HEART RATE VARIABILITY, DYSAUTONOMIA AND SPORTS RELATED CONCUSSION
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HEART RATE VARIABILITY, DYSAUTONOMIA AND SPORTS RELATED CONCUSSION Big Sky Athletic Training Sports Medicine Conference 2022 Robert J. Baker ATC, MD, PhD Program Director Primary Care Sports Medicine Professor Departments of Family and Community Medicine and Orthopedics Western Michigan University, Homer Stryker MD School of Medicine
OBJECTIVES: • To compare post-concussion recovery among the neurological domains of symptom evaluation, cognition, balance, ocular-motor, and autonomic nervous system [using the surrogate of heart rate variability (HRV)] and with the clinical determination that an athlete has recovered. • To describe the neurological effects of concussion within these domains and any association among the domains affected. • To describe longitudinal patterns of recovery from concussion within these domains.
ILLUSTRATIVE CASE • 15 year old male Concussion 3 months ago with soccer. • Most symptoms resolved in 1-2 weeks with PCP • Persistent symptoms of fatigue, low energy, shortness of breath with running. Previous Half Marathon runner now with symptoms at 2-3 miles. • Symptoms progress and presented at the ED • Follow up with Cardiology: EKG- ICRBB (rapid HR 93), Normal Echo, POTS • Labs: CBC Normal, TSH normal, Free T4 normal, CMP normal, Vitamin D 52, Ferritin 191
• General: Slight male, no acute distress. PHYSICAL EXAM • Heart: Normal s1, s2. No murmur, click, rub, or gallop was heard. • Peripheral pulses are 2+ and full throughout with no radial-femoral delay. Extremities are warm and well-perfused with no cyanosis, clubbing or edema noted. • Pulmonary/Chest: Effort normal and breath sounds normal. No respiratory distress. He has no wheezes. He has no rales. • Neurological: He is alert and oriented to person, place, and time. He has normal strength. He displays normal reflexes. No cranial nerve deficit. He exhibits normal muscle tone. He displays a negative Romberg sign. Coordination and gait normal. Immediate memory: recalled the 5 words easily Delayed recall score: 4/5 Concentration: digit backwards score is 4/5. Correct month in reverse order Balance: normal balance tests Coordination: normal finger to nose test • Psychiatric: He has a normal mood and affect. His speech is normal. Judgment and thought content normal. Cognition and memory are normal. He exhibits normal recent memory and normal remote memory.
SAMPLE HEART RATE TRAINING ZONE CALCULATIONS UPMC 5-Stage Exertion Protocol for Concussion • Stage 1: 30%-40% maximal exertion 113-126 Light aerobic conditioning 0.3 (HRR) + RHR = 0.3 (124) +76 • Stage 2: 40%-60% maximal exertion 126-150 Light to moderate aerobic conditioning 0.4 (HRR) + RHR = 0.4 (124) + 76 • Stage 3: 60%-80% maximal exertion 150-175 Moderately aggressive aerobic exercise 0.6 (HRR) + RHR = 0.6 (124) + 76 • Stage 4: 80% maximal exertion 175 80% exertion avoiding contact 0.8 (HRR) + RHR = 0.8(124) + 76 • Stage 5: 100% 200 Full exertion for sports with contact Miranda, N. A., Boris, J. R., Kouvel, K. M., & Stiles, L. (2018). Activity and exercise intolerance after concussion: Identification and management of postural orthostatic tachycardia syndrome. Journal of Neurologic Physical Therapy, 42(3), 163–171. https://doi.org/10.1097 /NPT.0000000000000231
CLINICAL QUESTIONS • Role of Dysautonomia Prolonged Concussion Symptoms? • Role of POTS and Post Concussion Symptoms? • Can We Measure of HRV with Mobile Device?
