Substantial and reversible brain gray matter reduction but no acute brain lesions in ultramarathon runners: Experience from the TransEurope-FootRace Project

BMC Medicine

Volumn 10, Issue , 2012, Pages

  Freund, Wolfgang ^a   Faust, Sonja ^a   Birklein, Frank ^b   Gaser, Christian ^c   Wunderlich, Arthur P ^a   Müller, Marguerite ^a   Billich, Christian ^a   Juchems, Markus S ^a   Schmitz, Bernd L ^a   Grön, Georg ^a   Schütz, Uwe H ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Body weight; Brain volume; Catabolism; DWI; Lesion; MRI; Ultramarathon

Indexed keywords

ADULT; ARTICLE; BODY WEIGHT; BRAIN SIZE; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; FLUID ATTENUATED INVERSION RECOVERY; FOLLOW UP; GRAY MATTER; HUMAN; MALE; MARATHON RUNNER; NEUROPHYSIOLOGY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; UNIVERSITY HOSPITAL;

ADULT; AGED; BRAIN; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; ORGAN SIZE; PROSPECTIVE STUDIES; RUNNING;

EID: 84871370696     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-10-170     Document Type: Article

References (57)

1. Schulze I. TransEurope-FootRace 2009. Bari-Nordkap - 4.487,7 km in 64 Tagesetappen 2010, Leipzig, Germany: Engelsdorfer Verlag.
2. Schuetz UH, Schmidt-Trucksäss A, Knechtle B, Machann J, Wiedelbach H, Erhardt M, Freund W, Gröninger S, Brunner H, Schulze I, Brambs HJ, Billich C. The Transeurope Footrace Project: longitudinal data acquisition in a cluster randomized mobile MRI observational cohort study on 44 endurance runners at a 64-stage 4,486km transcontinental ultramarathon. BMC Med 2012, 10:78. 10.1186/1741-7015-10-78, 3409063, 22812450.
3. Almond CS, Shin AY, Fortescue EB, Mannix RC, Wypij D, Binstadt BA, Duncan CN, Olson DP, Salerno AE, Newburger JW, Greenes DS. Hyponatremia among runners in the Boston Marathon. N Engl J Med 2005, 352:1550-1556. 10.1056/NEJMoa043901, 15829535.
4. Levine BD, Thompson PD. Marathon maladies. N Engl J Med 2005, 352:1516-1518. 10.1056/NEJMp058043, 15829532.
5. Noakes TD, Sharwood K, Speedy D, Hew T, Reid S, Dugas J, Almond C, Wharam P, Weschler L. Three independent biological mechanisms cause exercise-associated hyponatremia: evidence from 2,135 weighed competitive athletic performances. Proc Natl Acad Sci USA 2005, 102:18550-18555. 10.1073/pnas.0509096102, 1311740, 16344476.
6. Kashyap AS, Anand KP, Kashyap S. Sudden collapse of a young female cross country runner. Br J Sports Med 2006, 40:e11. 10.1136/bjsm.2005.020446, 2577555, 16556775.
7. Ayus JC, Varon J, Arieff AI. Hyponatremia, cerebral edema, and noncardiogenic pulmonary edema in marathon runners. Ann Intern Med 2000, 132:711-714.
8. Ayus JC. Sodium and potassium disorders. Textbook of critical care 2000, 853-861. Philadelphia, PA: WB Saunders, Shoemaker WC.
9. Bailey DM, Bartsch P, Knauth M, Baumgartner RW. Emerging concepts in acute mountain sickness and high-altitude cerebral edema: from the molecular to the morphological. Cell Mol Life Sci 2009, 66:3583-3594. 10.1007/s00018-009-0145-9, 3085779, 19763397.
10. Decker DA, Falchook AD, Yachnis AT, Waters MF. Radiographic and pathologic findings in an atypical brainstem variant of reversible posterior leukoencephalopathy syndrome. Neurologist 2009, 15:364-366. 10.1097/NRL.0b013e3181951ac7, 19901722.
