Hippocampal proton MR spectroscopy as a novel approach in the assessment of radiation injury and the correlation to neurocognitive function impairment: initial experiences
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
26474857
PubMed Central
PMC4609038
DOI
10.1186/s13014-015-0518-1
PII: 10.1186/s13014-015-0518-1
Knihovny.cz E-resources
- MeSH
- Biomarkers analysis MeSH
- Hippocampus radiation effects MeSH
- Kaplan-Meier Estimate MeSH
- Cognition Disorders diagnosis etiology MeSH
- Cranial Irradiation adverse effects MeSH
- Aspartic Acid analogs & derivatives analysis MeSH
- Middle Aged MeSH
- Humans MeSH
- Magnetic Resonance Spectroscopy methods MeSH
- Brain Neoplasms mortality radiotherapy secondary MeSH
- Neuropsychological Tests MeSH
- Memory MeSH
- Protons MeSH
- Radiation Injuries diagnosis MeSH
- Aged MeSH
- Check Tag
- Middle Aged MeSH
- Humans MeSH
- Male MeSH
- Aged MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Biomarkers MeSH
- Aspartic Acid MeSH
- N-acetylaspartate MeSH Browser
- Protons MeSH
BACKGROUND: The hippocampus is considered as the main radiosensitive brain structure responsible for postradiotherapy cognitive decline. We prospectively assessed correlation of memory change to hippocampal N-acetylaspartate (h-tNAA) concentration, a neuronal density and viability marker, by (1)H-MR spectroscopy focused on the hippocampus. METHODS: Patients with brain metastases underwent whole brain radiotherapy (WBRT) to a dose of 30 Gy in ten fractions daily. Pre-radiotherapy (1)H-MR spectroscopy focused on the h-tNAA concentration and memory testing was performed. Memory was evaluated by Auditory Verbal Learning Test (AVLT) and Brief Visuospatial Memory Test-Revised (BVMT-R). Total recall, recognition and delayed recall were reported. The both investigation procedures were repeated 4 months after WBRT and the h-tNAA and memory changes were correlated. RESULTS: Of the 20 patients, ten passed whole protocol. The h-tNAA concentration significantly decreased from pre-WBRT 8.9, 8.86 and 8.88 [mM] in the right, left and both hippocampi to 7.16, 7.65 and 7.4 after WBRT, respectively. In the memory tests a significant decrease was observed in AVLT total-recall, BVMT-R total-recall and BVMT-R delayed-recall. Weak to moderate correlations were observed between left h-tNAA and AVLT recognition and all BVMT-R subtests and between the right h-tNAA and AVLT total-recall. CONCLUSIONS: A significant decrease in h-tNAA after WBRT was proven by (1)H-MR spectroscopy as a feasible method for the in vivo investigation of radiation injury. Continuing patient recruitment focusing on other cognitive tests and metabolites is needed.
Department of Clinical Psychology St Anne's University Hospital Brno Pekarska 53 Brno Czech Republic
Department of Neurosurgery St Anne's University Hospital Brno Pekarska 53 656 91 Brno Czech Republic
See more in PubMed
Tabouret E, Chinot O, Metellus P, Tallet A, Viens P, Gonçalves A, et al. Recent trends in epidemiology of brain metastases: an overview. Anticancer Res. 2012;32:4655–62. PubMed
Laack NN, Brown PD. Cognitive sequelae of brain radiation in adults. Semin Oncol. 2004;31:702–13. doi: 10.1053/j.seminoncol.2004.07.013. PubMed DOI
Tallet AV, Azria D, Barlesi F, Spano J-P, Carpentier AF, Gonçalves A, et al. Neurocognitive function impairment after whole brain radiotherapy for brain metastases: actual assessment. Radiat Oncol. 2012;7:77. doi: 10.1186/1748-717X-7-77. PubMed DOI PMC
Gondi V, Pugh SL, Tome WA, Caine C, Corn B, Kanner A, et al. Preservation of Memory With Conformal Avoidance of the Hippocampal Neural Stem-Cell Compartment During Whole-Brain Radiotherapy for Brain Metastases (RTOG 0933): A Phase II Multi-Institutional Trial. J Clin Oncol. 2014;32(34):3810–6. doi: 10.1200/JCO.2014.57.2909. PubMed DOI PMC
Gondi V, Hermann BP, Mehta MP, Tomé WA. Hippocampal dosimetry predicts neurocognitive function impairment after fractionated stereotactic radiotherapy for benign or low-grade adult brain tumors. Int J Radiat Oncol Biol Phys. 2013;85:348–54. doi: 10.1016/j.ijrobp.2012.11.031. PubMed DOI