Role of Dysautonomia Prolonged Concussion Symptoms? Harmon KG, Clugston JR, Dec K, et al. American Medical Society for Sports Medicine position statement on concussion in sport. Br J Sports Med. 2019;53(4):213-225. doi:10.1136/bjsports-2018-100338
THEORY OF PROLONGED SYMPTOMS Physiologic -> Autonomic nervous system (ANS) dysfunction (dysautonomia) 1. Mechanical changes & neuro- metabolic -> alterations cerebral circulation 2. Metabolic and physiologic changes outside the brain Higher heart rates at rest Elevated HR cognitive and physiological stress Severe TBI & SRC associated with greater sympathetic nervous activity Hovda DA, Lee SM, Smith ML, et al. The neurochemical and metabolic cascade following brain injury: moving from animal models to man. J Neurotrauma. & lower parasympathetic activity 1995;12(5):903-906. Leddy, J. J., Sandhu, H., Sodhi, V., Baker, J. G., & Willer, B. (2012). Rehabilitation of concussion and post-concussion syndrome. Sports Health, 4(2), 147–154. https://doi.org /10.1177/1941738111433673
THEORY OF PROLONGED SYMPTOMS Autonomic dysregulation TBI severity Improves during TBI recovery Altered endocrine or Neuropeptide milieu after TBI Autoregulation: cerebral blood flow changes in systemic blood pressure Symptoms often reappear or worsen with physical and/or mental exertion Secondary insults: hypotension, intracranial hypertension, and dehydration Leddy, J. J., Sandhu, H., Sodhi, V., Baker, J. G., & Willer, B. (2012). Rehabilitation of concussion and post-concussion syndrome. Sports Health, 4(2), 147–154. https://doi.org /10.1177/1941738111433673
THEORY OF PROLONGED SYMPTOMS Physiologic Altered ANS balance -> pulmonary ventilation altered during exertion The primary ANS control center is located in the brainstem Twisting mechanism (glancing blow) Alter central ANS regulation cardiorespiratory/ventilation fMRI ANS diffusely distributed beyond the brainstem Leddy, J. J., Sandhu, H., Sodhi, V., Baker, J. G., & Willer, B. (2012). Rehabilitation of concussion and post- concussion syndrome. Sports Health, 4(2), 147–154. https://doi.org /10.1177/1941738111433673
ROLE OF EVALUATION OF DYSAUTONOMIA IN • ANS dysfunction after a mild TBI -> changes in heart CONCUSSION? rate variability • Autonomic disfunction in the post-acute stage after a concussion • long term effects of mild TBI on the autonomic nervous system unknown? • systemic effects of ANS dysfunction in mild TBI? • Persistence of autonomic dysfunction after symptomatic resolution of concussions -> return-to- play protocols? Esterov, D., Greenwald, BD. (2017). Autonomic dysfunction after mild traumatic brain injury. Brain Sci. 7 (100); doi:10.3390/brainsci7080100
ROLE OF POTS AND POST CONCUSSION SYMPTOMS? Pediatric: 11.4% of individuals Activation of the sympathetic diagnosed with POTS report onset nervous system of symptoms within 3 months of sustaining a concussion lightheadedness shortness of breath chest pain tachycardia palpitations standing/with exertion exercise intolerance Miranda, N. A., Boris, J. R., Kouvel, K. M., & Stiles, L. (2018). Activity and exercise intolerance after concussion: Identification and management of postural orthostatic tachycardia syndrome. Journal of Neurologic Physical Therapy, 42(3), 163–171. https://doi.org/10.1097 /NPT.0000000000000231
HEART RATE AND HEART RATE VARIABILITY AT REST AND DURING EXERCISE IN BOYS WHO SUFFERED A SEVERE TRAUMATIC BRAIN INJURY AND TYPICALLY-DEVELOPED CONTROLS • Heart rate (HR) and heart rate variability (HRV) at rest and during exercise in children with post-severe traumatic brain injury • Children post-TBI demonstrated higher mean HR values at rest (TBI 91.87.0 beats per minute vs 72.07.1 beats per minute in controls, p
HEART RATE VARIABILITY IN NEUROREHABILITATION PATIENTS WITH SEVERE ACQUIRED BRAIN INJURY • Patients with traumatic brain injury (TBI) by means of reduced heart rate variability (HRV). It was hypothesized that patient groups with other ABI etiology (mainly stroke, subarachnoid hemorrhage and anoxia) would also present reduced HRV • HRV appeared identical across ABI etiology • HRV was considerably reduced in an heterogenic ABI patient group admitted for neurorehabilitation Vistisen, S. T., Hansen, T. K., Jensen, J., Nielsen, J. F., & Fleischer, J. (2014). Heart rate variability in neurorehabilitation patients with severe acquired brain injury. Brain Injury, 28(2), 196–202. https://doi.org/10.3109 /02699052.2013.860477
