Frequency analysis unveils cardiac autonomic dysfunction after mild traumatic brain injury

Journal of Neurotrauma

Volumn 28, Issue 9, 2011, Pages 1727-1738

  Hilz, Max J ^a,b   Defina, Philip A ^c   Anders, Stefan ^a   Koehn, Julia ^a   Lang, Christoph J ^a   Pauli, Elisabeth ^a   Flanagan, Steven R ^b   Schwab, Stefan ^a   Marthol, Harald ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c International Brain Research Foundation   (United States)

Author keywords

autonomic dysfunction; baroreflex; cardiovascular modulation; head trauma; TBI

Indexed keywords

ADULT; ANALYSIS OF VARIANCE; ARTICLE; AUTONOMIC DYSFUNCTION; BLOOD PRESSURE; BREATHING; CARDIOVASCULAR DISEASE; CLINICAL ARTICLE; FEMALE; HUMAN; MALE; OSCILLATION; PARASYMPATHETIC INNERVATION; PRESSORECEPTOR REFLEX; SENSITIVITY ANALYSIS; STANDING; SUPINE POSITION; SYMPATHETIC FUNCTION; TRAUMATIC BRAIN INJURY; VAGUS NERVE STIMULATION;

ADOLESCENT; ADULT; AUTONOMIC NERVOUS SYSTEM; AUTONOMIC NERVOUS SYSTEM DISEASES; BAROREFLEX; BLOOD PRESSURE; BRAIN INJURIES; CARDIOVASCULAR DISEASES; FEMALE; HEART RATE; HUMANS; MALE; MIDDLE AGED; SUPINE POSITION;

EID: 80054811496     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1497     Document Type: Article

References (55)