11. Bartynski WS. Posterior reversible encephalopathy syndrome, part 1: fundamental imaging and clinical features. AJNR Am J Neuroradiol 2008, 29:1036-1042. 10.3174/ajnr.A0928, 18356474.
12. Bartynski WS. Posterior reversible encephalopathy syndrome, part 2: controversies surrounding pathophysiology of vasogenic edema. AJNR Am J Neuroradiol 2008, 29:1043-1049. 10.3174/ajnr.A0929, 18403560.
13. Scobie BA. Gastrointestinal emergencies with marathon-type running: omental infarction with pancreatitis and liver failure with portal vein thrombosis. N Z Med J 1998, 111:211-212.
14. Holman ND, Schneider AJ. Multi-organ damage in exertional heat stroke. Neth J Med 1989, 35:38-43.
15. Slavich G, Poser S, Antonutto G, Fregolent R, Piccoli G, Enrico di Prampero P. Prolonged nocturnal asystole and cerebral neurogliosis in a marathon runner. J Cardiovasc Med 2011, 12:901-903.
16. Pantoni L. Leukoaraiosis: from an ancient term to an actual marker of poor prognosis. Stroke 2008, 39:1401-1403. 10.1161/STROKEAHA.107.505602, 18340098.
17. van Straaten EC, Fazekas F, Rostrup E, Scheltens P, Schmidt R, Pantoni L, Inzitari D, Waldemar G, Erkinjuntti T, Mantyla R, Wahlund LO, Barkhof F. Impact of white matter hyperintensities scoring method on correlations with clinical data: the LADIS study. Stroke 2006, 37:836-840. 10.1161/01.STR.0000202585.26325.74, 16439704.
18. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36. 10.1006/nimg.2001.0786, 11525331.
19. Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Markesbery WR. Age and gender effects on human brain anatomy: a voxel-based morphometric study in healthy elderly. Neurobiol Aging 2007, 28:1075-1087. 10.1016/j.neurobiolaging.2006.05.018, 16774798.
20. O'Brien JT, Paling S, Barber R, Williams ED, Ballard C, McKeith IG, Gholkar A, Crum WR, Rossor MN, Fox NC. Progressive brain atrophy on serial MRI in dementia with Lewy bodies, AD, and vascular dementia. Neurology 2001, 56:1386-1388. 10.1212/WNL.56.10.1386, 11376193.
21. Fox NC, Crum WR, Scahill RI, Stevens JM, Janssen JC, Rossor MN. Imaging of onset and progression of Alzheimer's disease with voxel-compression mapping of serial magnetic resonance images. Lancet 2001, 358:201-205. 10.1016/S0140-6736(01)05408-3, 11476837.
22. Rudick RA, Fisher E, Lee JC, Simon J, Jacobs L. Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 1999, 53:1698-1704. 10.1212/WNL.53.8.1698, 10563615.
23. Tabrizi SJ, Scahill RI, Durr A, Roos RA, Leavitt BR, Jones R, Landwehrmeyer GB, Fox NC, Johnson H, Hicks SL, Kennard C, Craufurd D, Frost C, Langbehn DR, Reilmann R, Stout JC. Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol 2011, 10:31-42. 10.1016/S1474-4422(10)70276-3, 21130037.
24. Katzman DK, Lambe EK, Mikulis DJ, Ridgley JN, Goldbloom DS, Zipursky RB. Cerebral gray matter and white matter volume deficits in adolescent girls with anorexia nervosa. J Pediatr 1996, 129:794-803. 10.1016/S0022-3476(96)70021-5, 8969719.
25. Gunston GD, Burkimsher D, Malan H, Sive AA. Reversible cerebral shrinkage in kwashiorkor: an MRI study. Arch Dis Child 1992, 67:1030-1032. 10.1136/adc.67.8.1030, 1793595, 1520007.
26. Geibprasert S, Gallucci M, Krings T. Alcohol-induced changes in the brain as assessed by MRI and CT. Eur Radiol 2010, 20:1492-1501. 10.1007/s00330-009-1668-z, 19997850.
