A potential biomarker in sports-related concussion: Brain functional connectivity alteration of the default-mode network measured with longitudinal resting-state fMRI over thirty days

Journal of Neurotrauma

Volumn 32, Issue 5, 2015, Pages 327-341

  Zhu, David C ^a,b   Covassin, Tracey ^b   Nogle, Sally ^b   Doyle, Scarlett ^a,b   Russell, Doozie ^c   Pearson, Randolph L ^d   Monroe, Jeffrey ^b   Liszewski, Christine M ^e   DeMarco, J Kevin ^a   Kaufman, David I ^c  

^a St John Hospital and Medical Center   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c East Lansing   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e Michigan State University   (United States)

Author keywords

default mode network; diffusion tensor imaging; mild traumatic brain injury; resting state fMRI; sports related concussion

Indexed keywords

ADULT; ARTICLE; ATHLETE; BRAIN FUNCTION; COGNITIVE DEFECT; CONTROLLED STUDY; DEFAULT MODE NETWORK; DIFFUSION TENSOR IMAGING; DISEASE MARKER; FOOTBALL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; LONGITUDINAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE SCANNER; PILOT STUDY; RESTING STATE NETWORK; SPORT INJURY; THREE DIMENSIONAL IMAGING; BRAIN INJURIES; COMPUTER ASSISTED DIAGNOSIS; DIFFUSION WEIGHTED IMAGING; INJURIES; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES; YOUNG ADULT;

BRAIN INJURIES; DIFFUSION MAGNETIC RESONANCE IMAGING; FOOTBALL; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PILOT PROJECTS; YOUNG ADULT;

EID: 84924138795     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3413     Document Type: Article

References (53)