MULTIMODAL ASSESSMENT OF SPORT- RELATED CONCUSSION • Determine which assessments best identify athletes with sport-related concussion (SRC) from healthy controls in the acute/early subacute phase (within 10 days of SRC) of injury. • Prospective, cohort, specialty concussion clinic • Multimodal evaluation that are most robust at discriminating SRC acute/early subacute phase: 1. Symptom report 2. Symptoms on vestibular/oculomotor assessment Sherry NS, Fazio-Sumrok V, Sufrinko A, Collins MW, Kontos AP. Multimodal Assessment of Sport-Related Concussion. Clin J Sport Med. 2021;31(3):244-249. doi:10.1097/JSM.0000000000000740
HEART RATE VARIABILITY OF RECENTLY CONCUSSED ATHLETES AT REST AND EXERCISE • Neuroautonomic cardiovascular regulation (HRV) in recently concussed athletes at rest and in response to low- moderate steady-state exercise, using heart rate variability • No difference at rest was detected between the concussed athletes and their matched controls • Exercise tests: concussed group demonstrated a significant decrease in the mean RR interval, and low- and high- frequency power (P 0.05) • Low-moderate steady-state exercise elicits a neuroautonomic cardiovascular dysfunction in concussed athletes (exercise induced uncoupling between Gall, B., Parkhouse, W., & Goodman, D. (2004). Heart rate the autonomic and cardiovascular variability of recently concussed athletes at rest and exercise. systems). Medicine & Science in Sports & Exercise, 36(8), 1269–1274. https://doi.org/10.1249/01.MSS.0000135787.73757.4D
HEART RATE VARIABILITY OF ATHLETES ACROSS CONCUSSION RECOVERY MILESTONES: A PRELIMINARY STUDY. • Heart rate variability (HRV) in athletes with concussion across three phases of recovery • Prospective matched control group: 1. HRV 2. Symptoms Questionnaire • 3 phases of recovery (1) symptomatic; (2). asymptomatic; and (3) one-week after return-to-play (RTP) • Athletes with concussion displayed autonomic dysfunction in some measures of HRV that persisted beyond RTP and were related to a previous history of concussion Senthinathan, A., Mainwaring, L. M., & Hutchison, M. (2017). Heart rate variability of athletes across concussion recovery milestones: A preliminary study. Clinical Journal of Sport Medicine, 27(3), 288–295. https://doi.org/10.1097 /JSM.0000000000000337
Autonomic Function Following Concussion in Youth Athletes: An Exploration of Heart Rate Variability Using 24-hour Recording Methodology • Heart rate variability (HRV) is a non-invasive physiological indicator of the autonomic nervous system, capturing the reciprocal interplay between the sympathetic and parasympathetic nervous systems • 24 h recording methodology • (1) evaluate the physiological effects of a concussion in youth athletes • (2) describe the trajectory of physiological change resolution of self-reported post- concussion symptoms. • The raw beat-to-beat time intervals captured can be transformed to derive time domain and frequency domain measures Paniccia M, Taha T, Keightley M, et al. Autonomic Function Following Concussion in Youth Athletes: An Exploration of Heart Rate Variability Using 24-hour Recording Methodology. J Vis Exp. 2018;(139):58203. Published 2018 Sep 21. doi:10.3791/58203
POST CONCUSSIVE DISORDERS (PCD) 1. Physiological post-PCD: characterized by concussion symptoms from alterations in cerebral blood flow secondary to autonomic nervous system dysfunction 2. Vestibulo-ocular PCD: characterized by symptoms secondary to dysfunction of the vestibular and oculomotor systems 3. Cervicogenic PCD: characterized by muscle trauma and inflammation secondary to cervical spine somatosensory system. 4. Clinical depression 5. Post traumatic mood disorders 6. Migraine headaches Leddy, J. J., Sandhu, H., Sodhi, V., Baker, J. G., & Willer, B. (2012). Rehabilitation of concussion and post-concussion syndrome. Sports Health, 4(2), 147–154. https://doi.org /10.1177/1941738111433673 Esterov, D., Greenwald, BD. (2017). Autonomic dysfunction after mild traumatic brain injury. Brain Sci. 7 (100); doi:10.3390/brainsci7080100
