Perfusion deficits in patients with mild traumatic brain injury characterized by dynamic susceptibility contrast MRI

NMR in Biomedicine

Volumn 26, Issue 6, 2013, Pages 651-663

  Liu, Wei ^a,b   Wang, Binquan ^a,b   Wolfowitz, Rachel ^a,b,c   Yeh, Ping Hong ^a,b   Nathan, Dominic E ^a,b   Graner, John ^a,c   Tang, Haiying ^d   Pan, Hai ^a,b   Harper, Jamie ^a,c   Pham, Dzung ^e   Oakes, Terrence R ^a,c   French, Louis M ^d,e,f   Riedy, Gerard ^a,c  

^a National Capital Neuroimaging Consortium (NCNC)   (United States)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c National Intrepid Center of Excellence   (United States)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^e Center for Neuroscience and Regenerative Medicine (CNRM)   (United States)

^f WALTER REED ARMY MEDICAL CENTER   (United States)

Author keywords

Arterial input function; Dynamic susceptibility weighted MRI; Perfusion; Relative cerebral flood flow; Traumatic brain injury

Indexed keywords

ARTERIAL INPUT FUNCTION; DYNAMIC SUSCEPTIBILITY CONTRAST; DYNAMIC SUSCEPTIBILITY CONTRAST MRIS; FLOOD FLOW; MILD TRAUMATIC BRAIN INJURIES; NEUROPSYCHOLOGICAL ASSESSMENT; PERFUSION; TRAUMATIC BRAIN INJURIES;

AUTOMATION; BRAIN; MAGNETIC SUSCEPTIBILITY; PSYCHOPHYSIOLOGY; REGRESSION ANALYSIS;

NEUROIMAGING;

GADOLINIUM PENTETATE;

ADULT; ANTERIOR CINGULATE; ARTICLE; BLAST INJURY; BRAIN BLOOD FLOW; BRAIN MAPPING; BRAIN PERFUSION; BRAIN REGION; BRAIN SIZE; CEREBELLUM; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTRAST ENHANCEMENT; CONTROLLED STUDY; CORRELATION ANALYSIS; CUNEUS; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REACTION TIME; SCORING SYSTEM; SELF REPORT; STRESS; TEMPORAL GYRUS; TRAUMATIC BRAIN INJURY; VERBAL MEMORY;

ADULT; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; COGNITION; CONTRAST MEDIA; FEMALE; GADOLINIUM DTPA; HUMANS; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE;

EID: 84876786800     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2910     Document Type: Article

References (79)