1. American College of Cardiology Cardiovascular Technology Assessment Committee. (1993). Heart rate variability for risk stratification of life-threatening arrhythmias. J. Am. Coll. Cardiol. 22, 948-950.
2. Barbic, F., Perego, F., Canesi, M., Gianni, M., Biagiotti, S., Costantino, G., Pezzoli, G., Porta, A., Malliani, A., and Furlan, R. (2007). Early abnormalities of vascular and cardiac autonomic control in Parkinson's disease without orthostatic hypotension. Hypertension 49, 120-126.
3. Barron, H.V., and Viskin, S. (1998). Autonomic markers and prediction of cardiac death after myocardial infarction. Lancet 351, 461-462.
4. Benarroch, E.E. (1997). Central Autonomic Network: Functional Organization and Clinical Correlations. Futura Publishing Company, Inc.: Armonk, NY.
5. Black, M., and Graham, D.I. (2002). Sudden unexplained death in adults caused by intracranial pathology. J. Clin. Pathol. 55, 44-50.
6. Brown, A.W., Leibson, C.L., Malec, J.F., Perkins, P.K., Diehl, N.N., and Larson, D.R. (2004). Long-term survival after traumatic brain injury: A population-based analysis. NeuroRehabilitation 19, 37-43.
7. Cencetti, S., Lagi, A., Cipriani, M., Fattorini, L., Bandinelli, G., and Bernardi, L. (1999). Autonomic control of the cerebral circulation during normal and impaired peripheral circulatory control. Heart 82, 365-372.
8. Centers for Disease Control and Prevention (CDC), National Center for Injury Prevention and Control. (2003). Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. Centers for Disease Control and Prevention: Atlanta.
9. Chan, C.T., Shen, X.S., Picton, P., and Floras, J. (2008). Nocturnal home hemodialysis im-proves baroreflex effectiveness index of end-stage renal disease patients. J. Hypertens. 26, 1795-1800.
10. Chan, C.T., Jain, V., Picton, P., Pierratos, A., and Floras, J.S. (2005). Nocturnal hemodialysis increases arterial baroreflex sensitivity and compliance and normalizes blood pressure of hypertensive patients with end-stage renal disease. Kidney Int. 68, 338-344.
11. Cole, C.R., Blackstone, E.H., Pashkow, F.J., Snader, C.E., and Lauer, M.S. (1999). Heart-rate recovery immediately after exercise as a predictor of mortality. N. Engl. J. Med. 341, 1351-1357.
12. Dutsch, M., Burger, M., Dorfler, C., Schwab, S., and Hilz, M.J. (2007). Cardiovascular autonomic function in post-stroke patients. Neurology 69, 2249-2255.
13. Flaada, J.T., Leibson, C.L., Mandrekar, J.N., Diehl, N., Perkins, P.K., Brown, A.W., and Malec, J.F. (2007). Relative risk of mortality after traumatic brain injury: A population-based study of the role of age and injury severity. J. Neurotrauma 24, 435-445.
14. Hilz, M.J., Dutsch, M., Perrine, K., Nelson, P.K., Rauhut, U., and Devinsky, O. (2001). Hemispheric influence on autonomic modulation and baroreflex sensitivity. Ann. Neurol. 49, 575-584.
15. Hilz, M.J. (2002). Quantitative autonomic functional testing in clinical trials, in: Neuromuscular Function and Disease. R. Brown, C. Bolton, and M. Aminoff (eds), W.B. Saunders Company: Philadelphia, pps. 1899-1929.
16. Hilz, M.J., Devinsky, O., Doyle, W., Mauerer, A., and Dutsch, M. (2002). Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. Brain 125, 985-995.
17. Hilz, M.J., and Schwab, S. (2008). Stroke-induced sudden-autonomic death: Areas of fatality beyond the insula. Stroke 39, 2421-2422.
18. Hilz, M.J., Marthol, H., Schwab, S., Kolodny, E.H., Brys, M., Stemper, B. (2010). Enzyme replacement therapy improves cardiovascular responses to orthostatic challenge in Fabry patients. J. Hypertens. 28, 1438-1448.
19. Holm, L., Cassidy, J.D., Carroll, L.J., and Borg, J. (2005). Summary of the WHO Collaborating Centre for Neurotrauma Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. 37, 137-141.
20. Honzikova, N., Semrad, B., Fiser, B., and Labrova, R. (2000). Baroreflex sensitivity determined by spectral method and heart rate variability, and two-years mortality in patients after myocardial infarction. Physiol. Res. 49, 643-650.
21. Huang, M., Theilmann, R.J., Robb, A., Angeles, A., Nichols, S., Drake, A., Dandrea, J., Levy, M., Holland, M., Song, T., Ge, S., Hwang, E., Yoo, K., Cui, L., Baker, D.G., Trauner, D., Coimbra, R., and Lee, R.R. (2009). Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J. Neurotrauma 26, 1213-1226.
22. Huikuri, H.V., Makikallio, T., Airaksinen, K.E., Mitrani, R., Castellanos, A., and Myerburg, R.J. (1999). Measurement of heart rate variability: A clinical tool or a research toy? J. Am. Coll. Cardiol 34, 1878-1883.
23. Johansson, M., Gao, S.A., Friberg, P., Annerstedt, M., Carlström, J., Ivarsson, T., Jensen, G., Ljungman, S., Mathillas, O., Nielsen, F.D., and Strömbom, U. (2007). Baroreflex effectiveness index and baroreflex sensitivity predict all-cause mortality and sudden death in hypertensive patients with chronic renal failure. J. Hypertens. 25, 163-168.
24. Krause, M., Rudiger, H., Bald, M., Nake, A., and Paditz, E. (2009). Autonomic blood pressure control in children and adolescents with type 1 diabetes mellitus. Pediatr. Diabetes 10, 255-263.
25. Lanfranchi, P.A., and Somers, V.K. (2002). Arterial baroreflex function and cardiovascular variability: Interactions and implications. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R815-R826.
26. La Rovere, M.T., Bigger, J.T.Jr., Marcus, F.I., Mortara, A., and Schwartz, P.J. (1998). Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351, 478-484.
27. La Rovere, M.T., Pinna, G.D., Hohnloser, S.H., Marcus, F.I., Mortara, A., Nohara, R., Bigger, J.T., Jr., Camm, A.J., and Schwartz, P.J. (2001). Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: Implications for clinical trials. Circulation 103, 2072-2077.
