Int J Sports Med 2019; 40(13): 856-862
DOI: 10.1055/a-0958-9548
Clinical Sciences
© Georg Thieme Verlag KG Stuttgart · New York

MRI Brain Changes After Marathon Running: Results of the Berlin Beat of Running Study

Juliane Herm
1   Department of Neurology, Charité, Universitätsmedizin Berlin, Berlin, Germany
2   Center for Stroke Research, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Karl Georg Haeusler
3   Department of Neurology, Universitätsklinikum Würzburg, Würzburg, Germany
,
Claudia Kunze
2   Center for Stroke Research, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Matthias Krüll
4   SMS Medical Institute Berlin GmbH, Berlin, Germany
5   SCC EVENTS GmbH, Berlin, Germany
,
Lars Brechtel
6   Carl Remigius Medical School, Physician Assistance, Hamburg, Germany
7   Berlin Academy of Sports Medicine, Sports Medicine, Berlin, Germany
,
Jürgen Lock
4   SMS Medical Institute Berlin GmbH, Berlin, Germany
5   SCC EVENTS GmbH, Berlin, Germany
,
Peter U. Heuschmann
8   Institute of Clinical Epidemiology and Biometry, University of Würzburg, Würzburg, Germany
9   Clinical Trial Center Würzburg, University of Würzburg, Würzburg, Germany
10   Comprehensive Heart Failure Center, University of Würzburg, Würzburg, Germany
,
Wilhelm Haverkamp
11   Department of Cardiology, Charité Universitätsmedizin Berlin, Campus Virchow-Klinikum, Berlin, Germany
,
Hauke Heekeren
12   Department of Education and Psychology, Freie Universität Berlin, Berlin, Germany
,
Thomas Liman
1   Department of Neurology, Charité, Universitätsmedizin Berlin, Berlin, Germany
2   Center for Stroke Research, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Matthias Endres
1   Department of Neurology, Charité, Universitätsmedizin Berlin, Berlin, Germany
2   Center for Stroke Research, Charité Universitätsmedizin Berlin, Berlin, Germany
13   Charité Universitätsmedizin Berlin, German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany
14   Charité Universitätsmedizin Berlin, Excellence Cluster NeuroCure, Berlin, Germany
15   German Center for Cardiovascular Research (DZHK), Berlin, Germany
,
Jochen B. Fiebach*
2   Center for Stroke Research, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Gerhard Jan Jungehulsing*
16   Department of Neurology, Jüdisches Krankenhaus Berlin, Berlin, Germany
› Institutsangaben
Funding: The investigator-initiated Berlin Beat of Running Study was supported by the SCC EVENTS GmbH, Berlin and by an unrestricted study grant from Bayer HealthCare and Sanofi. The GETEMED AG (Teltow, Germany) provided the ECG-recorders and comprehensive technical support. KGH, JH, CK, JBF, ME and GJJ received funding from the Federal Ministry of Education and Research via the grant Center for Stroke Research Berlin (01 EO 0801). ME receives support from the Volkswagen-Stiftung. ME recieved funding from the German Research Foundation.

Clinical Trials Registrierung: clinicaltrials.gov NCT01428778
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Publikationsverlauf



accepted 04. Juni 2019

Publikationsdatum:
10. September 2019 (online)

Abstract

Several studies report neurological complications such as brain injury induced by ischemia or edema following exhaustive endurance sport. We aimed to detect the frequency of acute brain lesions after a marathon race. In the prospective observational Berlin Beat of Running study, 110 experienced endurance athletes underwent 3-Tesla brain MRI exams 2–3 days prior and within 2 days after a marathon run. MRI results were compared to an age- and sex-matched control group of 68 non-athletes, including the “Age-Related White Matter Changes” (ARWMC) scale to assess white matter lesions (WML) in the brain. 108 athletes (median age 48 years, 24% female, 8% with hypertension; 0% with diabetes) completed the race. No athlete reported neurological deficits, but a single acute ischemic lesion was detected in diffusion-weighted MRI after the race in one athlete. No other acute brain lesions compared to prior MRI were found. An ARWMC score ≥4 was found in 15% of athletes and 12% of non-athletic controls (p=0.7). Chronic ischemic lesions were not found in athletes but in four controls (6%) (p=0.02). In conclusion, acute ischemic brain lesions may be found in endurance runners. Every seventh endurance athlete and every ninth control showed evidence for substantial white matter lesions.

* Authors contributed equally.


