Regional Variation in Brain White Matter Diffusion Index Changes following Chemoradiotherapy: A Prospective Study Using Tract-Based Spatial Statistics

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Chapman, Christopher H ^a   Nazem Zadeh, Mohammad ^a   Lee, Oliver E ^a   Schipper, Matthew J ^a   Tsien, Christina I ^a   Lawrence, Theodore S ^a   Cao, Yue ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; CARBOPLATIN; CETUXIMAB; GEMCITABINE; PACLITAXEL;

ADULT; AGED; ARTICLE; BRAIN FORNIX; BRAIN METASTASIS; BRAIN RADIATION; CHEMORADIOTHERAPY; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DRUG RESPONSE; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; MALE; PROSPECTIVE STUDY; RADIATION RESPONSE; WHITE MATTER;

ADULT; AGED; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CHEMORADIOTHERAPY; COGNITION; CORPUS CALLOSUM; DEMYELINATING DISEASES; DIFFUSION TENSOR IMAGING; FEMALE; FORNIX, BRAIN; GAMMA RAYS; GYRUS CINGULI; HUMANS; MALE; MELANOMA; MIDDLE AGED; NERVE FIBERS, MYELINATED; PROSPECTIVE STUDIES;

EID: 84874625654     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057768     Document Type: Article

References (54)

