Effects of endurance training on brain structures in chronic schizophrenia patients and healthy controls

Schizophrenia Research

Volumn 173, Issue 3, 2016, Pages 182-191

  Malchow, Berend ^a   Keeser, Daniel ^a   Keller, Katriona ^a,b   Hasan, Alkomiet ^a   Rauchmann, Boris Stephan ^a   Kimura, Hiroshi ^a,c   Schneider Axmann, Thomas ^a   Dechent, Peter ^b   Gruber, Oliver ^b   Ertl Wagner, Birgit ^a   Honer, William G ^d   Hillmer Vogel, Ursula ^b   Schmitt, Andrea ^a,e   Wobrock, Thomas ^b,f   Niklas, Andree ^b   Falkai, Peter ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c CHIBA UNIVERSITY   (Japan)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f Darmstadt Dieburg Clinics   (Germany)

Author keywords

Brain morphology; Endurance training; Longitudinal; Magnetic resonance imaging; Schizophrenia

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; BRAIN SIZE; CINGULATE GYRUS; COMORBIDITY; CONTROLLED STUDY; ENDURANCE TRAINING; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; INFERIOR TEMPORAL GYRUS; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MENTAL DISEASE; MIDDLE TEMPORAL GYRUS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; TEMPORAL CORTEX; VOXEL BASED MORPHOMETRY; CLINICAL TRIAL; COGNITIVE REMEDIATION THERAPY; COMPUTER ASSISTED THERAPY; DIAGNOSTIC IMAGING; ENDURANCE; EXERCISE; FOLLOW UP; KINESIOTHERAPY; ORGAN SIZE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; TREATMENT OUTCOME;

ADULT; COGNITIVE REMEDIATION; EXERCISE; EXERCISE THERAPY; FEMALE; FOLLOW-UP STUDIES; GRAY MATTER; HIPPOCAMPUS; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; PHYSICAL ENDURANCE; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; THERAPY, COMPUTER-ASSISTED; TREATMENT OUTCOME;

EID: 84922822260     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.01.005     Document Type: Article

References (66)