1. National Center for Injury Prevention and Control. Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. Atlanta, GA: Centers for Disease Control and Prevention; 2003.
2. Sosin DM, Sniezek JE, Thurman DJ. Incidence of mild and moderate brain injury in the United States, 1991. Brain Inj. 1996; 10(1): 47-54.
3. Definition of Mild Traumatic Brain Injury. J. Head Trauma Rehabil. 1993; 8: 86-87.
4. Bradshaw BGD. chairman Traumatic Brain Injury Task Force, TBI Task Force Report, January 17, 2008.
5. Warden D. Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 2006; 21(5): 398-402.
6. Arciniegas DB, Anderson CA, Topkoff JL. Mild traumatic brain injury: A neuropsychiatric approach to diagnosis, evaluation, and treatment. Neuropsychiatr. Dis. Treat. 2005; 1: 311-327.
7. Zasler ND, Katz DI, Zafonte RD (eds). Brain Injury Medicine: Principles and Practice. Demos Medical: New York; 2006, pp. 333-371.
8. Dikmen S, Machamer J, Fann JR, Temkin NR. Rates of symptom reporting following traumatic brain injury. J. Int. Neuropsychol. Soc. 2010; 16: 401-411.
9. Schneiderman AI, Braver ER, Kang HK. Understanding sequelae of injury mechanisms and mild traumatic brain injury incurred during the conflicts in Iraq and Afghanistan: persistent postconcussive symptoms and posttraumatic stress disorder. Am. J. Epidemiol. 2008; 167(12): 1446-1452.
10. Hoge CW, McGurk D, Thomas JL, Cox AL, Engel CC, Castro CA. Mild traumatic brain injury in U.S. soldiers returning from Iraq. N. Engl. J. Med. 2008; 358(5): 453-463.
11. Belanger HG, Kretzmer T, Vanderploeg RD, French LM. Symptom complaints following combat-related traumatic brain injury: relationship to traumatic brain injury severity and posttraumatic stress disorder. J. Int. Neuropsychol. Soc. 2010; 16: 194-199.
12. Kelly MP, Coldren RL, Parish RV, Dretsch MN, Russell ML. Assessment of acute concussion in the combat environment. Arch. Clin. Neuropsychol. 2012; 27(4): 375-388.
13. Belanger HG, Curtiss G, Demery JA, Lebowitz BK, Vanderploeg RD. Factors moderating neuropsychological outcomes following mild traumatic brain injury: a meta-analysis. J. Int. Neuropsychol. Soc. 2005; 11(3): 215-227.
14. Belanger HG, Vanderploeg RD. The neuropsychological impact of sports-related concussion: a meta-analysis. J. Int. Neuropsychol. Soc. 2005; 11(4): 345-357.
15. Vasterling JJ, Proctor SP, Amoroso P, Kane R, Heeren T, White RF. Neuropsychological outcomes of army personnel following deployment to the Iraq War. J. Am. Med. Assoc. 2006; 296(5): 519-529.
16. Vasterling JJ, Brailey K, Proctor SP, Kane R, Heeren T, Franz M. Neuropsychological outcomes of mild traumatic brain injury, post-traumatic stress disorder and depression in Iraq-deployed US Army soldiers. Br. J. Psychiatry 2012; 201: 186-192.
17. Kou Z, Wu Z, Tong KA, Holshouser B, Benson RR, Hu J, Haacke EM. The role of advanced MR imaging findings as biomarkers of traumatic brain injury. J. Head Trauma Rehabil. 2010; 25(4): 267-282.
18. Nakashima T, Nakayama N, Miwa K, Okumura A, Soeda A, Iwama T. Focal brain glucose hypometabolism in patients with neuropsychologic deficits after diffuse axonal injury. Am. J. Neuroradiol. 2007; 28(2): 236-242.
19. Abdel-Dayem HM, Abu-Judeh H, Kumar M, Atay S, Naddaf S, El-Zeftawy H, Luo JQ. SPECT brain perfusion abnormalities in mild or moderate traumatic brain injury. Clin. Nucl. Med. 1998; 23(5): 309-317.
20. Shin YB, Kim SJ, Kim IJ, Kim YK, Kim DS, Park JH, Yeom SR. Voxel-based statistical analysis of cerebral blood flow using Tc-99m ECD brain SPECT in patients with traumatic brain injury: group and individual analyses. Brain Inj. 2006; 20(6): 661-667.
21. Van Laere KJ, Warwick J, Versijpt J, Goethals I, Audenaert K, Van Heerden B, Dierckx R. Analysis of clinical brain SPECT data based on anatomic standardization and reference to normal data: an ROC-based comparison of visual, semiquantitative, and voxel-based methods. J. Nucl. Med. 2002; 43(4): 458-469.