1. Taphoorn MJB, Klein M, (2004) Cognitive deficits in adult patients with brain tumours. Lancet Neurol 3: 159-168 doi:10.1016/S1474-4422(04)00680-5.
2. Crossen JR, Garwood D, Glatstein E, Neuwelt EA, (1994) Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. J Clin Oncol 12: 627-642.
3. Douw L, Klein M, Fagel SS, van den Heuvel J, Taphoorn MJ, et al. (2009) Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8: 810-818 doi:10.1016/S1474-4422(09)70204-2.
4. Hsiao K-Y, Yeh S-A, Chang C-C, Tsai P-C, Wu J-M, et al. (2010) Cognitive function before and after intensity-modulated radiation therapy in patients with nasopharyngeal carcinoma: a prospective study. Int J Radiat Oncol Biol Phys 77: 722-726 doi:10.1016/j.ijrobp.2009.06.080.
5. Roman DD, Sperduto PW, (1995) Neuropsychological effects of cranial radiation: current knowledge and future directions. Int J Radiat Oncol Biol Phys 31: 983-998.
6. Surma-aho O, Niemela M, Vilkki J, Kouri M, Brander A, et al. (2001) Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56: 1285-1290 doi:10.1212/WNL.56.10.1285.
7. Okada S, Okeda R, (2001) Pathology of radiation myelopathy. Neuropathology 21: 247-265.
8. Akiyama K, Tanaka R, Sato M, Takeda N, (2001) Cognitive dysfunction and histological findings in adult rats one year after whole brain irradiation. Neurol Med Chir (Tokyo) 41: 590-598.
9. Constine LS, Konski A, Ekholm S, McDonald S, Rubin P, (1988) Adverse effects of brain irradiation correlated with MR and CT imaging. Int J Radiat Oncol Biol Phys 15: 319-330.
10. Assaf Y, Pasternak O, (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34: 51-61 doi:10.1007/s12031-007-0029-0.
11. Mac Donald CL, Dikranian K, Bayly P, Holtzman D, Brody D, (2007) Diffusion Tensor Imaging Reliably Detects Experimental Traumatic Axonal Injury and Indicates Approximate Time of Injury. Journal of Neuroscience 27: 11869-11876 doi:10.1523/jneurosci.3647-07.2007.
12. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, et al. (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17: 1429-1436.
13. Song S-K, Yoshino J, Le TQ, Lin S-J, Sun S-W, et al. (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neurology 26: 132-140 doi:10.1016/j.neuroimage.2005.01.028.
14. Sun S-W, Liang H-F, Cross AH, Song S-K, (2008) Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. Neuroimage 40: 1-10 doi:10.1016/j.neuroimage.2007.11.049.
15. Wang S, Wu EX, Qiu D, Leung LHT, Lau H-F, et al. (2009) Longitudinal diffusion tensor magnetic resonance imaging study of radiation-induced white matter damage in a rat model. Cancer Res 69: 1190-1198 doi:10.1158/0008-5472.CAN-08-2661.
16. Song S-K, Sun S-W, Ju W-K, Lin S-J, Cross AH, et al. (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20: 1714-1722.
17. Khong P-L, Kwong DLW, Chan GCF, Sham JST, Chan F-L, et al. (2003) Diffusion-tensor imaging for the detection and quantification of treatment-induced white matter injury in children with medulloblastoma: a pilot study. AJNR Am J Neuroradiol 24: 734-740.
18. Leung LHT, Ooi GC, Kwong DLW, Chan GCF, Cao G, et al. (2004) White-matter diffusion anisotropy after chemo-irradiation: a statistical parametric mapping study and histogram analysis. Neuroimage 21: 261-268.
19. Lawrence YR, Li XA, Naqa el I, Hahn CA, Marks LB, et al. (2010) Radiation dose-volume effects in the brain (QUANTEC). Int J Radiat Oncol Biol Phys 76: S20-S27 doi:10.1016/j.ijrobp.2009.02.091.
20. Ghia A, Tomé W, Thomas S, Cannon G, Khuntia D, et al. (2007) Distribution of brain metastases in relation to the hippocampus: implications for neurocognitive functional preservation. Int J Radiat Oncol Biol Phys 68: 971.
21. Marsh JC, Godbole R, Diaz AZ, Gielda BT, Turian JV, (2011) Sparing of the hippocampus, limbic circuit and neural stem cell compartment during partial brain radiotherapy for glioma: A dosimetric feasibility study. J Med Imaging Radiat Oncol 55: 442-449 doi:10.1111/j.1754-9485.2011.02282.x.
22. Radiation Therapy Oncology Group; National Cancer Institute (2010) Avoiding the Hippocampus During Whole-Brain Radiation Therapy in Treating Patients With Brain Metastases. Available: http://clinicaltrials.gov/show/NCT01227954. Accessed 2012 Oct 29.
23. Monje ML, Mizumatsu S, Fike JR, Palmer TD, (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8: 955-962 doi:10.1038/nm749.
24. Dellani PR, Eder S, Gawehn J, Vucurevic G, Fellgiebel A, et al. (2008) Late structural alterations of cerebral white matter in long-term survivors of childhood leukemia. Journal of magnetic resonance imaging: JMRI 27: 1250-1255 doi:10.1002/jmri.21364.
25. Qiu D, Kwong DLW, Chan GCF, Leung LHT, Khong P-L, (2007) Diffusion tensor magnetic resonance imaging finding of discrepant fractional anisotropy between the frontal and parietal lobes after whole-brain irradiation in childhood medulloblastoma survivors: reflection of regional white matter radiosensitivity? Int J Radiat Oncol Biol Phys 69: 846-851 doi:10.1016/j.ijrobp.2007.04.041.
26. Chapman CH, Nagesh V, Sundgren PC, Buchtel H, Chenevert TL, et al. (2012) Diffusion tensor imaging of normal-appearing white matter as biomarker for radiation-induced late delayed cognitive decline. Int J Radiat Oncol Biol Phys 82: 2033-2040 doi:10.1016/j.ijrobp.2011.01.068.