Suh JH. Hippocampal-Avoidance Whole-Brain Radiation Therapy: A New Standard for Patients With Brain Metastases? J Clin Oncol. 2014;32(34):3789–91. doi: 10.1200/JCO.2014.58.4367. PubMed DOI PMC
Brown PD, Pugh S, Laack NN, Wefel JS, Khuntia D, Meyers C, et al. Memantine for the prevention of cognitive dysfunction in patients receiving whole-brain radiotherapy: a randomized, double-blind, placebo-controlled trial. Neuro Oncol. 2013;15:1429–37. doi: 10.1093/neuonc/not114. PubMed DOI PMC
Kazda T, Jancalek R, Pospisil P, Sevela O, Prochazka T, Vrzal M, et al. Why and how to spare the hippocampus during brain radiotherapy: the developing role of hippocampal avoidance in cranial radiotherapy. Radiat Oncol. 2014;9:139. doi: 10.1186/1748-717X-9-139. PubMed DOI PMC
Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AMA. N-Acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol. 2007;81:89–131. doi: 10.1016/j.pneurobio.2006.12.003. PubMed DOI PMC
Greene-Schloesser D, Robbins ME, Peiffer AM, Shaw EG, Wheeler KT, Chan MD, et al. Radiation-induced brain injury: A review. Front Oncol. 2012;2:73. PubMed PMC
Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8:955–62. doi: 10.1038/nm749. PubMed DOI
Monje ML, Palmer T. Radiation injury and neurogenesis. Curr Opin Neurol. 2003;16:129–34. doi: 10.1097/00019052-200304000-00002. PubMed DOI
Sperduto PW, Berkey B, Gaspar LE, Mehta M, Curran W. A new prognostic index and comparison to three other indices for patients with brain metastases: an analysis of 1,960 patients in the RTOG database. Int J Radiat Oncol Biol Phys. 2008;70(2):510–4. doi: 10.1016/j.ijrobp.2007.06.074. PubMed DOI
Mrzílkova J, Koutela A, Kutova M, Patzelt M, Ibrahim I, Al-Kayssi D, et al. Hippocampal spatial position evaluation on MRI for research and clinical practice. PLoS One. 2014;9(12):e115174. doi: 10.1371/journal.pone.0115174. PubMed DOI PMC
Provencher SW. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 2001;14(4):260–4. doi: 10.1002/nbm.698. PubMed DOI
Jiru F, Skoch A, Wagnerova D, Dezortova M, Hajek M. jSIPRO - analysis tool for magnetic resonance spectroscopic imaging. Comput Methods Programs Biomed. 2013;112(1):173–88. doi: 10.1016/j.cmpb.2013.06.018. PubMed DOI
Jiru F, Skoch A, Klose U, Grodd W, Hajek M. Error images for spectroscopic imaging by LCModel using Cramer-Rao bounds. MAGMA. 2006;19(1):1–14. doi: 10.1007/s10334-005-0018-7. PubMed DOI
Koay E, Sulman EP. Management of brain metastasis: past lessons, modern management, and future considerations. Curr Oncol Rep. 2012;14(1):70–8. doi: 10.1007/s11912-011-0205-9. PubMed DOI
Kazda T, Pospíšil P, Doleželová H, Jančálek R, Slampa P. Whole brain radiotherapy: Consequences for personalized medicine. Rep Pract Oncol Radiother. 2013;18(3):133–8. doi: 10.1016/j.rpor.2013.03.002. PubMed DOI PMC
Rock EP, Fine HA, Meyers CA. Refining endpoints in brain tumor clinical trials. J Neurooncol. 2012;108(2):227–30. doi: 10.1007/s11060-012-0813-8. PubMed DOI
Taphoorn MJB, Klein M. Cognitive deficits in adult patients with brain tumours. Lancet Neurol. 2004;3(3):159–68. doi: 10.1016/S1474-4422(04)00680-5. PubMed DOI
Wong CS, Van der Kogel AJ. Mechanisms of radiation injury to the central nervous system: implications for neuroprotection. Mol Interv. 2004;4(5):273–84. doi: 10.1124/mi.4.5.7. PubMed DOI
Mehta MP, Gondi V, Tomé WA. Why avoid the hippocampus? A comprehensive review. Radiother Oncol. 2010;97(3):370–6. doi: 10.1016/j.radonc.2010.09.013. PubMed DOI PMC
Awad R, Fogarty G, Hong A, Kelly P, Ng D, Santos D, et al. Hippocampal avoidance with volumetric modulated arc therapy in melanoma brain metastases - the first Australian experience. Radiat Oncol. 2013;8:62. doi: 10.1186/1748-717X-8-62. PubMed DOI PMC
Mehta MP, Shapiro WR, Phan SC, Gervais R, Carrie C, Chabot P, et al. Motexafin gadolinium combined with prompt whole brain radiotherapy prolongs time to neurologic progression in non-small-cell lung cancer patients with brain metastases: results of a phase III trial. Int J Radiat Oncol Biol Phys. 2009;73(4):1069–76. doi: 10.1016/j.ijrobp.2008.05.068. PubMed DOI
