychology; The Ohio State University; Columbus Ohio U.S.A
| | - Julian Koenig
- Department of Psychology; The Ohio State University; Columbus Ohio U.S.A
- Section for Translation Psychobiology in Child and Adolescent Psychiatry; Department of Child and Adolescent Psychiatry; Centre for Psychosocial Medicine; University of Heidelberg; Heidelberg Germany
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45
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Pain-autonomic relationships: implications for experimental design and the search for an “objective marker” for pain. Pain 2017; 158:2064-2065. [DOI: 10.1097/j.pain.0000000000001035] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/08/2023]
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Chien JH, Colloca L, Korzeniewska A, Cheng JJ, Campbell CM, Hillis AE, Lenz FA. Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy. Neuroscience 2017; 346:81-93. [PMID: 28077278 PMCID: PMC5426483 DOI: 10.1016/j.neuroscience.2016.12.047] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2016] [Revised: 12/24/2016] [Accepted: 12/27/2016] [Indexed: 12/28/2022]
Abstract
Imaging studies have described hemodynamic activity during fear conditioning protocols with stimulus trains in which a visual conditioned stimulus (CS+) is paired with an aversive unconditioned stimulus (US, painful laser pulse) while another visual stimulus is unpaired (CS-). We now test the hypothesis that CS Event Related Spectral Perturbations (ERSPs) are related to ratings of CS Expectancy (likelihood of pairing with the US), Valence (unpleasantness) and Salience (ability to capture attention). ERSP windows in EEG were defined by both time after the CS and frequency, and showed increased oscillatory power (Event Related Synchronization, ERS) in the Delta/Theta Windows (0-8Hz) and the Gamma Window (30-55Hz). Decreased oscillatory power (Event Related Desynchronization - ERD) was found in Alpha (8-14Hz) and Beta Windows (14-30Hz). The Delta/Theta ERS showed a differential effect of CS+ versus CS- at Prefrontal, Frontal and Midline Channels, while Alpha and Beta ERD were greater at Parietal and Occipital Channels early in the stimulus train. The Gamma ERS Window increased from habituation to acquisition over a broad area from frontal and occipital electrodes. The CS Valence and Salience were greater for CS+ than CS-, and were correlated with each other and with the ERD at overlapping channels, particularly in the Alpha Window. Expectancy and CS Skin Conductance Response were greater for CS+ than CS- and were correlated with ERSP at fewer channels than Valence or Salience. These results suggest that Alpha ERSP activity during fear conditioning reflects Valence and Salience of the CSs more than conditioning per se.
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Affiliation(s)
- J H Chien
- Department of Neurosurgery, Johns Hopkins University, Baltimore, USA
| | - L Colloca
- Department of Pain Translational Symptom Science, School of Nursing, and Department of Anesthesiology, School of Medicine, University of Maryland, Baltimore, USA
| | - A Korzeniewska
- Departments of Neurology and Cognitive Science, Johns Hopkins University, Baltimore, USA
| | - J J Cheng
- Department of Neurosurgery, Emory University, Atlanta, USA
| | - C M Campbell
- Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, USA
| | - A E Hillis
- Departments of Neurology and Cognitive Science, Johns Hopkins University, Baltimore, USA
| | - F A Lenz
- Department of Neurosurgery, Johns Hopkins University, Baltimore, USA.
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Ye JJ, Lee KT, Lin JS, Chuang CC. Observing continuous change in heart rate variability and photoplethysmography-derived parameters during the process of pain production/relief with thermal stimuli. J Pain Res 2017; 10:527-533. [PMID: 28331355 PMCID: PMC5348136 DOI: 10.2147/jpr.s129287] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/26/2023] Open
Abstract
Continuously monitoring and efficiently managing pain has become an important issue. However, no study has investigated a change in physiological parameters during the process of pain production/relief. This study modeled the process of pain production/relief using ramped thermal stimulation (no pain: 37°C water, process of pain production: a heating rate of 1°C/min, and subject feels pain: water kept at the painful temperature for each subject, with each segment lasting 10 min). In this duration, the variation of the heat rate variability and photoplethysmography-derived parameters was observed. A total of 40 healthy individuals participated: 30 in the trial group (14 males and 16 females with a mean age of 22.5±1.9 years) and 10 in the control group (7 males and 3 females with a mean age of 22.5±1.3 years). The results showed that the numeric rating scale value was 5.03±1.99 when the subjects felt pain, with a temperature of 43.54±1.70°C. Heart rate, R-R interval, low frequency, high frequency, photoplethysmography amplitude, baseline, and autonomic nervous system state showed significant changes during the pain production process, but these changes differed during the period Segment D (painful temperature 10: min). In summary, the study observed that physiological parameters changed qualitatively during the process of pain production and relief and found that the high frequency, low frequency, and photoplethysmography parameters seemed to have different responses in four situations (no pain, pain production, pain experienced, and pain relief). The trends of these variations may be used as references in the clinical setting for continuously observing pain intensity.