CAN WE MEASURE OF HRV WITH MOBILE DEVICE? Paniccia M, Taha T, Keightley M, et al. Autonomic Function Following Concussion in Youth Athletes: An Exploration of Heart Rate Variability Using 24-hour Recording Methodology. J Vis Exp. 2018;(139):58203. Published 2018 Sep 21. doi:10.3791/58203
VALIDITY OF THE ELITE HRV SMARTPHONE APPLICATION FOR EXAMINING HEART RATE VARIABILITY IN A FIELD-BASED SETTING • Relationship and validity between a vagal-related HRV index, rMSSD, when derived from a smartphone application accessible with most operating systems against a frequently used computer software program, Kubios HRV 2.2 • While differences exist between the two sources of HRV analysis however, further research is warranted, as this smartphone HRV application may offer a reliable platform when assessing parasympathetic modulation Perrotta, A. S., Jeklin, A. T., Hives, B. A., Meanwell, L. E., & Warburton, D. E. R. (2017). Validity of the elite HRV smartphone application for examining heart rate variability in a field-based setting. The Journal of Strength and Conditioning Research, 31(8), 2296–2302. https://doi.org /10.1519/JSC.0000000000001841
FACE COOLING EXPOSES CARDIAC PARASYMPATHETIC AND SYMPATHETIC DYSFUNCTION IN RECENTLY CONCUSSED COLLEGE • Concussed college ATHLETES athletes (CA) have attenuated parasympathetic and sympathetic responses to face cooling (FC) • These data indicate that symptomatic concussed patients have impaired cardiac parasympathetic and sympathetic activation Johnson, B. D., O’Leary, M. C., McBryde, M., Sackett, J. R., Schlader, Z. J., & Leddy, J. J. (2018). Face cooling exposes cardiac parasympathetic and sympathetic dysfunction in recently concussed college athletes. Physiological Reports, 6(9), e13694. https://doi.org/10.14814/phy2.13694
MOBILE EVALUATION OF HEART RATE VARIABILITY USING THE DIVER’S REFLEX Significantly decreased compared to at rest • Validates prior research with larger sample sizes and proposes a model for establishing baseline HRV reactivity in healthy participants • RMSSD was elevated at 1 and 2 min (+47.4 ms, p < .0001; +16.5 ms, p = .014) following face cooling and fell to baseline at 3 min (+4.6 ms, p = .52) • LF/HF ratio decreased following face cooling at 2 and 3 min (change from rest %: 2 min, −33%, p = .007; 3 min, −50%, p = < .0001) • The Elite HRV platform can detect an elevation in RMSSD in the first minute following face cooling with a return to baseline in the second and third minutes. It can also detect a consistent decrease in LF/HF following face cooling Seltzer, H., Pellman, M., Warchock, R., Billian, J., & Baker, R. (2021). Mobile evaluation of heart rate variability using the Diver’s Reflex. NeuroRegulation, 8(2), 96–103. https://doi.org/10.15540/nr.8.2.96
MOBILE EVALUATION OF HEART RATE VARIABILITY USING THE DIVER’S REFLEX Significantly increased compared to at rest Seltzer, H., Pellman, M., Warchock, R., Billian, J., & Baker, R. (2021). Mobile evaluation of heart rate variability using the Diver’s Reflex. NeuroRegulation, 8(2), 96–103. https://doi.org/10.15540/nr.8.2.96
AUTONOMIC DYSFUNCTION SUMMARY • Ongoing central and systemic physiologic regulatory dysfunction has been proposed as a mechanism for persistent systems in patients with PCS • Concussion can result in transient or more persistent autonomic dysregulation and ultimately POTS and hyperadrenergic states • Fatigue, dizziness, tachycardia, headaches, nausea, exercise intolerance Leddy Neurorehabilitation 2007 Miranda J Neurol Phys Ther 2018
AUTONOMIC DYSFUNCTION SUMMARY FUTURE DIRECTIONS • Understanding ANS dysfunction at rest following concussion recovery and post recovery • Current literature is limited by small sample sizes, lack of female or pediatric participants, methodological heterogeneity and lack of follow-up • While there is some evidence to suggest changes during physical activity following concussion, methodological limitations • Understanding the effect of concussion on ANS will contribute to the development of more comprehensive concussion management strategies Blake, T. A., McKay, C. D., Meeuwisse, W. H., & Emery, C. A. (2016). The impact of concussion on cardiac autonomic function: A systematic review. Brain Injury, 30(2), 132–145. https://doi.org/10.3109/02699052.2015.1093659
