Association between Muscle Damage and Head Impacts in High School American Football

Abstract

Subconcussive head impacts (SHI), defined as impacts to the cranium that do not result in concussion symptoms, are gaining traction as a major public health concern. The contribution of physiological factors such as physical exertion and muscle damage to SHI-dependent changes in neurological measures remains unknown. A prospective longitudinal study examined the association between physiological factors and SHI kinematics in 15 high school American football players over one season. Players wore a sensor-installed mouthguard for all practices and games, recording frequency and magnitude of all head impacts. Serum samples were collected at 12 time points (pre-season, pre- and post-game for five in-season games, and post-season) and were assessed for an isoenzyme of creatine kinase (CK-MM) primarily found in skeletal muscle. Physical exertion was estimated in the form of excess post-exercise oxygen consumption (EPOC) from heart rate data captured during the five games. Mixed-effect regression models indicated that head impact kinematics were significantly and positively associated with change in CK-MM but not EPOC. There was a significant and positive association between CK-MM and EPOC. These data suggest that when examining SHI, effects of skeletal muscle damage should be considered when using outcome measures that may have an interaction with muscle damage.

Key words

exercise physiology - subconcussive head impacts, creatine kinase

• References

• 1 Bailes JE, Petraglia AL, Omalu BI, Nauman E, Talavage T. Role of subconcussion in repetitive mild traumatic brain injury. J Neurosurg 2013; 119: 1235-1245
• 2 Montenigro PH, Alosco ML, Martin BM, Daneshvar DH, Mez J, Chaisson CE, Nowinski CJ, Au R, McKee AC, Cantu RC, McClean MD, Stern RA, Tripodis Y. Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players. J Neurotrauma 2017; 34: 328-340
• 3 Lipton ML, Kim N, Zimmerman ME, Kim M, Stewart WF, Branch CA, Lipton RB. Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 2013; 268: 850-857
• 4 McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, Lee HS, Wojtowicz SM, Hall G, Baugh CM, Riley DO, Kubilus CA, Cormier KA, Jacobs MA, Martin BR, Abraham CR, Ikezu T, Reichard RR, Wolozin BL, Budson AE, Goldstein LE, Kowall NW, Cantu RC. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013; 136: 43-64
• 5 Mez J, Daneshvar DH, Kiernan PT, Abdolmohammadi B, Alvarez VE, Huber BR, Alosco ML, Solomon TM, Nowinski CJ, McHale L, Cormier KA, Kubilus CA, Martin BM, Murphy L, Baugh CM, Montenigro PH, Chaisson CE, Tripodis Y, Kowall NW, Weuve J, McClean MD, Cantu RC, Goldstein LE, Katz DI, Stern RA, Stein TD, McKee AC. Clinicopathological evaluation of chronic traumatic encephalopathy in players of American Football. JAMA 2017; 318: 360-370
• 6 Caccese JB, Best C, Lamond LC, DiFabio M, Kaminski TW, Watson D, Getchell N, Buckley TA. Effects of repetitive head impacts on a concussion assessment battery. Med Sci Sports Exerc 2019; 51: 1355-1361
• 7 Gysland SM, Mihalik JP, Register-Mihalik JK, Trulock SC, Shields EW, Guskiewicz KM. The relationship between subconcussive impacts and concussion history on clinical measures of neurologic function in collegiate football players. Ann Biomed Eng 2012; 40: 14-22
• 8 McAllister TW, Flashman LA, Maerlender A, Greenwald RM, Beckwith JG, Tosteson TD, Crisco JJ, Brolinson PG, Duma SM, Duhaime AC, Grove MR, Turco JH. Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes. Neurology 2012; 78: 1777-1784
• 9 Hwang S, Ma L, Kawata K, Tierney R, Jeka JJ. Vestibular dysfunction after subconcussive head impact. J Neurotrauma 2017; 34: 8-15
• 10 Kawata K, Rubin LH, Lee JH, Sim T, Takahagi M, Szwanki V, Bellamy A, Darvish K, Assari S, Henderer JD, Tierney R, Langford D. Association of football subconcussive head impacts with ocular near point of convergence. JAMA Ophthalmol 2016; 134: 763-769
