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Early Sympathetic Neural Responses During a Cold Pressor Test Linked To Early sympathetic neural responses during a cold pressor test linked to ANGOR UNIVERSITY pain perception Huang, Mu; Yoo, Jeung-Ki; Stickford, Abigail; Moore, Jonathan; Hendrix, Joseph ; Crandall, Craig; Fu, Qi Clinical Autonomic Research DOI: 10.1007/s10286-019-00635-7 PRIFYSGOL BANGOR / B Published: 01/04/2021 Peer reviewed version Cyswllt i'r cyhoeddiad / Link to publication Dyfyniad o'r fersiwn a gyhoeddwyd / Citation for published version (APA): Huang, M., Yoo, J-K., Stickford, A., Moore, J., Hendrix, J., Crandall, C., & Fu, Q. (2021). Early sympathetic neural responses during a cold pressor test linked to pain perception. Clinical Autonomic Research , 31(2), 215-224. https://doi.org/10.1007/s10286-019-00635-7 Hawliau Cyffredinol / General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. 29. Sep. 2021 1 1 Early sympathetic neural responses during a cold pressor test 2 linked to pain perception 3 Mu Huang1,2, Jeung-Ki Yoo1,3, Abigail S.L. Stickford1,4, Jonathan P. Moore1,5, Joseph M. Hendrix1,6, 4 Craig G. Crandall1,3, Qi Fu1,3 5 1Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital Dallas; 6 2 Department of Health Care Sciences, University of Texas Southwestern Medical Center, 7 Dallas; 8 3 Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas; 9 4 Department of Health and Exercise Science, Appalachian State University; 10 5 School of Sport, Health and Exercise Sciences, Bangor University; 11 6 Department of Anesthesiology & Pain Management, University of Texas Southwestern 12 Medical Center, Dallas. 13 Tables: 1 14 Figures: 8 15 Corresponding author: Qi Fu, M.D., Ph.D., 16 UT Southwestern Medical Center 17 Institute for Exercise and Environmental Medicine 18 Texas Health Presbyterian Hospital Dallas 19 7232 Greenville Avenue, Suites 435, Dallas, Texas 75231 20 Phone: (214) 345-8125; Fax: (214) 345-4618 21 Email: [email protected] 22 Running Title: Pain perception and initial sympathetic responses 23 2 24 Abstract 25 Purpose: There is considerable interindividual variability in the perception of pain. Given that pain 26 management is a major public health problem, gaining insight into underlying physiology of these 27 perceptual differences is important. We tested the hypothesis that when interindividual variability in 28 initial muscle sympathetic nerve activity (MSNA) responses to a cold pressor test (CPT) is 29 identified, the divergent responses will be linked to differences in pain perception in healthy young 30 men and women. 31 Methods: In the supine position, blood pressure (BP) and MSNA were measured at baseline and 32 during a 2-minute CPT. Immediately following the CPT, pain was rated (range 0-10). 33 Results: Two groups were established: positive responders (Pos, n=12) and negative responders 34 (Neg, n=12) based on the initial (first 30 s) MSNA response profiles (Pos:12±9, Neg:-3±3 35 bursts/min, P<0.0001). MSNA response profiles throughout the CPT were different between 36 groups (P<0.0001). Peak MSNA increases were different (Pos:27±11, Neg:9±5 bursts/min, 37 P<0.0001) and corresponded with initial MSNA responses (R2=0.6881, P<0.0001). Blood pressure 38 responses were also different throughout the CPT (P<0.0001). Most importantly, the perception of 39 pain induced by the CPT was different between the two partitioned groups (Pos:8±1, Neg:4±1, 40 P<0.0001). 41 Conclusions: The results indicate that in healthy young men and women, there are divergent 42 initial sympathetic neural responses to a given painful stimulus that are linked to the magnitude of 43 pain perception. These findings highlight the distinctive sympathetic patterns that may contribute to 44 the considerable interindividual variability in the perception of pain. 3 45 Key Words: Pain; Blood Pressure; Muscle Sympathetic Nerve Activity; Individual 46 Differences 47 Introduction 48 Pain is a major public health problem, with more than 100 million American adults 49 experiencing chronic pain conditions and costing society at least 560-635 billion dollars annually to 50 treat and manage (27). The pathophysiology and subsequent experience of pain is highly complex 51 and results in substantial variability in its perception (36, 58). One of many factors that may 52 modulate the responses to and perception of pain is the health of the cardiovascular system (45). 53 In fact, the systems modulating pain and blood pressure (BP) appear to be inherently linked (6, 23, 54 43, 44). This is demonstrated in several recent observational studies suggesting that a relationship 55 exists between pain responses and the risk of cardiovascular disease (7, 19, 25). 