1. Langlois, J.A., Rutland-Brown, W., and Wald, M.M. (2006). The epidemiology and impact of traumatic brain injury: a brief overview. J. Head Trauma Rehabil. 21, 375-378.
2. Ruff, R.M. (2011). Mild traumatic brain injury and neural recovery: rethinking the debate. NeuroRehabilitation 28, 167-180.
3. Giza, C.C., Kutcher, J.S., Ashwal, S., Barth, J., Getchius, T.S., Gioia, G.A., Gronseth, G.S., Guskiewicz, K., Mandel, S., Manley, G., McKeag, D.B., Thurman, D.J., and Zafonte, R. (2013). Summary of evidence-based guideline update: Evaluation and management of concussion in sports: Report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 80, 2250-2257.
4. Mayers, L.B. and Redick, T.S. (2012). Clinical utility of ImPACT assessment for postconcussion return-to-play counseling: psychometric issues. J. Clin. Exp. Neuropsychol. 34, 235-242.
5. McCrea, M., Guskiewicz, K., Randolph, C., Barr, W.B., Hammeke, T.A., Marshall, S.W., and Kelly, J.P. (2009). Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion. Neurosurgery 65, 876-882.
6. McCrea, M., Guskiewicz, K.M., Marshall, S.W., Barr, W., Randolph, C., Cantu, R.C., Onate, J.A., Yang, J., and Kelly, J.P. (2003). Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 290, 2556-2563.
7. Lau, B.C., Kontos, A.P., Collins, M.W., Mucha, A., and Lovell, M.R. (2011). Which on-field signs/symptoms predict protracted recovery from sport-related concussion among high school football players? Am. J. Sports Med. 39, 2311-2318.
8. Fox, M.D. and Raichle, M.E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711.
9. Basser, P.J., Pajevic, S., Pierpaoli, C., Duda, J., and Aldroubi, A. (2000). In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 44, 625-632.
10. Behrens, T.E., Berg, H.J., Jbabdi, S., Rushworth, M.F., and Woolrich, M.W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34, 144-155.
11. Le Bihan, D., Mangin, J.F., Poupon, C., Clark, C.A., Pappata, S., Molko, N., and Chabriat, H. (2001). Diffusion tensor imaging: concepts and applications. J. Magn. Reson. Imaging 13, 534-546.
12. Guskiewicz, K.M., Weaver, N.L., Padua, D.A., and Garrett, W.E., Jr. (2000). Epidemiology of concussion in collegiate and high school football players. Am. J. Sports Med. 28, 643-650.
13. Raichle, M.E. and Mintun, M.A. (2006). Brain work and brain imaging. Annu. Rev. Neurosci. 29, 449-476.
14. Johnson, B., Zhang, K., Gay, M., Horovitz, S., Hallett, M., Sebastianelli, W., and Slobounov, S. (2012). Alteration of brain default network in subacute phase of injury in concussed individuals: resting-state fMRI study. Neuroimage 59, 511-518.
15. Slobounov, S.M., Gay, M., Zhang, K., Johnson, B., Pennell, D., Sebastianelli, W., Horovitz, S., and Hallett, M. (2011). Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. Neuroimage 55, 1716-1727.
16. Zhang, K., Johnson, B., Gay, M., Horovitz, S.G., Hallett, M., Sebastianelli, W., and Slobounov, S. (2012). Default mode network in concussed individuals in response to the YMCA physical stress test. J. Neurotrauma 29, 756-765.
17. Mayer, A.R., Mannell, M.V., Ling, J., Gasparovic, C., and Yeo, R.A. (2011). Functional connectivity in mild traumatic brain injury. Hum. Brain Mapp. 32, 1825-1835.
18. Zhou, Y., Milham, M.P., Lui, Y.W., Miles, L., Reaume, J., Sodickson, D.K., Grossman, R.I., and Ge, Y. (2012). Default-mode network disruption in mild traumatic brain injury. Radiology 265, 882-892.
19. Shumskaya, E., Andriessen, T.M., Norris, D.G., and Vos, P.E. (2012). Abnormal whole-brain functional networks in homogeneous acute mild traumatic brain injury. Neurology 79, 175-182.
20. Messe, A., Caplain, S., Pelegrini-Issac, M., Blancho, S., Levy, R., Aghakhani, N., Montreuil, M., Benali, H., and Lehericy, S. (2013). Specific and evolving resting-state network alterations in post-concussion syndrome following mild traumatic brain injury. PLoS One 8, e65470.
21. Han, K., Mac Donald, C.L., Johnson, A.M., Barnes, Y., Wierzechowski, L., Zonies, D., Oh, J., Flaherty, S., Fang, R., Raichle, M.E., and Brody, D.L. (2014). Disrupted modular organization of resting-state cortical functional connectivity in U.S. military personnel following concussive 'mild' blast-related traumatic brain injury. Neuroimage 84, 76-96.
22. Mayer, A.R., Ling, J., Mannell, M.V., Gasparovic, C., Phillips, J.P., Doezema, D., Reichard, R., and Yeo, R.A. (2010). A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74, 643-650.
23. Aoki, Y., Inokuchi, R., Gunshin, M., Yahagi, N., and Suwa, H. (2012). Diffusion tensor imaging studies of mild traumatic brain injury: a meta-analysis. J. Neurol. Neurosurg. Psychiatry 83, 870-876.
24. Zhang, K., Johnson, B., Pennell, D., Ray, W., Sebastianelli, W., and Slobounov, S. (2010). Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study. Exp. Brain Res. 204, 57-70.