• 11 Kawata K, Tierney R, Phillips J, Jeka JJ. Effect of Repetitive Sub-concussive head impacts on ocular near point of convergence. Int J Sports Med 2016; 37: 405-410
• 12 Zonner SW, Ejima K, Fulgar CC, Charleston CN, Huibregtse ME, Bevilacqua ZW, Kawata K. Oculomotor response to cumulative subconcussive head impacts in US High School Football Players: A pilot longitudinal study. JAMA Ophthalmol 2019; 137: 265-270
• 13 Kawata K, Rubin LH, Takahagi M, Lee JH, Sim T, Szwanki V, Bellamy A, Tierney R, Langford D. Subconcussive impact-dependent increase in plasma S100beta levels in collegiate football players. J Neurotrauma 2017; 34: 2254-2260
• 14 Oliver JM, Jones MT, Kirk KM, Gable DA, Repshas JT, Johnson TA, Andreasson U, Norgren N, Blennow K, Zetterberg H. Serum neurofilament Light in american Football Athletes over the course of a season. J Neurotrauma 2016; 33: 1784-1789
• 15 Zonner SW, Ejima K, Bevilacqua ZW, Huibregtse ME, Charleston C, Fulgar C, Kawata K. Association of increased serum S100B levels with high school football subconcussive head impacts. Front Neurol 2019; 10: 327
• 16 Bahrami N, Sharma D, Rosenthal S, Davenport EM, Urban JE, Wagner B, Jung Y, Vaughan CG, Gioia GA, Stitzel JD, Whitlow CT, Maldjian JA. Subconcussive head impact exposure and white matter tract changes over a single season of youth football. Radiology 2016; 281: 919-926
• 17 Slobounov SM, Walter A, Breiter HC, Zhu DC, Bai X, Bream T, Seidenberg P, Mao X, Johnson B, Talavage TM. The effect of repetitive subconcussive collisions on brain integrity in collegiate football players over a single football season: A multi-modal neuroimaging study. Neuroimage Clin 2017; 14: 708-718
• 18 Di Battista AP, Rhind SG, Richards D, Churchill N, Baker AJ, Hutchison MG. Altered blood biomarker profiles in athletes with a history of repetitive head impacts. PLoS One 2016; 11: e0159929
• 19 Shahim P, Tegner Y, Wilson DH, Randall J, Skillback T, Pazooki D, Kallberg B, Blennow K, Zetterberg H. Blood biomarkers for brain injury in concussed professional ice hockey players. JAMA Neurol 2014; 71: 684-692
• 20 Gill J, Merchant-Borna K, Jeromin A, Livingston W, Bazarian J. Acute plasma tau relates to prolonged return to play after concussion. Neurology 2017; 88: 595-602
• 21 Shahim P, Zetterberg H, Tegner Y, Blennow K. Serum neurofilament light as a biomarker for mild traumatic brain injury in contact sports. Neurology 2017; 88: 1788-1794
• 22 Marchi N, Bazarian JJ, Puvenna V, Janigro M, Ghosh C, Zhong J, Zhu T, Blackman E, Stewart D, Ellis J, Butler R, Janigro D. Consequences of repeated blood-brain barrier disruption in football players. PLoS One 2013; 8: e56805
• 23 Abd-Elfattah HM, Abdelazeim FH, Elshennawy S. Physical and cognitive consequences of fatigue: A review. J Adv Res 2015; 6: 351-358
• 24 Anderson RE, Hansson LO, Nilsson O, Dijlai-Merzoug R, Settergren G. High serum S100B levels for trauma patients without head injuries. Neurosurgery 2001; 48: 1255-1258
• 25 Otto M, Holthusen S, Bahn E, Sohnchen N, Wiltfang J, Geese R, Fischer A, Reimers CD. Boxing and running lead to a rise in serum levels of S-100B protein. Int J Sports Med 2000; 21: 551-555
• 26 Khan MA, Moiz JA, Raza S, Verma S, Shareef MY, Anwer S, Alghadir A. Physical and balance performance following exercise induced muscle damage in male soccer players. J Phys Ther Sci 2016; 28: 2942-2949
• 27 Borsheim E, Bahr R. Effect of exercise intensity, duration and mode on post-exercise oxygen consumption. Sports Med 2003; 33: 1037-1060
• 28 Wallimann T, Schlosser T, Eppenberger HM. Function of M-line-bound creatine kinase as intramyofibrillar ATP regenerator at the receiving end of the phosphorylcreatine shuttle in muscle. J Biol Chem 1984; 259: 5238-5246
• 29 Baird MF, Graham SM, Baker JS, Bickerstaff GF. Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J Nutr Metab 2012; 2012: 960363