22. Humayun MS, Presty SK, Lafrance ND, Holcomb HH, Loats H, Long DM, Wagner HN, Gordon B. Local cerebral glucose abnormalities in mild closed head injured patients with cognitive impairments. Nucl. Med. Commun. 1989; 10(5): 335-344.
23. Ruff RM, Crouch JA, Troster AI, Marshall LF, Buchsbaum MS, Lottenberg S, Somers LM. Selected cases of poor outcome following a minor brain trauma: comparing neuropsychological and positron emission tomography assessment. Brain Inj. 1994; 8(4): 297-308.
24. Gross H, Kling A, Henry G, Herndon C, Lavretsky H. Local cerebral glucose metabolism in patients with long-term behavioral and cognitive deficits following mild traumatic brain injury. J. Neuropsych. Clin. N. 1996; 8(3): 324-334.
25. Bonne O, Gilboa A, Louzoun Y, Kempf-Sherf O, Katz M, Fishman Y, Ben-Nahum Z, Krausz Y, Bocher M, Lester H, Chisin R, Lerer B. Cerebral blood flow in chronic symptomatic mild traumatic brain injury. Psychiatr. Res. 2003; 124(3): 141-152.
26. Ichise M, Chung DG, Wang P, Wortzman G, Gray BG, Franks W. Technetium-99m-HMPAO SPECT, CT and MRI in the evaluation of patients with chronic traumatic brain injury: a correlation with neuropsychological performance. J. Nucl. Med. 1994; 35(2): 217-226.
27. Umile EM, Sandel ME, Alavi A, Terry CM, Plotkin RC. Dynamic imaging in mild traumatic brain injury: support for the theory of medial temporal vulnerability. Arch. Phys. Med. Rehabil. 2002; 83(11): 1506-1513.
28. Belanger HG, Vanderploeg RD, Curtiss G, Warden DL. Recent neuroimaging techniques in mild traumatic brain injury. J. Neuropsych. Clin. N. 2007; 19(1): 5-20.
29. Manley GT, Diaz-Arrastia R, Brophy M, Engel D, Goodman C, Gwinn K, Veenstra TD, Ling G, Ottens AK, Tortella F, Hayes RL. Common data elements for traumatic brain injury: recommendations from the biospecimens and biomarkers working group. Arch. Phys. Med. Rehabil. 2010; 91: 1667-1672.
30. Shumskya E, Andriessen TMJC, Norris DG, Vos PE. Abnormal whole-brain functional networks in homogeneous acute mild traumatic brain injury. Neurology 2012; 79: 175-182.
31. McDonald BC, Saykin AJ, McAllister TW. Functional MRI of mild traumatic brain injury (mTBI): progress and perspectives from the first decade of studies. Brain Imaging Behav. 2012; 6: 193-207.
32. Menon DK, Schwab K, Wright DW, Maas AI. Position statement: definition of traumatic brain injury. Arch. Phys. Med. Rehabil. 2010; 91: 1637-1640.
33. Rempp KA, Brix G, Wenz F, Becker CR, Guckel F, Lorenz WJ. Quantification of regional cerebral blood flow and volume with dynamic susceptibility contrast-enhanced MR imaging. Radiology 1994; 193: 637-641.
34. Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: mathematical approach and statistical analysis. Magn. Reson. Med. 1996; 36(5): 715-725.
35. Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gyldensted C, Rosen BR. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: experimental comparison and preliminary results. Magn. Reson. Med. 1996; 36(5): 726-736.
36. Ostergaard L, Smith DF, Vestergaard-Poulsen P, Hansen SB, Gee AD, Gjedde A, Gyldensted C. Absolute cerebral blood flow and blood volume measured by magnetic resonance imaging bolus tracking: comparison with positron emission tomography values. J. Cereb. Blood Flow Metab. 1998; 18(4): 425-432.
37. Miao Y, Juhasz C, Wu J, Tarabishy B, Lang Z, Behen ME, Kou Z, Ye Y, Chugani HT, Hu J. Clinical correlates of white matter blood flow perfusion changes in Sturge-Weber syndrome: a dynamic MR perfusion-weighted imaging study. Am. J. Neuroradiol. 2011; 32(7): 1280-1285.
38. Bjornerud A, Emblem KE. A fully automated method for quantitative cerebral hemodynamic analysis using DSC-MRI. J. Cereb. Blood Flow Metab. 2010; 30(5): 1066-1078.
39. Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci. USA 1992; 89: 212-216.
40. Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, Koretsky AP, Leigh JS. Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed. 1994; 7: 75-82.
41. Conturo TE, Akbudak E, Kotys MS, Chen ML, Chun SJ, Hsu RM, Sweeney CC, Markham J. Arterial input functions for dynamic susceptibility contrast MRI: requirements and signal options. J. Magn. Reson. Imaging 2005; 22(6): 697-703.
42. Ruminski J, Karczewski B. Automatic recognition of the arterial input function. Comput. Recog. Syst. 2005; 30: 671-677.
43. Mlynash M, Eyngorn I, Bammer R, Moseley M, Tong DC. Automated method for generating the arterial input function on perfusion-weighted MR imaging: validation in patients with stroke. Am. J. Neuroradiol. 2005; 26: 1479-1486.
44. Rausch M, Scheffler K, Rudin M, Radu EW. Analysis of input functions from different arterial branches with gamma variable functions and cluster analysis for quantitative blood volume measurements. Magn. Reson. Imaging 2000; 18: 1235-1243.
45. Peruzzo D, Bertoldo A, Zanderigo F, Cobelli C. Automatic selection of arterial input function on dynamic contrast-enhanced MR images. Comput. Methods Prog. Biol. 2011; 104(3): e148-e157.
46. Carroll TJ, Rowley HA, Haughton VM. Automatic calculation of the arterial input function for cerebral perfusion imaging with MR imaging. Radiology 2003; 227(2): 593-600.
47. Butman JA, Tasciyan T. Automated computation of the arterial input function for dynamic susceptibility bolus tracking brain perfusion MRI. Proc. Int. Soc. Magn. Reson. Med. 2005; 13: 1126.
48. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996; 29(3): 162-173.
49. Weisskoff RM, Zuo CS, Boxerman JL, Rosen BR. Microscopic susceptibility variation and transverse relaxation: theory and experiment. Magn. Reson. Med. 1994; 31: 601-610.
50. Meier P, Zierler KL. On the theory of the indicator-dilution method for measurement of blood flow and volume. J. Appl. Physiol. 1954; 12: 731-744.
51. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 Suppl 1: S208-S219.
52. Mukherjee P, Kang HC, Videen TO, McKinstry RC, Powers WJ, Derdeyn CP. Measurement of cerebral blood flow in chronic carotid occlusive disease: comparison of dynamic susceptibility contrast perfusion MR imaging with positron emission tomography. Am. J. Neuroradiol. 2003; 24: 862-871.
53. Lammertsma AA, Brooks DJ, Beaney RP, Turton DR, Kensett MJ, Heather JD, Marshall J, Jones T. In vivo measurement of regional cerebral haematocrit using positron emission tomography. J. Cereb. Blood Flow Metab. 1984; 4(3): 317-322.
54. Kim J, Whyte J, Patel S, Avants B, Europa E, Wang J, Slattery J, Gee JC, Coslett HB, Detre JA. Resting cerebral blood flow alterations in chronic traumatic brain injury: an arterial spin labeling perfusion FMRI study. J. Neurotrauma 2010; 27(8): 1399-1411.
55. Stamatakis EA, Wilson JT, Hadley DM, Wyper DJ. SPECT imaging in head injury interpreted with statistical parametric mapping. J. Nucl. Med. 2002; 43(4): 476-483.
56. Hofman PA, Stapert SZ, van Kroonenburgh MJ, Jolles J, de Kruijk J, Wilmink JT. MR imaging, single-photon emission CT, and neurocognitive performance after mild traumatic brain injury. Am. J. Neuroradiol. 2001; 22(3): 441-449.
57. Ge Y, Patel MB, Chen Q, Grossman EJ, Zhang K, Miles L, Sabb JS, Reaume J, Grossman RI. Assessment of thalamic perfusion in patients with mild traumatic brain injury by true FISP arterial spin labeling MR imaging at 3T. Brain Inj. 2009; 23: 666-674.
58. Casey BJ, Trainor R, Giedd J, Vauss Y, Vaituzis CK, Hamburger S, Kozuch P, Rapoport JL. The role of the anterior cingulate in automatic and controlled processes: a developmental neuroanatomical study. Dev. Psychobiol. 1997; 30(1): 61-69.