25. Zhu, D.C., Majumdar, S., Korolev, I.O., Berger, K.L., and Bozoki, A.C. (2013). Alzheimer's disease and amnestic mild cognitive impairment weaken connections within the default-mode network: a multi-modal imaging study. J. Alzheimers Dis. 34, 969-984.
26. Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., and Shulman, G.L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 98, 676-682.
27. Greicius, M.D., Srivastava, G., Reiss, A.L., and Menon, V. (2004). Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U. S. A. 101, 4637-4642.
28. Greicius, M.D., Supekar, K., Menon, V., and Dougherty, R.F. (2009). Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 19, 72-78.
29. Supekar, K., Menon, V., Rubin, D., Musen, M., and Greicius, M.D. (2008). Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput. Biol. 4, e1000100.
30. Zhang, H.Y., Wang, S.J., Liu, B., Ma, Z.L., Yang, M., Zhang, Z.J., and Teng, G.J. (2010). Resting brain connectivity: changes during the progress of Alzheimer disease. Radiology 256, 598-606.
31. Buckner, R.L., Andrews-Hanna, J.R., and Schacter, D.L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1-38.
32. Woolsey, T.A., Hanaway, J., and Gado, M.H. (2003). The brain atlas: a visual guide to the human central nervous system. 2nd ed. John Wiley & Sons, Inc.: Hoboken, New Jersey.
33. Iverson, G.L., Lovell, M.R., and Collins, M.W. (2005). Validity of ImPACT for measuring processing speed following sports-related concussion. J. Clin. Exp. Neuropsychol. 27, 683-689.
34. Schatz, P. (2010). Long-term test-retest reliability of baseline cognitive assessments using ImPACT. Am. J. Sports Med. 38, 47-53.
35. Schatz, P., Pardini, J.E., Lovell, M.R., Collins, M.W., and Podell, K. (2006). Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. Arch. Clin. Neuropsychol. 21, 91-99.
36. Schatz, P. and Sandel, N. (2013). Sensitivity and specificity of the online version of ImPACT in high school and collegiate athletes. Am. J. Sports Med 41, 321-326.
37. th International Conference on Concussion in Sport held in Zurich, November 2012. Br. J. Sports Med. 47, 250-258.
38. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., and Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1, S208-S219.
39. Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29, 162-173.
40. Ward, B. (2000). Deconvolution analysis of fMRI time series Data. Available at: http://afni.nimh.nih.gov/pub/dist/doc/manual/Deconvolvem.pdf. Accessed October 25, 2014.
41. Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., and Dale, A.M. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355.
42. Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., and Raichle, M.E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 102, 9673-9678.
43. Yeo, B.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., Roffman, J.L., Smoller, J.W., Zollei, L., Polimeni, J.R., Fischl, B., Liu, H., and Buckner, R.L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125-1165.
44. Ward, B. (2000). Simultaneous inference for fMRI data. Available at http://afni.nimh.nih.gov/pub/dist/doc/manual/AlphaSim.pdf. Accessed December 8, 2014.
45. Behrens, T.E., Woolrich, M.W., Jenkinson, M., Johansen-Berg, H., Nunes, R.G., Clare, S., Matthews, P.M., Brady, J.M., and Smith, S.M. (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50, 1077-1088.
46. Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., Hua, K., Faria, A.V., Mahmood, A., Woods, R., Toga, A.W., Pike, G.B., Neto, P.R., Evans, A., Zhang, J., Huang, H., Miller, M.I., van Zijl, P., and Mazziotta, J. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40, 570-582.
47. Giza, C.C. and Hovda, D.A. (2001). The neurometabolic cascade of concussion. J. Athl. Train. 36, 228-235.
48. Maugans, T.A., Farley, C., Altaye, M., Leach, J., and Cecil, K.M. (2012). Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics 129, 28-37.
49. Zhu, D.C. and Majumdar, S. (2014). Integration of resting-state FMRI and diffusion-weighted MRI connectivity analyses of the human brain: limitations and improvement. J. Neuroimaging 24, 176-186.
50. Murphy, K., Birn, R.M., Handwerker, D.A., Jones, T.B., and Bandettini, P.A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44, 893-905.
51. Harris, J.L., Yeh, H.W., Choi, I.Y., Lee, P., Berman, N.E., Swerdlow, R.H., Craciunas, S.C., and Brooks, W.M. (2012). Altered neurochemical profile after traumatic brain injury: (1)H-MRS biomarkers of pathological mechanisms. J. Cereb. Blood Flow Metab. 32, 2122-2134.
52. Bey, T. and Ostick, B. (2009). Second impact syndrome. West J Emerg Med 10, 6-10.
53. McKee, A.C., Cantu, R.C., Nowinski, C.J., Hedley-Whyte, E.T., Gavett, B.E., Budson, A.E., Santini, V.E., Lee, H.S., Kubilus, C.A., and Stern, R.A. (2009). Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 68, 709-735.