1. Andersson J.L.R., Jenkinson M., Smith S. Non-linear optimisation. FMRIB Technical Report TR07JA1 2007.
2. Andersson J.L.R., Jenkinson M., Smith S. Non-linear registration, aka Spatial normalisation. FMRIB Technical Report TR07JA2 2007.
3. Borg G. Perceived exertion as an indicator of somatic stress. Scand. J. Rehabil. Med. 1970, 2(2):92-98.
4. Cooper D., Barker V., Radua J., Fusar-Poli P., Lawrie S.M. Multimodal voxel-based meta-analysis of structural and functional magnetic resonance imaging studies in those at elevated genetic risk of developing schizophrenia. Psychiatry Res. 2014, 221(1):69-77.
5. DeLisi L.E., Sakuma M., Maurizio A.M., Relja M., Hoff A.L. Cerebral ventricular change over the first 10 years after the onset of schizophrenia. Psychiatry Res. 2004, 130(1):57-70.
6. Duvernoy H.M., Cattin F., Risold P.Y. The Human Hippocampus - Functional Anatomy, Vascularization and Serial Sections with MRI 2013, Springer, Heidelberg New York Dordrecht London. 4th ed.
7. Ellison-Wright I., Bullmore E. Anatomy of bipolar disorder and schizophrenia: a meta-analysis. Schizophr. Res. 2010, 117(1):1-12.
8. Erickson K.I., Kramer A.F. Aerobic exercise effects on cognitive and neural plasticity in older adults. Br. J. Sports Med. 2009, 43(1):22-24.
9. Erickson K.I., Raji C.A., Lopez O.L., Becker J.T., Rosano C., Newman A.B., Gach H.M., Thompson P.M., Ho A.J., Kuller L.H. Physical activity predicts gray matter volume in late adulthood: the Cardiovascular Health Study. Neurology 2010, 75(16):1415-1422.
10. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., Kim J.S., Heo S., Alves H., White S.M., Wojcicki T.R., Mailey E., Vieira V.J., Martin S.A., Pence B.D., Woods J.A., McAuley E., Kramer A.F. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(7):3017-3022.
11. Falkai P., Malchow B., Wobrock T., Gruber O., Schmitt A., Honer W.G., Pajonk F.G., Sun F., Cannon T.D. The effect of aerobic exercise on cortical architecture in patients with chronic schizophrenia: a randomized controlled MRI study. Eur. Arch. Psychiatry Clin. Neurosci. 2013, 263(6):469-473.
12. Faul F., Erdfelder E., Lang A.G., Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 2007, 39(2):175-191.
13. Fedorov A., Beichel R., Kalpathy-Cramer J., Finet J., Fillion-Robin J.C., Pujol S., Bauer C., Jennings D., Fennessy F., Sonka M., Buatti J., Aylward S., Miller J.V., Pieper S., Kikinis R. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn. Reson. Imaging 2012, 30(9):1323-1341.
14. Garber C.E., Blissmer B., Deschenes M.R., Franklin B.A., Lamonte M.J., Lee I.M., Nieman D.C., Swain D.P. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med. Sci. Sports Exerc. 2011, 43(7):1334-1359.
15. Hamada M., Murase N., Hasan A., Balaratnam M., Rothwell J.C. The role of interneuron networks in driving human motor cortical plasticity. Cereb. Cortex 2013, 23(7):1593-1605.
16. Hasan A., Falkai P., Wobrock T., Lieberman J., Glenthoj B., Gattaz W.F., Thibaut F., Moller H.J., W.T.f.o.T.G.f.Schizophrenia World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of schizophrenia, part 2: update 2012 on the long-term treatment of schizophrenia and management of antipsychotic-induced side effects. World J. Biol. Psychiatry 2013, 14(1):2-44.
17. Ho A.J., Raji C.A., Becker J.T., Lopez O.L., Kuller L.H., Hua X., Dinov I.D., Stein J.L., Rosano C., Toga A.W., Thompson P.M. The effects of physical activity, education, and body mass index on the aging brain. Hum. Brain Mapp. 2011, 32(9):1371-1382.
18. Ho B.C., Andreasen N.C., Ziebell S., Pierson R., Magnotta V. Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch. Gen. Psychiatry 2011, 68(2):128-137.
19. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am. J. Psychiatry 2005, 162(12):2233-2245.
20. Honea R.A., Thomas G.P., Harsha A., Anderson H.S., Donnelly J.E., Brooks W.M., Burns J.M. Cardiorespiratory fitness and preserved medial temporal lobe volume in Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2009, 23(3):188-197.