• 30 Friden J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand 2001; 171: 321-326
• 31 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2020 update.. Int J Sports Med 2019; 40: 813-817
• 32 Wu LC, Nangia V, Bui K, Hammoor B, Kurt M, Hernandez F, Kuo C, Camarillo DB. In vivo evaluation of wearable head impact sensors. Ann Biomed Eng 2016; 44: 1234-1245
• 33 Smolander J, Ajoviita M, Juuti T, Nummela A, Rusko H. Estimating oxygen consumption from heart rate and heart rate variability without individual calibration. Clin Physiol Funct Imaging 2011; 31: 266-271
• 34 Gaesser GA, Brooks GA. Metabolic bases of excess post-exercise oxygen consumption: A review. Med Sci Sports Exerc 1984; 16: 29-43
• 35 Broglio SP, Eckner JT, Martini D, Sosnoff JJ, Kutcher JS, Randolph C. Cumulative head impact burden in high school football. J Neurotrauma 2011; 28: 2069-2078
• 36 Broglio SP, Williams RM, O’Connor KL, Goldstick J. Football Players’ head-impact exposure after limiting of full-contact practices. J Athl Train 2016; 51: 511-518
• 37 Urban JE, Davenport EM, Golman AJ, Maldjian JA, Whitlow CT, Powers AK, Stitzel JD. Head impact exposure in youth football: High school ages 14 to 18 years and cumulative impact analysis. Ann Biomed Eng 2013; 41: 2474-2487
• 38 Brancaccio P, Maffulli N, Limongelli FM. Creatine kinase monitoring in sport medicine. Br Med Bull 2007; 81-82 209-230
• 39 Hoffman JR, Maresh CM, Newton RU, Rubin MR, French DN, Volek JS, Sutherland J, Robertson M, Gomez AL, Ratamess NA, Kang J, Kraemer WJ. Performance, biochemical, and endocrine changes during a competitive football game. Med Sci Sports Exerc 2002; 34: 1845-1853
• 40 Lang H, Wurzburg U. Creatine kinase, an enzyme of many forms. Clin Chem 1982; 28: 1439-1447
• 41 Stone JD, Kreutzer A, Mata JD, Nystrom MG, Jagim AR, Jones MT, Oliver JM. Changes in creatine kinase and hormones over the course of an American Football Season. J Strength Cond Res 2019; 33: 2481-2487
• 42 Kraemer WJ, Looney DP, Martin GJ, Ratamess NA, Vingren JL, French DN, Hatfield DL, Fragala MS, Spiering BA, Howard RL, Cortis C, Szivak TK, Comstock BA, Dunn-Lewis C, Hooper DR, Flanagan SD, Volek JS, Anderson JM, Maresh CM, Fleck SJ. Changes in creatine kinase and cortisol in National Collegiate Athletic Association Division I American football players during a season. J Strength Cond Res 2013; 27: 434-441
• 43 Hoffman JR, Kang J, Ratamess NA, Faigenbaum AD. Biochemical and hormonal responses during an intercollegiate football season. Med Sci Sports Exerc 2005; 37: 1237-1241
• 44 Gleason BH, Sams ML, Salley JT, Pustina AA, Stone MH. global positioning system analysis of a high school football scrimmage. J Strength Cond Res 2017; 31: 2183-2188
• 45 Godek SF, Bartolozzi AR, Godek JJ. Sweat rate and fluid turnover in American football players compared with runners in a hot and humid environment. Br J Sports Med 2005; 39: 205-211
• 46 Pincivero DM, Bompa TO. A physiological review of American football. Sports Med 1997; 23: 247-260
• 47 Iosia MF, Bishop PA. Analysis of exercise-to-rest ratios during division IA televised football competition. J Strength Cond Res 2008; 22: 332-340
• 48 Rhea MR, Hunter RL, Hunter TJ. Competition modeling of American football: Observational data and implications for high school, collegiate, and professional player conditioning. J Strength Cond Res 2006; 20: 58-61
• 49 Camarillo DB, Shull PB, Mattson J, Shultz R, Garza D. An instrumented mouthguard for measuring linear and angular head impact kinematics in American football. Ann Biomed Eng 2013; 41: 1939-1949
• 50 Kendall B, Eston R. Exercise-induced muscle damage and the potential protective role of estrogen. Sports Med 2002; 32: 103-123
• 51 Shumate JB, Brooke MH, Carroll JE, Davis JE. Increased serum creatine kinase after exercise: A sex-linked phenomenon. Neurology 1979; 29: 902-904