Relaxo-volumetric multispectral quantitative magnetic resonance imaging of the brain over the human lifespan: global and regional aging patterns

Magnetic Resonance Imaging

Volumn 27, Issue 7, 2009, Pages 895-906

  Saito, Naoko ^a   Sakai, Osamu ^a   Ozonoff, Al ^b   Jara, Hernán ^a,c  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^c Boston University   (United States)

Author keywords

Full human lifespan; Multispectral quantitative MRI; Relaxo volumetric brain aging patterns

Indexed keywords

ADOLESCENT; ADULT; AGED; AGING; ALGORITHM; ARTICLE; BRAIN; BRAIN SIZE; CEREBELLUM; CEREBROSPINAL FLUID; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; FEMALE; GRAY MATTER; HUMAN; IMAGE ANALYSIS; INFANT; KERNEL METHOD; LIFESPAN; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VOLUMETRY; WHITE MATTER;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ALGORITHMS; BRAIN; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; INFANT; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 68349125556     PISSN: 0730725X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mri.2009.05.006     Document Type: Article

References (65)

1. Ogg R.J., and Steen R.G. Age-related changes in brain T1 are correlated with iron concentration. Magn Reson Med 40 (1998) 749-753
2. Steen R.G., and Schroeder J. Age-related changes in the pediatric brain: proton T1 in healthy children and in children with sickle cell disease. Magn Reson Imaging 21 (2003) 9-15
3. Thornton J.S., Amess P.N., Penrice J., Chong W.K., Wyatt J.S., and Ordidge R.J. Cerebral tissue water spin-spin relaxation times in human neonates at 2.4 tesla: methodology and the effects of maturation. Magn Reson Imaging 17 9 (1999) 1289-1295
4. Counsell S.J., Kennea N.L., Herlihy A.H., Allsop J.M., Harrison M.C., Cowan F.M., et al. T2 relaxation values in the developing preterm brain. AJNR Am J Neuroradiol 24 (2003) 1654-1660
5. Ding X.Q., Kucinski T., Wittkugel O., Goebell E., Grzyska U., Gorg M., et al. Normal brain maturation characterized with age-related T2 relaxation times: an attempt to develop a quantitative imaging measure for clinical use. Invest Radiol 39 (2004) 740-746
6. Saito N., Sakai O., and Jara H. Global and regional brain ageing patterns over the human lifespan with T2 histogram. Book of Abstracts: Annual Meeting of 46th American Society of Neuroradiology (2008), ASNR, New Orleans (LA) 216
7. Raz N., Rodrigue K.M., and Haacke E.M. Brain aging and its modifiers insights from in vivo neuromorphometry and susceptibility weighted imaging. Ann N Y Acad Sci 1097 (2007) 84-93
8. Gideon P., Thomsen C., and Henriksen O. Increased self-diffusion of brain water in normal aging. J Magn Reson Imaging 4 (1994) 185-188
9. Helenius J., Soinne L., Perkio J., Salonen O., Kangasmaki A., Kaste M., et al. Diffusion-weighted MR imaging in normal human brains in various age groups. AJNR Am J Neuroradiol 23 (2002) 194-199
10. Naganawa S., Sato K., Katagiri T., Mimura T., and Ishigaki T. Regional ADC values of the normal brain: differences due to age, gender, and laterality. Eur Radiol 13 (2003) 6-11
11. Càmara E., Bodammer N., Rodríguez-Fornells A., and Tempelmann C. Age-related water diffusion changes in human brain: a voxel-based approach. NeuroImage 34 (2007) 1588-1599
12. Gattu R., Benson R.R., Myrtheunjayan B., Kennedy K., Raz N., Kou Z., et al. Aging and fractional anisotropy: global and regional results. Book of Abstracts: 16th Scientific Meeting & Exhibition of the International Society for Magnetic Resonance (2008), ISMRM, Toronto, Canada 71