Rooney JW, Laack NN. Pharmacological interventions to treat or prevent neurocognitive decline after brain radiation. CNS Oncol. 2013;2(6):531–41. doi: 10.2217/cns.13.60. PubMed DOI PMC
Kantarci K. Proton MRS in mild cognitive impairment. J Magn Reson Imaging. 2013;37(4):770–7. doi: 10.1002/jmri.23800. PubMed DOI PMC
Tumati S, Martens S, Aleman A. Magnetic resonance spectroscopy in mild cognitive impairment: systematic review and meta-analysis. Neurosci Biobehav Rev. 2013;37(10 Pt 2):2571–86. doi: 10.1016/j.neubiorev.2013.08.004. PubMed DOI
Targosz-Gajniak MG, Siuda JS, Wicher MM, Banasik TJ, Bujak MA, Augusciak-Duma AM, et al. Magnetic resonance spectroscopy as a predictor of conversion of mild cognitive impairment to dementia. J Neurol Sci. 2013;335(1–2):58–63. doi: 10.1016/j.jns.2013.08.023. PubMed DOI
Kantarci K, Weigand SD, Przybelski SA, Preboske GM, Pankratz VS, Vemuri P, et al. MRI and MRS predictors of mild cognitive impairment in a population-based sample. Neurology. 2013;81(2):126–33. doi: 10.1212/WNL.0b013e31829a3329. PubMed DOI PMC
Usenius T, Usenius JP, Tenhunen M, Vainio P, Johansson R, Soimakallio S, et al. Radiation-induced changes in human brain metabolites as studied by 1H nuclear magnetic resonance spectroscopy in vivo. Int J Radiat Oncol Biol Phys. 1995;33(3):719–24. doi: 10.1016/0360-3016(95)02011-Y. PubMed DOI
Estève F, Rubin C, Grand S, Kolodié H, Le Bas JF. Transient metabolic changes observed with proton MR spectroscopy in normal human brain after radiation therapy. Int J Radiat Oncol Biol Phys. 1998;40(2):279–86. doi: 10.1016/S0360-3016(97)00714-1. PubMed DOI
Movsas B, Li BS, Babb JS, Fowble BL, Nicolaou N, Gonen O, et al. Quantifying radiation therapy-induced brain injury with whole-brain proton MR spectroscopy: initial observations. Radiology. 2001;221(2):327–31. PubMed
Lee MC, Pirzkall A, McKnight TR, Nelson SJ. 1H-MRSI of radiation effects in normal-appearing white matter: dose-dependence and impact on automated spectral classification. J Magn Reson Imaging. 2004;19(4):379–88. doi: 10.1002/jmri.20017. PubMed DOI
Kaminaga T, Shirai K. Radiation-induced brain metabolic changes in the acute and early delayed phase detected with quantitative proton magnetic resonance spectroscopy. J Comput Assist Tomogr. 2005;29(3):293–7. doi: 10.1097/01.rct.0000161422.95625.8a. PubMed DOI
Sundgren PC, Nagesh V, Elias A, Tsien C, Junck L, Gomez Hassan DM, et al. Metabolic alterations: a biomarker for radiation-induced normal brain injury-an MR spectroscopy study. J Magn Reson Imaging. 2009;29(2):291–7. doi: 10.1002/jmri.21657. PubMed DOI PMC
Chawla S, Wang S, Kim S, Sheriff S, Lee P, Rengan R, et al. Radiation Injury to the Normal Brain Measured by 3D-Echo-Planar Spectroscopic Imaging and Diffusion Tensor Imaging: Initial Experience. J Neuroimaging. 2015;25(1):97–104. doi: 10.1111/jon.12070. PubMed DOI
Lee TM, Yip JT, Jones-Gotman M. Memory deficits after resection from left or right anterior temporal lobe in humans: a meta-analytic review. Epilepsia. 2002;43(3):283–91. doi: 10.1046/j.1528-1157.2002.09901.x. PubMed DOI
Patel SK, Wong AL, Wong FL, Breen EC, Hurria A, Smith M, et al. Inflammatory Biomarkers, Comorbidity, and Neurocognition in Women With Newly Diagnosed Breast Cancer. J Natl Cancer Inst. 2015;107(8):djv 131. doi: 10.1093/jnci/djv131. PubMed DOI PMC
Perssons J, Herlitz A, Engman J, Morell A, Sjölie D, Wikström J, et al. Remembering our origin: Gender differences in spatial memory are reflected in gender differences in hippocampal lateralization. Behav Brain Res. 2013;256(8):219–228. doi: 10.1016/j.bbr.2013.07.050. PubMed DOI
Sidhu MK, Stretton J, Winston GP, Symms M, Thompson PJ, Koepp MJ, et al. Memory fMRI predicts verbal memory decline after anterior temporal lobe resection: Gender differences in spatial memory are reflected in gender differences in hippocampal lateralization. Neurology. 2015;84(15):1512–1519. doi: 10.1212/WNL.0000000000001461. PubMed DOI PMC
Chang EL, Wefel JS, Hess KR, Allen PK, Lang FF, Kornguth DG, et al. Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol. 2009;10(11):1037–44. doi: 10.1016/S1470-2045(09)70263-3. PubMed DOI