56 Acute pain leads to a rapid rise in BP, which in turn may reveal both short- and long term 57 cardiovascular risk (9, 34, 35, 50, 57). Experimentally, inducing noxious stimuli such as strong 58 pressure in the nail, mechanical pressure on the skin, hypertonic saline injection in the skin and 59 muscle, and immersion of the hand in ice water (cold pressor test, CPT), leads to the activation of 60 the sympathetic nervous system via a somatosensory reflex. The subsequent increase in efferent 61 sympathetic outflow (muscle sympathetic nerve activity (MSNA)), evokes downstream 62 cardiovascular responses and an elevation in BP (8, 30, 40, 41, 57). Effectively, experimentally- 63 induced pain allows for a functional model to demonstrate the strong relationship between 64 sympathetically-driven cardiovascular changes and the perception of pain (47). 65 Very much like the considerable interindividual variability in the perception of pain (20, 47), 66 there is interindividual variability in efferent sympathetic outflow during established 67 sympathoexcitatory stimuli. Indeed, it has recently been demonstrated that during mental stress 68 and hand grip, interindividual differences exist in the MSNA response (18, 26). Particularly 4 69 interesting, MSNA response variability during mental stress was apparent even in the initial 30 s of 70 the stress, wherein individuals exhibited either a rise or fall in sympathetic activity (26). Early 71 studies evaluating MSNA observed initial sympathoinhibition responses to noxious stimuli, 72 including the CPT (14, 30, 47). Adaptation to pain is composed of both inhibitory and facilitatory 73 influences (6, 38); however, it is unclear how the initial, individual MSNA responses relate to 74 subjective perception of pain. 75 Thus, the primary objective of this study is to determine if distinct MSNA response patterns 76 are linked with differences in the perception of pain. Based on the previous studies (30, 33, 47), we 77 hypothesized that there would be substantial interindividual variability in initial sympathetic neural 78 responses to CPT-induced acute pain. We further hypothesized that the initial MSNA responses 79 would correspond to the peak MSNA, BP responses, and perception of pain. Understanding this 80 relationship may set the foundation for future research on chronic pain as well as pain-induced 81 changes related to cardiovascular health. 82 Methods 83 Ethical Approval 84 All participants were informed of the purpose, procedures, and risks of the study before 85 providing written informed consent. The protocol and consent were approved by the Institutional 86 Review Boards at the University of Texas Southwestern Medical Center and Texas Health 87 Presbyterian Hospital Dallas (IRB # STU092013-036, STU082016-057, STU092017-068). This 88 research study conformed to standards set by the Declaration of Helsinki, except for registration in 89 a database. 90 Subjects 5 91 Twenty-four healthy subjects (14 women and 10 men; 32±9 [mean±SD] years old, body 92 mass index [BMI]: 26±3 kg/m2) participated. Descriptive characteristics of the subjects are outlined 93 in Table 1. All subjects were normotensive and had no evidence of cardiopulmonary, neurological 94 or renal disease, based on history and physical examination at the time of the study. No subject 95 smoked, used recreational drugs, or had other significant medical problems. No woman was 96 pregnant during the experiment. Parental history of hypertension was obtained in each subject. 97 Measurements 98 Cardiovascular Variables 99 Heart rate (HR) was determined from lead II of the electrocardiogram (ECG) (Hewlett- 100 Packard). Arm BP was measured by electrosphygmomanometry (model 4240, Suntech); with a 101 microphone placed over the brachial artery to detect Korotkoff sounds. Mean arterial pressure 102 (MAP) was calculated as [(SBP-DBP)/3] +DBP, where SBP and DBP are systolic and diastolic BP, 103 respectively. Respiration was monitored by a nasal cannula (Criticare systems, model 602-11). 104 Muscle Sympathetic Nerve Activity 105 Multiunit MSNA signals were obtained utilizing the microneurographic technique (55). 106 Briefly, a recording electrode was placed either in the peroneal nerve (n=19) at the popliteal fossa 107 or the radial nerve at the spiral groove (n=5), and a reference electrode was placed 108 subcutaneously 2 to 3 cm from the recording electrode (12, 39, 59). The nerve signals were 109 amplified (gain 70,000 to 160,000), band-pass filtered (700 to 2,000 Hz), full-wave rectified, and 110 integrated with a resistance-capacitance circuit – time constant 0.1 second (662C-3, 111 Bioengineering of University of Iowa).
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