27. Hua C, Merchant TE, Gajjar A, Broniscer A, Zhang Y, et al. (2012) Brain tumor therapy-induced changes in normal-appearing brainstem measured with longitudinal diffusion tensor imaging. Int J Radiat Oncol Biol Phys 82: 2047-2054 doi:10.1016/j.ijrobp.2011.03.057.
28. Nagesh V, Tsien CI, Chenevert TL, Ross BD, Lawrence TS, et al. (2008) Radiation-induced changes in normal-appearing white matter in patients with cerebral tumors: a diffusion tensor imaging study. Int J Radiat Oncol Biol Phys 70: 1002-1010 doi:10.1016/j.ijrobp.2007.08.020.
29. Nazem-Zadeh M-R, Chapman CH, Lawrence TL, Tsien CI, Cao Y, (2012) Radiation therapy effects on white matter fiber tracts of the limbic circuit. Med Phys 39: 5603 doi:10.1118/1.4745560.
30. Welzel T, Niethammer A, Mende U, Heiland S, Wenz F, et al. (2008) Diffusion tensor imaging screening of radiation-induced changes in the white matter after prophylactic cranial irradiation of patients with small cell lung cancer: first results of a prospective study. AJNR Am J Neuroradiol 29: 379-383 doi:10.3174/ajnr.A0797.
31. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, et al. (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31: 1487-1505 doi:10.1016/j.neuroimage.2006.02.024.
32. Cao Y, (2005) Development of Image Software Tools for Radiation Therapy Assessment. Med Phys 32: 2136.
33. Mori S, Oishi K, Jiang H, Jiang L, Li X, et al. (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40: 570-582 doi:10.1016/j.neuroimage.2007.12.035.
34. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, et al. (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philosophical Transactions of the Royal Society of London Series B 356: 1293 doi:10.1098/rstb.2001.0915.
35. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (Suppl 1): S208-S219 doi:10.1016/j.neuroimage.2004.07.051.
36. Smith SM, Nichols TE, (2009) Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44: 83-98 doi:10.1016/j.neuroimage.2008.03.061.
37. Nichols TE, Holmes AP, (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15: 1-25.
38. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological): 289-300.
39. Shah A, Jhawar SS, Goel A, (2012) Analysis of the anatomy of the Papez circuit and adjoining limbic system by fiber dissection techniques. Journal of Clinical Neuroscience 19: 289-298 doi:10.1016/j.jocn.2011.04.039.
40. Lautin A (2002) The Limbic Brain. New York, NY: Kluwer Academic Publishers.
41. Chua TC, Wen W, Chen X, Kochan N, Slavin MJ, et al. (2009) Diffusion tensor imaging of the posterior cingulate is a useful biomarker of mild cognitive impairment. Am J Geriatr Psychiatry 17: 602-613 doi:10.1097/JGP.0b013e3181a76e0b.
42. Wu TC, Wilde EA, Bigler ED, Yallampalli R, McCauley SR, et al. (2010) Evaluating the relationship between memory functioning and cingulum bundles in acute mild traumatic brain injury using diffusion tensor imaging. J Neurotrauma 27: 303-307 doi:10.1089/neu.2009.1110.
43. Zhuang L, Wen W, Zhu W, Trollor J, Kochan N, et al. (2010) White matter integrity in mild cognitive impairment: a tract-based spatial statistics study. Neuroimage 53: 16-25 doi:10.1016/j.neuroimage.2010.05.068.
44. van der Kogel AJ (1986) Radiation-induced damage in the central nervous system: an interpretation of target cell responses. Br J Cancer Suppl 7: 207-217.
45. Hattori T, Ito K, Aoki S, Yuasa T, Sato R, et al. (2012) White matter alteration in idiopathic normal pressure hydrocephalus: tract-based spatial statistics study. AJNR Am J Neuroradiol 33: 97-103.
46. Nonaka H, Akima M, Hatori T, Nagayama T, Zhang Z, et al. (2003) Microvasculature of the human cerebral white matter: arteries of the deep white matter. Neuropathology 23: 111-118.
47. Calvo W, Hopewell JW, Reinhold HS, Yeung TK, (1988) Time- and dose-related changes in the white matter of the rat brain after single doses of X rays. Br J Radiol 61: 1043-1052.
48. Hodges H, Katzung N, Sowinski P, Hopewell JW, Wilkinson JH, et al. (1998) Late behavioural and neuropathological effects of local brain irradiation in the rat. Behav Brain Res 91: 99-114.
49. Reinhold HS, Calvo W, Hopewell JW, van der Berg AP, (1990) Development of blood vessel-related radiation damage in the fimbria of the central nervous system. Int J Radiat Oncol Biol Phys 18: 37-42.
50. Miot-Noirault E, Akoka S, Hoffschir D, Pontvert D, Gaboriaud G, et al. (1996) Potential of T2 relaxation time measurements for early detection of radiation injury to the brain: experimental study in pigs. AJNR Am J Neuroradiol 17: 907-912.
51. Cao Y, (2011) The promise of dynamic contrast-enhanced imaging in radiation therapy. Semin Radiat Oncol 21: 147-156 doi:10.1016/j.semradonc.2010.11.001.
52. Yu JB, Shiao SL, Knisely JPS, (2007) A dosimetric evaluation of conventional helmet field irradiation versus two-field intensity-modulated radiotherapy technique. Int J Radiat Oncol Biol Phys 68: 621-631.
53. Richardson PG, Briemberg H, Jagannath S, Wen PY, Barlogie B, et al. (2006) Frequency, characteristics, and reversibility of peripheral neuropathy during treatment of advanced multiple myeloma with bortezomib. J Clin Oncol 24: 3113-3120.
54. Bokemeyer C, Berger CC, Kuczyk MA, Schmoll H, (1996) Evaluation of long-term toxicity after chemotherapy for testicular cancer. J Clin Oncol 11: 2923-2932.