27. Swayze VW, Andersen AE, Andreasen NC, Arndt S, Sato Y, Ziebell S. Brain tissue volume segmentation in patients with anorexia nervosa before and after weight normalization. Int J Eat Disord 2003, 33:33-44. 10.1002/eat.10111, 12474197.
28. Golden NH, Ashtari M, Kohn MR, Patel M, Jacobson MS, Fletcher A, Shenker IR. Reversibility of cerebral ventricular enlargement in anorexia nervosa, demonstrated by quantitative magnetic resonance imaging. J Pediatr 1996, 128:296-301. 10.1016/S0022-3476(96)70414-6, 8636835.
29. Castro-Fornieles J, Bargallo N, Lazaro L, Andres S, Falcon C, Plana MT, Junque C. A cross-sectional and follow-up voxel-based morphometric MRI study in adolescent anorexia nervosa. J Psychiatr Res 2009, 43:331-340. 10.1016/j.jpsychires.2008.03.013, 18486147.
30. Knudsen L, Drummond PD. Cold-induced limb pain decreases sensitivity to pressure-pain sensations in the ipsilateral forehead. Eur J Pain 2009, 13:1023-1029. 10.1016/j.ejpain.2008.12.005, 19171493.
31. Van den Eynde F, Treasure J. Neuroimaging in eating disorders and obesity: implications for research. Child Adolesc Psychiatr Clin N Am 2009, 18:95-115. 10.1016/j.chc.2008.07.016, 19014860.
32. Reimers CD, Knapp G, Tettenborn B. Impact of Physical Activity on Cognition. Can Physical Activity Prevent Dementia?. Aktuelle Neurologie 2012, 39:276-291.
33. Knechtle B, Duff B, Schulze I, Kohler G. A multi-stage ultra-endurance run over 1,200 km leads to a continuous accumulation of total body water. J Sports Sci Med 2008, 7:356-364.
34. Knechtle B, Knechtle P, Schuck R, Andonie JL, Kohler G. Effects of a Deca Iron Triathlon on body composition: a case study. Int J Sports Med 2008, 29:343-351. 10.1055/s-2007-965354, 17879892.
35. Knechtle B, Salas Fraire O, Andonie JL, Kohler G. Effect of a multistage ultra-endurance triathlon on body composition: World Challenge Deca Iron Triathlon 2006. Br J Sports Med 2008, 42:121-125.
36. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986, 1:307-310.
37. Jepsen JR, Laursen LH, Hagert CG, Kreiner S, Larsen AI. Diagnostic accuracy of the neurological upper limb examination I: inter-rater reproducibility of selected findings and patterns. BMC Neurol 2006, 6:8. 10.1186/1471-2377-6-8, 1402320, 16483371.
38. Portney LG, Watkins MP. Correlations. Foundations of Clinical Research: Applications to Practice 2000, 23:491-508. Upper Saddle River, NJ: Prentice Hall Health.
39. FIL Methods Group SPM 8. FIL Methods Group., http://www.fil.ion.ucl.ac.uk/spm/software/spm8/
40. Structural Brain Mapping Group VBM8 Toolbox. Structural Brain Mapping Group., http://dbm.neuro.uni-jena.de/vbm/download/
41. Tohka J, Zijdenbos A, Evans A. Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 2004, 23:84-97. 10.1016/j.neuroimage.2004.05.007, 15325355.
42. Kappos L, Traboulsee A, Constantinescu C, Eralinna JP, Forrestal F, Jongen P, Pollard J, Sandberg-Wollheim M, Sindic C, Stubinski B, Uitdehaag B, Li D. Long-term subcutaneous interferon beta-1a therapy in patients with relapsing-remitting MS. Neurology 2006, 67:944-953. 10.1212/01.wnl.0000237994.95410.ce, 17000959.
43. Zivadinov R, Reder AT, Filippi M, Minagar A, Stuve O, Lassmann H, Racke MK, Dwyer MG, Frohman EM, Khan O. Mechanisms of action of disease-modifying agents and brain volume changes in multiple sclerosis. Neurology 2008, 71:136-144. 10.1212/01.wnl.0000316810.01120.05, 18606968.