59. Dehaene S, Kerszberg M, Changeux JP. A neuronal model of a global workspace in effortful cognitive tasks. Proc. Natl. Acad. Sci. USA 1998; 95(24): 14 529-14 534.
60. Swick D, Jovanovic J. Anterior cingulate cortex and the Stroop task: neuropsychological evidence for topographic specificity. Neuropsychologia 2002; 40(8): 1240-1253.
61. Cabeza R, Nyberg L. Imaging cognition II: an empirical review of 275 PET and fMRI studies. J. Cogn. Neurosci. 2000; 12(1): 1-47.
62. Zysset S, Huber O, Ferstl E, von Cramon DY. The anterior frontomedian cortex and evaluative judgment: an fMRI study. Neuroimage 2002; 15(4): 983-991.
63. Kraus MF, Susmaras T, Caughlin BC, Walker CJ, Sweeney JA, Little DM. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007; 130: 2508-2519.
64. Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu. Rev. Neurosci. 2009; 32: 413-434.
65. Graner J, Pan H, Yeh P-H, Wang B, Oakes TR, Liu W, French LM, Munter F, Riedy G. fMRI of working memory in military traumatic brain injury. Proc. Int. Soc. Magn. Reson. Med. 2011; 3662.
66. Bryant R. Post-traumatic stress disorder vs traumatic brain injury. Dialogues Clin. Neurosci. 2011; 13(3): 251-262.
67. Levin HS, Brown SA, Song JX, McCauley SR, Boake C, Contant CF, Goodman H, Kotrla KJ. Depression and posttraumatic stress disorder at three months after mild to moderate traumatic brain injury. J. Clin. Exp. Neuropsychol. 2001; 23(6): 754-769.
68. Jamora CW, Young A, Ruff RM. Comparison of subjective cognitive complaints with neuropsychological tests in individuals with mild vs more severe traumatic brain injuries. Brain Inj. 2012; 26(1): 36-47.
69. Sayer NA, Chiros CE, Sigford B, Scott S, Clothier B, Pickett T, Lew HL. Characteristics and rehabilitation outcomes among patients with blast and other injuries sustained during the global war on terror. Arch. Phys. Med. Rehabil. 2008; 89: 163-170.
70. Kennedy JE, Leal FO, Lewis JD, Cullen MA, Amador RR. Posttraumatic stress symptoms in OIF/OEF service members with blast-related and non-blast-related mild TBI. NeuroRehabilitation 2010; 26: 223-231.
71. Belanger HG, Kretzmer T, Yoash-Gantz R, Pickett T, Jupler LA. Cognitive sequelae of blast-related versus other mechanisms of brain trauma. J. Int. Neuropsychol. Soc. 2009; 15: 1-8.
72. Lange RT, Pancholi S, Brickell TA, Sakura S, Bhagwat A, Merritt V, French LM. Neuropsychological outcome from blast versus non-blast mild traumatic brain injury in U.S. military service members. J. Int. Neuropsychol. Soc. 2012; 18: 595-605.
73. Field AS, Laurienti PJ, Yen Y-F, Burdette JH, Moody DM. Dietary caffeine consumption and withdrawal: confounding variables in quantitative cerebral perfusion studies? Radiology 2003; 227: 129-135.
74. Yamashita K, Kobayashi S, Yamaguchi S, Kitani M, Tsunematsu T. Effect of smoking on regional cerebral blood flow in the normal aged volunteers. Gerontology 1988; 34: 199-204.
75. Kubota K, Yamaguchi T, Abe Y, Fujiwara T, Hatazawa J, Matsuzawa T. Effects of smoking on regional cerebral blood flow in neurologically normal subjects. Stroke 1983; 14: 720-724.
76. Vlassenko A, Sheline YI, Fischer K, Mintun MA. Cerebral perfusion response to successful treatment of depression with different serotoninergic agents. J. Neuropsychiatry Clin. Neurosci. 2004; 16: 360-363.
77. Franklin TR, Wang Z, Sciortino N, Harper D, Li Y, Hakun J, Kildea S, Kampman K, Ehrman R, Detre JA, O'Brien CP, Childress AR. Modulation of resting brain cerebral blood flow by the GABA B agonist, baclofen: a longitudinal perfusion fMRI study. Drug Alcohol Depend. 2011; 117: 176-183.
78. Borghammer P, Cumming P, Aanerud J, Gjedde A. Artifactual subcortical hyperperfusion in PET studies normalized to global mean: lessons from Parkinson's disease. Neuroimage 2009; 45(2): 249-257.
79. Grunder G. "Absolute" or "relative": choosing the right outcome measure in neuroimaging. Neuroimage 2009; 45(2): 258-259.