REFERENCES • Patricios JS, et al. Br J Sports Med 2018;52:635–641. doi:10.1136/bjsports-2018-099079 • Hovda DA, Lee SM, Smith ML, et al. The neurochemical and metabolic cascade following brain injury: moving from animal models to man. J Neurotrauma. 1995;12(5):903-906. • Leddy, J. J., Sandhu, H., Sodhi, V., Baker, J. G., & Willer, B. (2012). Rehabilitation of concussion and post-concussion syndrome. Sports Health, 4(2), 147–154. https://doi.org /10.1177/1941738111433673 • Miranda, N. A., Boris, J. R., Kouvel, K. M., & Stiles, L. (2018). Activity and exercise intolerance after concussion: Identification and management of postural orthostatic tachycardia syndrome. Journal of Neurologic Physical Therapy, 42(3), 163–171. https://doi.org/10.1097 /NPT.0000000000000231 • Esterov, D., Greenwald, BD. (2017). Autonomic dysfunction after mild traumatic brain injury. Brain Sci. 7 (100); doi:10.3390/brainsci7080100 • Shaffer, F., & Ginsberg, J. P. (2017). An overview of heart rate variability metrics and norms. Frontiers in Public Health, 5, 258. https://doi.org/10.3389/fpubh.2017.00258 • Senthinathan, A., Mainwaring, L. M., & Hutchison, M. (2017). Heart rate variability of athletes across concussion recovery milestones: A preliminary study. Clinical Journal of Sport Medicine, 27(3), 288–295. https://doi.org/10.1097 /JSM.0000000000000337 • Gall, B., Parkhouse, W., & Goodman, D. (2004). Heart rate variability of recently concussed athletes at rest and exercise. Medicine & Science in Sports & Exercise, 36(8), 1269–1274. https://doi.org/10.1249/01.MSS.0000135787.73757.4D • Paniccia M, Taha T, Keightley M, et al. Autonomic Function Following Concussion in Youth Athletes: An Exploration of Heart Rate Variability Using 24-hour Recording Methodology. J Vis Exp. 2018;(139):58203. Published 2018 Sep 21. doi:10.3791/58203 • Leddy, J., Baker, J. G., Haider, M. N., Hinds, A., & Willer, B. (2017). A physiological approach to prolonged recovery from sport-related concussion. Journal of Athletic Training, 52(3), 299–308. https://doi.org/10.4085/1062-6050-51.11.08
REFERENCES • Sherry NS, Fazio-Sumrok V, Sufrinko A, Collins MW, Kontos AP. Multimodal Assessment of Sport-Related Concussion. Clin J Sport Med. 2021;31(3):244-249. doi:10.1097/JSM.0000000000000740 • Johnson, B. D., O’Leary, M. C., McBryde, M., Sackett, J. R., Schlader, Z. J., & Leddy, J. J. (2018). Face cooling exposes cardiac parasympathetic and sympathetic dysfunction in recently concussed college athletes. Physiological Reports, 6(9), e13694. https://doi.org/10.14814/phy2.13694 • Perrotta, A. S., Jeklin, A. T., Hives, B. A., Meanwell, L. E., & Warburton, D. E. R. (2017). Validity of the elite HRV smartphone application for examining heart rate variability in a field-based setting. The Journal of Strength and Conditioning Research, 31(8), 2296–2302. https://doi.org /10.1519/JSC.0000000000001841 • Blake, T. A., McKay, C. D., Meeuwisse, W. H., & Emery, C. A. (2016). The impact of concussion on cardiac autonomic function: A systematic review. Brain Injury, 30(2), 132–145. https://doi.org/10.3109/02699052.2015.1093659 • Vistisen, S. T., Hansen, T. K., Jensen, J., Nielsen, J. F., & Fleischer, J. (2014). Heart rate variability in neurorehabilitation patients with severe acquired brain injury. Brain Injury, 28(2), 196–202. https://doi.org/10.3109 /02699052.2013.860477 • Katz-Leurer, M., Rotem, H., Keren, O., & Meyer, S. (2010). Heart rate and heart rate variability at rest and during exercise in boys who suffered a severe traumatic brain injury and typically-developed controls. Brain Injury, 24(2), 110–114. https://doi.org/10.3109/02699050903508234 • Seltzer, H., Pellman, M., Warchock, R., Billian, J., & Baker, R. (2021). Mobile evaluation of heart rate variability using the Diver’s Reflex. NeuroRegulation, 8(2), 96–103. https://doi.org/10.15540/nr.8.2.96 • Harmon KG, Clugston JR, Dec K, et al. American Medical Society for Sports Medicine position statement on concussion in sport. Br J Sports Med. 2019;53(4):213-225. doi:10.1136/bjsports-2018-100338 • Hovda DA, Lee SM, Smith ML, et al. The neurochemical and metabolic cascade following brain injury: moving from animal models to man. J Neurotrauma. 1995;12(5):903-906.
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