28. Levine, B., Kovacevic, N., Nica, E.I., Cheung, G., Gao, F., Schwartz, M.L., and Black, S.E. (2008). The Toronto traumatic brain injury study: Injury severity and quantified MRI. Neurology 70, 771-778.
29. Malliani, A., Pagani, M., Lombardi, F., and Cerutti, S. (1991). Cardiovascular neural regulation explored in the frequency domain. Circulation 84, 482-492.
30. McMillan, T.M., and Teasdale, G.M. (2007). Death rate is increased for at least 7 years after head injury: A prospective study. Brain 130, 2520-2527.
31. McMillan, T.M., Teasdale, G.M., Weir, C.J., and Stewart, E. (2011). Death after head injury: The 13 year outcome of a case control study. J. Neurol. Neurosurg. Psychiatr. Jan 31. [Epub ahead of print].
32. Natelson, B.H., and Chang, Q. (1993). Sudden death. A neurocardiologic phenomenon. Neurol. Clin. 11, 293-308.
33. National Institute of Neurological Disorders and Stroke. (2002) Traumatic Brain Injury: Hope Through Research (NIH Publication No.: 02-158). National Institutes of Health: Bethesda, MD.
34. Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R.A., Sarkar, R., Lee, H., Meeker, M., Zimmerman, R.D., Manley, G.T., and McCandliss, B.D. (2008). Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: A 3T diffusion tensor imaging study of mild traumatic brain injury. Am. J. Neuroradiol. 29, 967-973.
35. Novak, V., Novak, P., and Low, P.A. (1997). Time-frequency analysis of cardiovascular function and its clinical applications, in: Clinical Autonomic Disorders. P.A. Low (ed), Lippincott-Raven Publishers: Philadelphia, pps. 323-348.
36. Oppenheimer, S.M., Cechetto, D.F., and Hachinski, V.C. (1990). Cerebrogenic cardiac arrhythmias. Cerebral electrocardiographic influences and their role in sudden death. Arch. Neurol. 47, 513-519.
37. Oppenheimer, S.M., Wilson, J.X., Guiraudon, C., and Cechetto, D.F. (1991). Insular cortex stimulation produces lethal cardiac arrhythmias: A mechanism of sudden death? Brain Res. 550, 115-121.
38. Oppenheimer, S. (2006). Cerebrogenic cardiac arrhythmias: Cortical lateralization and clinical significance. Clin. Auton. Res. 16, 6-11.
39. Orlandi, G., Fanucchi, S., Strata, G., Pataleo, L., Landucci Pellegrini, L., Prontera, C., Martini, A., and Murri, L. (2000). Transient autonomic nervous system dysfunction during hyperacute stroke. Acta Neurol. Scand. 102, 317-321.
40. Ormezzano, O., Cracowski, J.L., Quesada, J.L., Pierre, H., Mallion, J.M., and Baguet, J.P. (2008). EVAluation of the prognostic value of BARoreflex sensitivity in hypertensive patients: The EVABAR study. J. Hypertens. 26, 1373-1378.
41. Pagani, M., Lombardi, F., Guzzetti, S., Rimoldi, O., Furlan, R., Pizzinelli, P., Sandrone, G., Malfatto, G., Dell'Orto, S., and Piccaluga, E. (1986). Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympathovagal interaction in man and conscious dog. Circ. Res. 59, 178-193.
42. Pagani, M., Somers, V., Furlan, R., Dell'Orto, S., Conway, J., Baselli, G., Cerutti, S., Sleight, P., and Malliani, A. (1988). Changes in autonomic regulation induced by physical training in mild hypertension. Hypertension 12, 600-610.
43. Parati, G., Di Rienzo, M., and Mancia, G. (2001). Dynamic modulation of baroreflex sensitivity in health and disease. Ann. N.Y. Acad. Sci 940, 469-487.
44. Rosengard-Bärlund, M., Bernardi, L., Fagerudd, J., Mäntysaari, M., Afbjörkesten, C.G., Lind-holm, H., Forsblom, C., Wadén, J., Groop, P.H., and FinnDiane Study Group. (2009). Early autonomic dysfunction in type 1 diabetes: A reversible disorder? Diabetologia 52, 1164-1172.
45. Rudiger, H., and Bald, M. (2001). Spontaneous baroreflex sensitivity in children and young adults calculated in the time and frequency domain. Auton. Neurosci. 93, 71-78.
46. Rutgers, D.R., Toulgoat, F., Cazejust, J., Fillard, P., Lasjaunias, P., and Ducreux, D. (2008). White matter abnormalities in mild traumatic brain injury: A diffusion tensor imaging study. Am. J. Neuroradiol. 29, 514-519.
47. Schwartz, P.J., and La Rovere, M.T. (1998). ATRAMI: A mark in the quest for the prognostic value of autonomic markers. Autonomic Tone and Reflexes After Myocardial Infarction. Eur. Heart. J. 19, 1593-1595.
48. Singer, D.H., and Ori, Z. (1995). Changes in heart rate variability associated with sudden cardiac death, in: Heart Rate Variability. M. Malik, and A.J. Camm (eds), Futura: Armonk, NY, pps. 429-448.
49. Sykora, M., Diedler, J., Rupp, A., Turcani, P., and Steiner, T. (2009). Impaired baroreceptor reflex sensitivity in acute stroke is associated with insular involvement, but not with carotid atherosclerosis. Stroke 40, 737-742.
50. Sykora, M., Diedler, J., Rupp, A., Turcani, P., Rocco, A., and Steiner, T. (2008). Impaired baroreflex sensitivity predicts outcome of acute intracerebral hemorrhage. Crit. Care Med. 36, 3074-3079.
51. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation 93, 1043-1065.
52. Tokgozoglu, S.L., Batur, M.K., Topuoglu, M.A., Saribas, O., Kes, S., and Oto, A. (1999). Effects of stroke localization on cardiac autonomic balance and sudden death. Stroke 30, 1307-1311.
53. Tsuji, H., Larson, M.G., Venditti, F.J.Jr., Manders, E.S., Evans, J.C., Feldman, C.L., and Levy, D. (1996). Impact of reduced heart rate variability on risk for cardiac events. The Framingham Heart Study. Circulation 94, 2850-2855.
54. Wieling, W., and Karemaker, J.M. (1999). Measurement of heart rate and blood pressure, in: Autonomic Failure, 4th ed. C.J. Mathias, and R. Bannister (eds), Oxford University Press: New York, pps. 197-210.
55. Wieling, W., and van Lieshout, J.J. (1997).Maintenance of postural normotension in humans, in: Clinical Autonomic Disorders. P.A. Low (ed), Lippincott-Raven: Philadelphia, pps. 73-82.