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Affiliation(s)
- Jing-Jhao Ye
- Department of Biomedical Engineering, Chung Yuan Christian University, Chung Li, Taiwan
| | - Kuan-Ting Lee
- Department of Biomedical Engineering, Chung Yuan Christian University, Chung Li, Taiwan
| | - Jing-Siang Lin
- Department of Biomedical Engineering, Chung Yuan Christian University, Chung Li, Taiwan
| | - Chiung-Cheng Chuang
- Department of Biomedical Engineering, Chung Yuan Christian University, Chung Li, Taiwan
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Li X, Ge SN, Li Y, Wang HT. Neurokinin-1 Receptor-Immunopositive Neurons in the Medullary Dorsal Horn Provide Collateral Axons to both the Thalamus and Parabrachial Nucleus in Rats. Neurochem Res 2017; 42:375-388. [PMID: 28097463 DOI: 10.1007/s11064-016-2080-0] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2016] [Revised: 08/18/2016] [Accepted: 10/04/2016] [Indexed: 01/16/2023]
Abstract
It has been suggested that the trigemino-thalamic and trigemino-parabrachial projection neurons in the medullary dorsal horn (MDH) are highly implicated in the sensory-discriminative and emotional/affective aspects of orofacial pain, respectively. In previous studies, some neurons were reported to send projections to both the thalamus and parabrachial nucleus by way of collaterals in the MDH. However, little is known about the chemoarchitecture of this group of neurons. Thus, in the present study, we determined whether the neurokinin-1 (NK-1) receptor, which is crucial for primary orofacial pain signaling, was expressed in MDH neurons co-innervating the thalamus and parabrachial nucleus. Vesicular glutamate transporter 2 (VGLUT2) mRNA, a biomarker for the subgroup of glutamatergic neurons closely related to pain sensation, was assessed in trigemino-parabrachial projection neurons in the MDH. After stereotactic injection of fluorogold (FG) and cholera toxin subunit B (CTB) into the ventral posteromedial thalamic nucleus (VPM) and parabrachial nucleus (PBN), respectively, triple labeling with fluorescence dyes for FG, CTB and NK-1 receptor (NK-1R) revealed that approximately 76 % of the total FG/CTB dually labeled neurons were detected as NK-1R-immunopositive, and more than 94 % of the triple-labeled neurons were distributed in lamina I. In addition, by FG retrograde tract-tracing combined with fluorescence in situ hybridization (FISH) for VGLUT2 mRNA, 54, 48 and 70 % of FG-labeled neurons in laminae I, II and III, respectively, of the MDH co-expressed FG and VGLUT2 mRNA. Thus, most of the MDH neurons co-innervating the thalamus and PBN were glutamatergic. Most MDH neurons providing the collateral axons to both the thalamus and parabrachial nucleus in rats were NK-1R-immunopositive and expressed VGLUT2 mRNA. NK-1R and VGLUT2 in MDH neurons may be involved in both sensory-discriminative and emotional/affective aspects of orofacial pain processing.
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Affiliation(s)
- Xu Li
- Department of Colorectal Surgery, Changhai Hospital, The Second Military Medical University, Shanghai, 200433, China
| | - Shun-Nan Ge
- Department of Neurosurgery, Tangdu Hospital, The Fourth Military Medical University, Xi'an, 710038, China.
| | - Yang Li
- Department of Neurosurgery, Tangdu Hospital, The Fourth Military Medical University, Xi'an, 710038, China
| | - Han-Tao Wang
- Department of Colorectal Surgery, Changhai Hospital, The Second Military Medical University, Shanghai, 200433, China.