44. Jagust WJ, Noseworthy JH. Brain atrophy as a surrogate marker in MS: faster, simpler, better?. Neurology 2000, 54:782-783. 10.1212/WNL.54.4.782, 10690960.
45. Bourdeau I, Bard C, Noel B, Leclerc I, Cordeau MP, Belair M, Lesage J, Lafontaine L, Lacroix A. Loss of brain volume in endogenous Cushing's syndrome and its reversibility after correction of hypercortisolism. J Clin Endocrinol Metabol 2002, 87:1949-1954.
46. Enqvist JK, Mattsson CM, Johansson PH, Brink-Elfegoun T, Bakkman L, Ekblom BT. Energy turnover during 24 hours and 6 days of adventure racing. J Sports Sci 2010, 28:947-955. 10.1080/02640411003734069, 20544486.
47. Herbst L, Knechtle B, Lopez CL, Andonie JL, Fraire OS, Kohler G, Rust CA, Rosemann T. Pacing strategy and change in body composition during a deca iron triathlon. Chinese J Physiol 2011, 54:255-263.
48. Peters A, Schweiger U, Pellerin L, Hubold C, Oltmanns KM, Conrad M, Schultes B, Born J, Fehm HL. The selfish brain: competition for energy resources. Neurosci Biobehav Rev 2004, 28:143-180. 10.1016/j.neubiorev.2004.03.002, 15172762.
49. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA, Schteingart DE. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol Psychiatry 1999, 46:1595-1602. 10.1016/S0006-3223(99)00203-6, 10624540.
50. Hew-Butler T, Noakes TD, Soldin SJ, Verbalis JG. Acute changes in endocrine and fluid balance markers during high-intensity, steady-state, and prolonged endurance running: unexpected increases in oxytocin and brain natriuretic peptide during exercise. Eur J Endocrinol 2008, 159:729-737. 10.1530/EJE-08-0064, 18794210.
51. Kraemer WJ, Fragala MS, Watson G, Volek JS, Rubin MR, French DN, Maresh CM, Vingren JL, Hatfield DL, Spiering BA, Yu-Ho J, Hughes SL, Case HS, Stuempfle KJ, Lehmann DR, Bailey S, Evans DS. Hormonal responses to a 160-km race across frozen Alaska. Br J Sports Med 2008, 42:116-120. discussion 120.
52. Duning T, Kloska S, Steinstrater O, Kugel H, Heindel W, Knecht S. Dehydration confounds the assessment of brain atrophy. Neurology 2005, 64:548-550. 10.1212/01.WNL.0000150542.16969.CC, 15699394.
53. Siegel AJ, Verbalis JG, Clement S, Mendelson JH, Mello NK, Adner M, Shirey T, Glowacki J, Lee-Lewandrowski E, Lewandrowski KB. Hyponatremia in marathon runners due to inappropriate arginine vasopressin secretion. Am J Med 2007, 120:461 e411-467.
54. Knechtle B, Knechtle P, Rust CA, Gnadinger M, Imoberdorf R, Kohler G, Rosemann T, Ballmer P. Regulation of electrolyte and fluid metabolism in multi-stage ultra-marathoners. Horm Metab Res 2012, 44:919-926.
55. Freund W, Billich C, Brambs HJ, Weber F, Schuetz UH. MRI changes of achilles tendon and hindfoot in experienced runners and beginners during training and after a (half)-marathon competition [in German]. Zeitschrift fur Orthopadie und Unfallchirurgie 2011, 149:407-417. 10.1055/s-0030-1271074, 21567363.
56. Rüst CA, Knechtle B, Knechtle P, Rosemann T. Similarities and differences in anthropometry and training between recreational male 100-km ultra-marathoners and marathoners. J Sports Sci 2012, 30:1249-1257. 10.1080/02640414.2012.697182, 22724447.
57. Knechtle B, Knechtle P, Rosemann T. Low prevalence of exercise-associated hyponatremia in male 100 km ultra-marathon runners in Switzerland. Eur J Appl Physiol 2011, 111:1007-1016.