13. Zhu D.C., Zacks R.T., and Slade J.M. Brain adaptations in normal aging evaluated with diffusion tensor imaging. Book of Abstracts: 16th Scientific Meeting & Exhibition of the International Society for Magnetic Resonance (2008), ISMRM, Toronto, Canada 257
14. Nusbaum A.O., Tang C.Y., Buchsbaum M.S., Wei T.C., and Atlas S.W. Regional and global changes in cerebral diffusion with normal aging. AJNR Am J Neuroradiol 22 (2001) 136-142
15. Mukherjee P., Miller J.H., Shimony J.S., Conturo T.E., Lee B.C.P., Almli C.R., et al. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology 221 (2001) 349-358
16. Forbes K.P.N., Pipe J.G., and Bird C.R. Changes in brain water diffusion during the 1st year of life. Radiology 222 (2002) 405-409
17. Pfefferbaum A., and Sullivan E.V. Increased brain white matter diffusivity in normal adult aging: relationship to anisotropy and partial voluming. Magn Reson Med 49 (2003) 953-961
18. Snook L., Paulson L.A., Roy D., Phillips L., and Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. NeuroImage 26 (2005) 1164-1173
19. Ardekani S., Kumar A., Bartzokis G., and Sinha U. Exploratory voxel-based analysis of diffusion indices and hemispheric asymmetry in normal aging. Magn Reson Imaging 25 (2007) 154-167
20. Ge Y., Grossman R.I., Babb J.S., Rabin M.L., Mannon L.J., and Kolson D.L. Age-related total gray matter and white matter changes in normal adult brain: Part II. Quantitative magnetization transfer ratio histogram analysis. AJNR Am J Neuroradiol 23 (2002) 1334-1341
21. Ropele S., Enzinger C., Reishofer G., Schmidt R., and Fazekas F. The impact of cerebrovascular risk factors on brain tissue changes: a MTI study. Book of Abstracts: 16th Scientific Meeting & Exhibition of the International Society for Magnetic Resonance (2008), ISMRM, Toronto, Canada 71
22. Biagi L., Abbruzzese A., Bianchi M.C., Alsop D.C., Guerra A.D., and Tosetti M. Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging 25 (2007) 696-702
23. Wang Z., Fernández-Seara M., Alsop D.C., Liu W.C., Flax J.F., Benasich A.A., et al. Assessment of functional development in normal infant brain using arterial spin labeled perfusion MRI. NeuroImage 39 (2008) 973-978
24. Larsson E.M., Englund E., Gyorffy-Wagner Z., Brun A., Cronqvist S., and Persson B. Regional differences in the proton magnetic resonance relaxation times T1 and T2 within the normal human brain. Acta Radiol Diagn 27 (1986) 231-234
25. Johnson G., Ormerod I.E.C., Barnes D., Tofts P.S., and MacManus D. Accuracy and precision in the measurement of relaxation times from nuclear magnetic resonance images. Br J Radiol 60 (1987) 143-153
26. Breger R.K., Yetkin F.Z., Fischer M.E., Papke R.A., Haughton V.M., and Rimm A.A. T1 and T2 in the cerebrum: correlation with age, gender, and demographic factors. Radiology 181 (1991) 545-547
27. Agartz I., Saaf J., Wahlund L.O., and Wetterberg L. T1 and T2 relaxation time estimates in the normal human brain. Radiology 181 (1991) 537-543
28. Engelbrecht V., Rassek M., Preiss S., Wald C., and Modder U. Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. AJNR Am J Neuroradiol 19 (1998) 1923-1929
29. Wansapura J.P., Holland S.K., Dunn R.S., and Ball W.S. NMR relaxation times in the human brain at 3.0 tesla. J Magn Reson Imaging 9 (1999) 531-538
30. Gelman N., Ewing J.R., Gorell J.M., Spickler E.M., and Solomon E.G. Interregional variation of longitudinal relaxation rates in human brain at 3.0 T: relation to estimated iron and water contents. Magn Reson Med 45 (2001) 71-79