 
  • References

  • 1 Chakravarty EF, Hubert HB, Lingala VB, Fries JF. Reduced disability and mortality among aging runners: A 21-year longitudinal study. Arch Intern Med 2008; 168: 1638-1646
  • 2 Mora S, Cook N, Buring JE, Ridker PM, Lee I-M. Physical activity and reduced risk of cardiovascular events: Potential mediating mechanisms. Circulation 2007; 116: 2110-2118
  • 3 Winzer BM, Whiteman DC, Reeves MM, Paratz JD. Physical activity and cancer prevention: A systematic review of clinical trials. Cancer Causes Control 2011; 22: 811-826
  • 4 Kim JH, Malhotra R, Chiampas G, D’Hemecourt P, Troyanos C, Cianca J, Smith RN, Wang TJ, Roberts WO, Thompson PD, Baggish AL. Cardiac arrest during long-distance running races. N Engl J Med 2012; 366: 130-140
  • 5 Schwabe K, Schwellnus M, Derman W, Swanevelder S, Jordaan E. Medical complications and deaths in 21 and 56 km road race runners: A 4-year prospective study in 65 865 runners–SAFER study I. Br J Sports Med 2014; 48: 912-918
  • 6 Ganesalingam J, Jenkins IH, Vaughan J. Running out of brain. J Sports Med Phys Fitness 2014; 54: 370-372
  • 7 Sellmann T, Noetges P. [Neurological deterioration following a marathon - atypical manifestation of basilar artery occlusion]. Anasthesiol Intensivmed Notfallmed Schmerzther 2010; 45: 708-711
  • 8 Turagam MK, Flaker GC, Velagapudi P, Vadali S, Alpert MA. Atrial fibrillation in athletes: Pathophysiology, clinical presentation, evaluation and management. J Atr Fibrillation 2015; 8: 1309
  • 9 Hanke AA, Staib A, Görlinger K, Perrey M, Dirkmann D, Kienbaum P. Whole blood coagulation and platelet activation in the athlete: A comparison of marathon, triathlon and long distance cycling. Eur J Med Res 2010; 15: 59-65
  • 10 Spormann R, Harding U, Stuhr M, Röther J, Püschel K, Reifferscheid F. [Serious complications following a marathon run: Interactive case report of a dramatic course]. Anasthesiol Intensivmed Notfallmed Schmerzther 2012; 47: 696-702
  • 11 Otto M, Holthusen S, Bahn E, Söhnchen 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
  • 12 Freund W, Faust S, Birklein F, Gaser C, Wunderlich AP, Müller M, Billich C, Juchems MS, Schmitz BL, Grön G, Schütz UH. Substantial and reversible brain gray matter reduction but no acute brain lesions in ultramarathon runners: Experience from the TransEurope-FootRace Project. BMC Med 2012; 10: 170
  • 13 Tremblay S, Henry LC, Bedetti C, Larson-Dupuis C, Gagnon J-F, Evans AC, Théoret H, Lassonde M, Beaumont De L. Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain 2014; 137: 2997-3011
  • 14 Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: Systematic review and meta-analysis. BMJ 2010; 341: c3666
  • 15 Smith EE, Saposnik G, Biessels GJ, Doubal FN, Fornage M, Gorelick PB, Greenberg SM, Higashida RT, Kasner SE, Seshadri S. American Heart Association Stroke Council. Council on Cardiovascular Radiology and Intervention. Council on Functional Genomics and Translational Biology and Council on Hypertension. Prevention of stroke in patients with silent cerebrovascular disease: A scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2017; 48: e44-e71
  • 16 Herm J, Töpper A, Wutzler A, Kunze C, Krüll M, Brechtel L, Lock J, Fiebach JB, Heuschmann PU, Haverkamp W, Endres M, Jungehulsing GJ, Haeusler KG. Frequency of exercise-induced ST-T-segment deviations and cardiac arrhythmias in recreational endurance athletes during a marathon race: Results of the prospective observational Berlin Beat of Running study. BMJ Open 2017; 7: e015798
  • 17 Haeusler KG, Herm J, Kunze C, Krüll M, Brechtel L, Lock J, Hohenhaus M, Heuschmann PU, Fiebach JB, Haverkamp W, Endres M, Jungehulsing GJ. Rate of cardiac arrhythmias and silent brain lesions in experienced marathon runners: Rationale, design and baseline data of the Berlin Beat of Running study. BMC Cardiovasc Disord 2012; 12: 69