21. Hulshoff Pol H.E., Schnack H.G., Bertens M.G., van Haren N.E., van der Tweel I., Staal W.G., Baare W.F., Kahn R.S. Volume changes in gray matter in patients with schizophrenia. Am. J. Psychiatry 2002, 159(2):244-250.
22. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17(2):825-841.
23. Johansen-Berg H. The future of functionally-related structural change assessment. Neuroimage 2012, 62(2):1293-1298.
24. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
25. Kempton M.J., Stahl D., Williams S.C., DeLisi L.E. Progressive lateral ventricular enlargement in schizophrenia: a meta-analysis of longitudinal MRI studies. Schizophr. Res. 2010, 120(1-3):54-62.
26. Kenney W.L., Wilmore J., Costill D.L. Physiology of Sport and Exercise 2011, Human Kinetics, Champaign, USA. 5th ed.
27. Konrad C., Ukas T., Nebel C., Arolt V., Toga A.W., Narr K.L. Defining the human hippocampus in cerebral magnetic resonance images-an overview of current segmentation protocols. Neuroimage 2009, 47(4):1185-1195.
28. Lehrl S., Triebig G., Fischer B. Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol. Scand. 1995, 91(5):335-345.
29. Leung M., Cheung C., Yu K., Yip B., Sham P., Li Q., Chua S., McAlonan G. Gray matter in first-episode schizophrenia before and after antipsychotic drug treatment. Anatomical likelihood estimation meta-analyses with sample size weighting. Schizophr. Bull. 2011, 37(1):199-211.
30. Lieberman J.A., Tollefson G.D., Charles C., Zipursky R., Sharma T., Kahn R.S., Keefe R.S., Green A.I., Gur R.E., McEvoy J., Perkins D., Hamer R.M., Gu H., Tohen M. Antipsychotic drug effects on brain morphology in first-episode psychosis. Arch. Gen. Psychiatry 2005, 62(4):361-370.
31. Malchow B., Reich-Erkelenz D., Oertel-Knochel V., Keller K., Hasan A., Schmitt A., Scheewe T.W., Cahn W., Kahn R.S., Falkai P. The effects of physical exercise in schizophrenia and affective disorders. Eur. Arch. Psychiatry Clin. Neurosci. 2013, 263(6):451-467.
32. Mane A., Falcon C., Mateos J.J., Fernandez-Egea E., Horga G., Lomena F., Bargallo N., Prats-Galino A., Bernardo M., Parellada E. Progressive gray matter changes in first episode schizophrenia: a 4-year longitudinal magnetic resonance study using VBM. Schizophr. Res. 2009, 114(1-3):136-143.
33. May A. Experience-dependent structural plasticity in the adult human brain. Trends Cogn. Sci. 2011, 15(10):475-482.
34. Mitelman S.A., Brickman A.M., Shihabuddin L., Newmark R.E., Hazlett E.A., Haznedar M.M., Buchsbaum M.S. A comprehensive assessment of gray and white matter volumes and their relationship to outcome and severity in schizophrenia. Neuroimage 2007, 37(2):449-462.
35. Modinos G., Costafreda S.G., van Tol M.J., McGuire P.K., Aleman A., Allen P. Neuroanatomy of auditory verbal hallucinations in schizophrenia: a quantitative meta-analysis of voxel-based morphometry studies. Cortex 2013, 49(4):1046-1055.
36. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15(1):1-25.
37. Olabi B., Ellison-Wright I., McIntosh A.M., Wood S.J., Bullmore E., Lawrie S.M. Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol. Psychiatry 2011, 70(1):88-96.
38. Pajonk F.G., Wobrock T., Gruber O., Scherk H., Berner D., Kaizl I., Kierer A., Muller S., Oest M., Meyer T., Backens M., Schneider-Axmann T., Thornton A.E., Honer W.G., Falkai P. Hippocampal plasticity in response to exercise in schizophrenia. Arch. Gen. Psychiatry 2010, 67(2):133-143.
39. Palaniyappan L., Balain V., Radua J., Liddle P.F. Structural correlates of auditory hallucinations in schizophrenia: a meta-analysis. Schizophr. Res. 2012, 137(1-3):169-173.
40. Pereira A.C., Huddleston D.E., Brickman A.M., Sosunov A.A., Hen R., McKhann G.M., Sloan R., Gage F.H., Brown T.R., Small S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(13):5638-5643.
41. Reuter M., Fischl B. Avoiding asymmetry-induced bias in longitudinal image processing. Neuroimage 2011, 57(1):19-21.
42. Reuter M., Rosas H.D., Fischl B. Highly accurate inverse consistent registration: a robust approach. Neuroimage 2010, 53(4):1181-1196.