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Medeiros LF, Caumo W, Dussán-Sarria J, Deitos A, Brietzke A, Laste G, Campos-Carraro C, de Souza A, Scarabelot VL, Cioato SG, Vercelino R, de Castro AL, Araújo AS, Belló-Klein A, Fregni F, Torres ILS. Effect of Deep Intramuscular Stimulation and Transcranial Magnetic Stimulation on Neurophysiological Biomarkers in Chronic Myofascial Pain Syndrome. PAIN MEDICINE 2016; 17:122-35. [PMID: 26408420 DOI: 10.1111/pme.12919] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
Abstract
OBJECTIVE The aim was to assess the neuromodulation techniques effects (repetitive transcranial magnetic stimulation [rTMS] and deep intramuscular stimulation therapy [DIMST]) on pain intensity, peripheral, and neurophysiological biomarkers chronic myofascial pain syndrome (MPS) patients. DESIGN Randomized, double blind, factorial design, and controlled placebo-sham clinical trial. SETTING Clinical trial in the Laboratory of Pain and Neuromodulation at Hospital de Clínicas de Porto Alegre (NCT02381171). SUBJECTS We recruited women aged between 19- and 75-year old, with MPS diagnosis. METHODS Patients were randomized into four groups: rTMS + DIMST, rTMS + sham-DIMST, sham-rTMS + DIMST, sham-rTMS + sham-DIMST; and received 10 sessions for 20 minutes each one (rTMS and DIMST). Pain was assessed by visual analogue scale (VAS); neurophysiological parameters were assessed by transcranial magnetic stimulation; biochemical parameters were: BDNF, S100β, lactate dehydrogenase, inflammatory (TNF-α, IL6, and IL10), and oxidative stress parameters. RESULTS We observed the pain relief assessed by VAS immediately assessed before and after the intervention (P < 0.05, F(1,3)= 3.494 and F(1,3)= 4.656, respectively); in the sham-rTMS + DIMST group and both three active groups in relation to sham-rTMS + sham-DIMST group, respectively. There was an increase in the MEP after rTMS + sham-DIMST (P < 0.05). However, there was no change in all-peripheral parameters analyzed across the treatment (P > 0.05). CONCLUSION Our findings add additional evidence about rTMS and DIMST in relieving pain in MPS patients without synergistic effect. No peripheral biomarkers reflected the analgesic effect of both techniques; including those related to cellular damage. Additionally, one neurophysiological parameter (increased MEP amplitude) needs to be investigated.
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Kurek Eken M, Özkaya E, Tarhan T, İçöz Ş, Eroğlu Ş, Kahraman ŞT, Karateke A. Effects of closure versus non-closure of the visceral and parietal peritoneum at cesarean section: does it have any effect on postoperative vital signs? A prospective randomized study. J Matern Fetal Neonatal Med 2016; 30:922-926. [PMID: 27187047 DOI: 10.1080/14767058.2016.1190826] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/21/2022]
Abstract
OBJECTIVE To investigate the effect of peritonization at cesarean section on postoperative vital signs which was thought to be an indirect finding secondary to increased sympathetic activity originated from pain caused by stretched peritoneum. METHODS One hundred and thirty-three pregnant women were randomized to four groups; Closure of parietal peritoneum only (group 1; n = 32), closure of visceral and parietal peritoneums (group 2; n = 32), no closure of peritoneums (group 3; n = 32) and closure of the visceral peritoneum only (group 4; n = 32). All participants were monitored for blood pressure, pulse activity and hourly urinary output during the first postoperative 24 h. Postoperative pain was measured using a Visual Analogue Scale 6th and 24th hours after surgery. Return of bowel function was measured from the end of the operation to the first passage of flatus. Operating time, pre- and postoperative hemoglobin, postoperative complications, length of hospital stay and postoperative urine osmolarity were noted. RESULTS The mean surgery duration was significantly longer in group 2. Diuresis was found significantly decreased in group 2. Pulse rate and systolic and diastolic blood pressure were significantly higher in group 2. Closure of both peritoneums was associated with higher post-operative pain as assessed using Visual analogue scale score analyses in group 2. CONCLUSION Both visceral and parietal membrane closure in cesarean section should be avoided in women with hypertensive disorders, renal function abnormalities and autonomic dysfunction because of increased postoperative pain and associated sympathetic overactivity.
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Affiliation(s)
- Meryem Kurek Eken
- a Obstetric and Gynecology Department, Adnan Menderes University Medical Faculty , Aydin , Turkey
| | - Enis Özkaya
- b Zeynep Kamil Maternity and Children Hospital, Obstetric and Gynecology Department , İstanbul , Turkey , and
| | - Tuba Tarhan
- c Medipol University Medical Faculty Sefaköy Hospital , Istanbul , Turkey
| | - Şeyma İçöz
- b Zeynep Kamil Maternity and Children Hospital, Obstetric and Gynecology Department , İstanbul , Turkey , and
| | - Şebnem Eroğlu
- b Zeynep Kamil Maternity and Children Hospital, Obstetric and Gynecology Department , İstanbul , Turkey , and
| | - Ş Tuğba Kahraman
- c Medipol University Medical Faculty Sefaköy Hospital , Istanbul , Turkey
| | - Ateş Karateke
- b Zeynep Kamil Maternity and Children Hospital, Obstetric and Gynecology Department , İstanbul , Turkey , and
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