  • 18 Aust S, Alkan Härtwig E, Koelsch S, Heekeren HR, Heuser I, Bajbouj M. How emotional abilities modulate the influence of early life stress on hippocampal functioning. Soc Cogn Affect Neurosci 2014; 9: 1038-1045
  • 19 Kliemann D, Dziobek I, Hatri A, Baudewig J, Heekeren HR. The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders. J Neurosci 2012; 32: 9469-9476
  • 20 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sport Med 2017; 38: 1126-1131
  • 21 Launer LJ. Epidemiology of white matter lesions. Top Magn Reson Imaging 2004; 15: 365-367
  • 22 Grosse-Dresselhaus F, Galinovic I, Villringer K, Audebert HJ, Fiebach JB. Difficulty of MRI based identification of lesion age by acute infra-tentorial ischemic stroke. PLoS One 2014; 9: e92868
  • 23 Thomalla G, Cheng B, Ebinger M, Hao Q, Tourdias T, Wu O, Kim JS, Breuer L, Singer OC, Warach S, Christensen S, Treszl A, Forkert ND, Galinovic I, Rosenkranz M, Engelhorn T, Köhrmann M, Endres M, Kang D-W, Dousset V, Sorensen AG, Liebeskind DS, Fiebach JB, Fiehler J, Gerloff C. STIR and VISTA Imaging Investigators. DWI-FLAIR mismatch for the identification of patients with acute ischaemic stroke within 4–5 h of symptom onset (PRE-FLAIR): A multicentre observational study. Lancet Neurol 2011; 10: 978-986
  • 24 Calvo N, Brugada J, Sitges M, Mont L. Atrial fibrillation and atrial flutter in athletes. Br J Sports Med 2012; 46 (Suppl. 01) i37-i43
  • 25 Sorokin AV, Araujo CGS, Zweibel S, Thompson PD. Atrial fibrillation in endurance-trained athletes. Br J Sports Med 2011; 45: 185-188
  • 26 Wehrens XHT, Chiang DY, Li N. Chronic exercise: A contributing factor to atrial fibrillation?. J Am Coll Cardiol 2013; 62: 78-80
  • 27 Wilhelm M, Roten L, Tanner H, Schmid J-P, Wilhelm I, Saner H. Long-term cardiac remodeling and arrhythmias in nonelite marathon runners. Am J Cardiol 2012; 110: 129-135
  • 28 Nieuwlaat R, Prins MH, Le Heuzey J-Y, Vardas PE, Aliot E, Santini M, Cobbe SM, Widdershoven JWMG, Baur LH, Lévy S, Crijns HJGM. Prognosis, disease progression, and treatment of atrial fibrillation patients during 1 year: Follow-up of the Euro Heart Survey on atrial fibrillation. Eur Heart J 2008; 29: 1181-1189
  • 29 Batool S, O’Donnell M, Sharma M, Islam S, Dagenais GR, Poirier P, Lear SA, Wielgosz A, Teo K, Stotts G, McCreary CR, Frayne R, DeJesus J, Rangarajan S, Yusuf S, Smith EE. PURE Study Investigators. Incidental magnetic resonance diffusion-weighted imaging-positive lesions are rare in neurologically asymptomatic community-dwelling adults. Stroke 2014; 45: 2115-2117
  • 30 Saini M, Suministrado MSP, Hilal S, Dong YH, Venketasubramanian N, Ikram MK, Chen C. Prevalence and risk factors of acute incidental infarcts. Stroke 2015; 46: 2722-2727
  • 31 Yamada K, Nagakane Y, Sasajima H, Nakagawa M, Mineura K, Masunami T, Akazawa K, Nishimura T. Incidental acute infarcts identified on diffusion-weighted images: A university hospital-based study. Am J Neuroradiol 2008; 29: 937-940
  • 32 Steinicke R, Gaertner B, Grittner U, Schmidt W, Dichgans M, Heuschmann PU, Tanislav C, Putaala J, Kaps M, Endres M, Schmidt R, Fazekas F, Norrving B, Rolfs A, Martus P, Tatlisumak T, Enzinger C, Jungehulsing GJ. Kidney function and white matter disease in young stroke patients: Analysis of the stroke in young fabry patients study population. Stroke 2012; 43: 2382-2388
  • 33 Hopkins RO, Beck CJ, Burnett DL, Weaver LK, Victoroff J, Bigler ED. Prevalence of white matter hyperintensities in a young healthy population. J Neuroimaging 2006; 16: 243-251
  • 34 Albach FN, Brunecker P, Usnich T, Villringer K, Ebinger M, Fiebach JB, Nolte CH. Complete early reversal of diffusion-weighted imaging hyperintensities after ischemic stroke is mainly limited to small embolic lesions. Stroke 2013; 44: 1043-1048
  • 35 Fiehler J, Knudsen K, Kucinski T, Kidwell CS, Alger JR, Thomalla G, Eckert B, Wittkugel O, Weiller C, Zeumer H, Röther J. Predictors of apparent diffusion coefficient normalization in stroke patients. Stroke 2004; 35: 514-519