31. Rovaris M., Iannucci G., Cercignani M., Sormani M.P., Stefano N.D., Gerevini S., et al. Age-related changes in conventional, magnetization transfer, and diffusion-tensor MR imaging findings: study with whole-brain tissue histogram analysis. Radiology 227 (2003) 731-738
32. Zhang L., Thomas K.M., Davidson M.C., Casey B.J., Heier L.A., and Ulug A.M. MR quantitation of volume and diffusion changes in the developing brain. AJNR Am J Neuroradiol 26 (2005) 45-49
33. Suzuki S., Sakai O., and Jara H. Combined volumetric T1, T2 and secular-T2 quantitative MRI of the brain: age-related global changes (preliminary results). Magn Reson Imaging 24 (2006) 877-887
34. Jara H., Sakai O., Mankal P., Irving R.P., and Norbash A.M. Multispectral quantitative magnetic resonance imaging of brain iron stores: a theoretical perspective. Top Magn Reson Imaging 17 (2006) 19-30
35. Saito N., Sakai O., and Jara H. Combined multi-spectral quantitative MRI and volumetry of the brain with the mixed-TSE pulse sequence and bisecting dual clustering segmentation: a technique for studying regional ageing patterns in large populations. Book of Abstracts: 16th Scientific Meeting & Exhibition of the International Society for Magnetic Resonance (2008), ISMRM, Toronto, Canada 257
36. Hasan K.M., Halphen C., Boska M.D., and Narayana P.A. Diffusion tensor metrics, T2 relaxation, and volumetry of the naturally aging human caudate nuclei in healthy young and middle-aged adults: possible implications for the neurobiology of human brain aging and disease. Magn Reson Med 59 (2008) 7-13
37. Cho S., Jones D., Reddick W.E., Ogg R.J., and Steen R.G. Establishing norms for age-related changes in proton T1 of human brain tissue in vivo. Magn Reson Imaging 15 10 (1997) 1133-1143
38. McLaughlin N.C.R., Paul R.H., Grieve S.M., Williams L.M., Laidlaw D., DiCarlo M., et al. Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan. Int J Devl Neurosci 25 (2007) 215-221
39. Hasan K.M., Ewing-Cobbs L., Kramer L.A., Fletcher J.M., and Narayana P.A. Diffusion tensor quantification of the macrostructure and microstructure of human midsagittal corpus callosum across the lifespan. NMR Biomed 21 (2008) 1094-1101
40. Hasan K.M., Kamali A., Iftikhar A., Kramer L.A., Papanicolaou A.C., Fletcher J.M., et al. Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan. Brain Res (2008) 10.1016/j.brainres.2008.10.026
41. Lebel C., Walker L., Leemans A., Phillips L., and Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. NeuroImage 40 (2008) 1044-1055
42. Whitlow C.T., Pollock J.M., Mussat-Whitlow B.J., Kraft R., Tan H., Burdette J.H., et al. Age-related changes in global rates of cerebral perfusion from birth to age 92: a magnetic resonance arterial spin labeling investigation. Book of Abstracts: 94th Scientific Assembly and Annual Meeting, Radiological Society of North America (2009), RSNA, Chicago (IL) 402
43. Blatter D.D., Bigler E.D., Gale S.D., Johnson S.C., Anderson C.V., Burnett B.M., et al. Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. AJNR Am J Neuroradiol 16 (1995) 241-251
44. Guttmann C.R.G., Jolesz F.A., Kikinis R., Killiany R.J., Moss M.B., Sandor T., et al. White matter changes with normal aging. Neurology 50 (1998) 972-978
45. Resnick S.M., Goldszal A.F., Davatzikos C., Golski S., Kraut M.A., Metter E.J., et al. One-year age changes in MRI brain volumes in older adults. Cereb Cortex 10 (2000) 464-472
46. Courchesne E., Chisum H.J., Townsend J., Cowles A., Covington J., Egaas B., et al. Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216 (2000) 672-682