43. Reuter M., Schmansky N.J., Rosas H.D., Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 2012, 61(4):1402-1418.
44. Rey M.J., Schulz P., Costa C., Dick P., Tissot R. Guidelines for the dosage of neuroleptics. I: chlorpromazine equivalents of orally administered neuroleptics. Int. Clin. Psychopharmacol. 1989, 4(2):95-104.
45. Ridding M.C., Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol. 2010, 588(Pt 13):2291-2304.
46. Sagi Y., Tavor I., Hofstetter S., Tzur-Moryosef S., Blumenfeld-Katzir T., Assaf Y. Learning in the fast lane: new insights into neuroplasticity. Neuron 2012, 73(6):1195-1203.
47. Scheewe T.W., Backx F.J., Takken T., Jorg F., van Strater A.C., Kroes A.G., Kahn R.S., Cahn W. Exercise therapy improves mental and physical health in schizophrenia: a randomised controlled trial. Acta Psychiatr. Scand. 2013, 127(6):464-473.
48. Scheewe T.W., van Haren N.E., Sarkisyan G., Schnack H.G., Brouwer R.M., de Glint M., Hulshoff Pol H.E., Backx F.J., Kahn R.S., Cahn W. Exercise therapy, cardiorespiratory fitness and their effect on brain volumes: a randomised controlled trial in patients with schizophrenia and healthy controls. Eur. Neuropsychopharmacol. 2013, 23(7):675-685.
49. Sheehan D.V., Lecrubier Y., Sheehan K.H., Amorim P., Janavs J., Weiller E., Hergueta T., Baker R., Dunbar G.C. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 1998, 59(Suppl. 20):22-33. (quiz 34-57).
50. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17(3):143-155.
51. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 2009, 44(1):83-98.
52. Steen R.G., Mull C., McClure R., Hamer R.M., Lieberman J.A. Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br. J. Psychiatry 2006, 188:510-518.
53. Steinacker J.M., Liu Y., Reißnecker S. Stop criteria for ergometry. Dtsch. Z. Sportmed. 2002, 53(7 + 8):228-229.
54. Tamminga C.A., Stan A.D., Wagner A.D. The hippocampal formation in schizophrenia. Am. J. Psychiatry 2010, 167(10):1178-1193.
55. Van Haren N.E., Cahn W., Hulshoff Pol H.E., Kahn R.S. Confounders of excessive brain volume loss in schizophrenia. Neurosci. Biobehav. Rev. 2012, 37(10 Pt.1):2418-2423.
56. Van Leemput K., Bakkour A., Benner T., Wiggins G., Wald L.L., Augustinack J., Dickerson B.C., Golland P., Fischl B. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 2009, 19(6):549-557.
57. van Tol M.J., van der Meer L., Bruggeman R., Modinos G., Knegtering H., Aleman A. Voxel-based gray and white matter morphometry correlates of hallucinations in schizophrenia: the superior temporal gyrus does not stand alone. NeuroImage Clin. 2014, 4:249-257.
58. Vancampfort D., Knapen J., Probst M., Scheewe T., Remans S., De Hert M. A systematic review of correlates of physical activity in patients with schizophrenia. Acta Psychiatr. Scand. 2012, 125(5):352-362.
59. Velakoulis D., Wood S.J., Wong M.T., McGorry P.D., Yung A., Phillips L., Smith D., Brewer W., Proffitt T., Desmond P., Pantelis C. Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. Arch. Gen. Psychiatry 2006, 63(2):139-149.
60. Vita A., de Peri L. Hippocampal and amygdala volume reductions in first-episode schizophrenia. Br. J. Psychiatry 2007, 190:271.
61. Vita A., De Peri L., Silenzi C., Dieci M. Brain morphology in first-episode schizophrenia: a meta-analysis of quantitative magnetic resonance imaging studies. Schizophr. Res. 2006, 82(1):75-88.
62. Vita A., De Peri L., Deste G., Sacchetti E. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Trans. Psychiatry 2012, 2:e190.
63. Voss M.W., Vivar C., Kramer A.F., van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn. Sci. 2013, 17(10):525-544.
64. WHO International Statistical Classification of Diseases and Related Health Problems 10th Revision 2010, WHO, Geneva, Switzerland. 4th ed.
65. Woods S.W. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J. Clin. Psychiatry 2003, 64(6):663-667.
66. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20(1):45-57.