47. Bartzokis G., Beckson M., Lu P.H., Nuechterlein K.H., Edwards N., and Mintz J. Age-related changes in frontal and temporal lobe volumes in men. A magnetic resonance imaging study. Arch Gen Psychiatry 58 (2001) 461-465
48. Jernigan T.L., Archibald S.L., Fennema-Notestine C., Gamst A.C., Stout J.C., Bonner J., et al. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol Aging 22 (2001) 581-594
49. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N.A., Friston K.J., and Frackowiak R.S.J. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 14 (2001) 21-36
50. Ge Y., Grossman R.I., Babb J.S., Rabin M.L., Mannon L.J., and Kolson D.L. Age-related total gray matter and white matter changes in normal adult brain: Part I. Volumetric MR imaging analysis. AJNR Am J Neuroradiol 23 (2002) 1327-1333
51. Hulshoff Pol H.E., Schnack H.G., Bertens M.G., van Haren N.E.M., van der Tweel I., Staal W.G., et al. Volume changes in gray matter in patients with schizophrenia. Am J Psychiatry 159 (2002) 244-250
52. Tisserand D.J., Pruessner J.C., Sanz Arigita E.J., van Boxtel M.P.J., Evans A.C., Jolles J., et al. Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. NeuroImage 17 (2002) 657-669
53. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15 (2005) 1676-1689
54. DeCarli C., Massaro J., Harvey D., Hald J., Tullberg M., Au R., et al. Measures of brain morphology and infarction in the Framingham Heart Study: establishing what is normal. Neurobiol Aging 26 (2005) 491-510
55. Mewes A.U.J., Hüppi P.S., Als H., Rybicki F.J., Inder T.E., McAnulty G.B., et al. Regional brain development in serial magnetic resonance imaging of low-risk preterm infants. Pediatrics 118 (2006) 23-33
56. Matsuzawa J., Matsui M., Konishi T., Noguchi K., Gur R.C., Bilker W., et al. Age-related volumetric changes of brain gray and white matter in healthy infants and children. Cereb Cortex 11 (2001) 335-342
57. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., and Toga A.W. Mapping cortical change across the human life span. Nat Neurosci 6 3 (2003) 309-315
58. Walhovd K.B., Fjell A.M., Reinvang I., Lundervold A., Dale A.M., Eilertsen D.E., et al. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26 (2005) 1261-1270
59. O'Donnel M., Gore J.C., and Adams W.J. Toward an automated analysis system for NMRI: efficient pulse sequence for simultaneous T1-T2 imaging. Med Phys 13 2 (1986) 182-190
60. Graumann R., Fischer H., and Oppelt A. A new pulse sequence (SMART) for determining T1 T2 simultaneously. Med Phys 13 5 (1986) 644-647
61. In den Kleef J.J., and Cuppen J.J. RLSQ T1, T2, and rho calculations, combining ratios and least squares. Magn Reson Med 5 6 (1987) 513-524
62. Schmitt P., Griswold M.A., Jacob P.M., Kotas M., Gulani V., Flentje M., et al. Inversion recovery TrueFISP: quantification of T1, T2, and spin density. Magn Reson Med 51 4 (2004) 661-667
63. Gulani V., Schmitt P., Griswold M., Webb A.G., and Jakob P.M. Towards a single-sequence neurologic magnetic resonance imaging examination: multiple-contrast images from an IR TrueFISP experiment. Investigative Radiology. 39 12 (2004) 767-774
64. Tofts P.S. Chapter 5, Section B: Windows into the brain: measuring MR parameters. In: Tofts P.S. (Ed). Quantitative MRI of the Brain: Measuring Changes Caused by Disease (2003), John Wiley & Sons, West Sussex, England 83-475
65. Sluimer J.D., van der Flier W.M., Karas G.B., Fox N.C., Scheltens P., Barkhof F., et al. Whole-brain atrophy rate and cognitive decline: longitudinal MR study of memory clinic patients. Radiology 248 (2008) 590-598