Accumulation of iron in the putamen predicts its shrinkage in healthy older adults: A multi-occasion longitudinal study

NeuroImage

Volumn 128, Issue , 2016, Pages 11-20

  Daugherty, Ana M ^a   Raz, Naftali ^a,b  

^a WAYNE STATE UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Oxidative stress; R2*; Striatum; Susceptibility weighted imaging

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM ANTAGONIST; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; IRON;

ADULT; AGE; AGED; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; CARDIOVASCULAR RISK; CAUDATE NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HYPERTENSION; IRON STORAGE; LONGITUDINAL STUDY; MALE; NEOSTRIATUM; PREDICTION; PRIORITY JOURNAL; PUTAMEN; AGING; METABOLISM; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; FEMALE; HUMANS; IRON; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OXIDATIVE STRESS; PUTAMEN;

EID: 84954304574     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.12.045     Document Type: Article

References (81)

1. Adamo D.E., Daugherty A.M., Raz N. Brain iron content and grasp force-matching ability in older women. Brain Imaging Behav. 2014, 8(4):579-587.
2. 2 relaxation tiem in patients with Parkinson's disease. Neurology 1993, 43:697-700.
3. Aquino D., Bizzi A., Grisoli M., Garavaglia B., Bruzzone M.G., Nardocci N., Savoiardo M., Chiapparini L. Age-related iron deposition in the basal ganglia: quantitative analysis in healthy subjects. Radiology 2009, 252(1):165-172.
4. Bartzokis G., Lu P., Tingus K., Peters D.G., Amar C.P., Tishler T.A., Finn J.P., Willablanca P., Altshuler L.L., Mintz J., Neely E., Connor J.R. Gender and iron genes may modify associations between brain iron and memory in healthy aging. Neuropsychopharmacology 2011, 36:1375-1384.
5. Bartzokis G., Mintz J., Sultzer D., Marx P., Herzberg J.S., Phelan C.K., Marder S.R. In vivo MR evaluation of age-related increases in brain iron. AJNR 1994, 15(6):1129-1138.
6. Berry C., Brosnan M.J., Fennel J., Hamilton C.A., Dominiczak A.F. Oxidative stress and vascular damage in hypertension. Curr. Opin. Nephrol. Hypertens. 2001, 10(2):247-255.
7. Blasco G., Puig J., Daunis-I-Estadella J., Molina X.L., Xifra G., Fernández-Aranda F., Pedraza S., Ricart W., Portero-Otín M., Fernández-Real J. Brain iron overload, insulin resistance and cognitive performance in obese subjects: a preliminary MRI case-control study. Diabetes Care 2014, 37(11):3076-3083.
8. Brown G.C., Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 2012, 12(1):1-4.
9. Cherubini A., Péran P., Caltagirone C., Sabatini U., Spalletta G. Aging of subcortical nuclei: microstructural, mineralization and atrophy modifications measured in vivo using MRI. NeuroImage 2009, 48:29-36.
10. Daugherty A., Raz N. Age-related differences in iron content of subcortical nuclei observed in vivo: a meta-analysis. NeuroImage 2013, 70:113-121.
11. Daugherty A.M., Raz N. Appraising the role of iron in brain aging and cognition: promises and limitations of MRI. Neuropsychol. Rev. 2015, 25(3):272-287.
12. Daugherty A.M., Haacke E.M., Raz N. Striatal iron content predicts its shrinkage and changes in working memory after two years in healthy adults. J. Neurosci. 2015, 35(17):6731-6743.
13. Dröge W., Schipper H.M. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 2007, 6:361-370.
14. Finch C.E., Crimmins E.M. Inflammatory exposure and historical changes in human life-spans. Science 2004, 305:1736-1739.
15. Finch C.E., Foster J.R., Mirsky A.E. Ageing and the regulation of cell activities during exposure to cold. J. Gen. Physiol. 1969, 54:690-712.
16. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psych. Res. 1975, 12:189-198.
17. Fukunaga M., Li T.Q., van Gelderen P., de Zwart J.A., Shmueli K., Yao B., Lee J., Maric D., Aronova M.A., Zhang G., Leapman R.D., Schenck J.F., Merkle H., Duyn J.H. Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3834-3839.
18. Ghadery C., Pirpamer L., Hofer E., Langkammer C., Petrovic K., Loitfelder M., Schwingenschuh P., Seiler S., Duering M., Jouvent E., Schmidt H., Fazekas F., Mangin J.F., Chabriat H., Dichgans M., Ropele S., Schmidt R. R2* mapping for brain iron: associations with cognition in normal aging. Neurobiol. Aging 2015, 36:925-932.
19. Glasser M.F., Van Essen D.C. Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. J. Neurosci. 2011, 31(32):11597-11616.
20. Görlach A., Dimova E.Y., Petry A., Martínez-Ruiz A., Hernansanz-Agustín P., Rolo A.P., Palmeira C.M., Kietzmann T. Reactive oxygen species, nutrition, hypoxia and diseases: problems solved?. Redox Biol. 2015, 6:372-385.
21. Grammas P. Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. J. Neuroinflammation 2011, 8:26.
22. Haacke E.M., Cheng N.Y.C., House M.J., Liu Q., Neelaavalli J., Ogg R.J., Khan A., Ayaz M., Kirsch W., Obenaus A. Imaging iron stores in the brain using magnetic resonance imaging. Magn. Reson. Imaging 2005, 23(1):1-25.
23. Haacke E.M., Liu S., Busch S., Zheng W., Wu D., Ye Y. Quantitative susceptibility mapping: current status and future directions. Magn. Reson. Imaging 2015, 33:1-25.
24. Haacke E.M., Miao Y., Liu M., Habib C.A., Katkuri Y., Liu T., Yang Z., Lang Z., Hu J., Wu J. Correlation of putative iron content as represented by changes in R2* and phase with age in deep gray matter of healthy adults. J. Magn. Reson. Imaging 2010, 32:561-576.
25. Hallgren B., Sourander P. The effect of age on the non-haemin iron in the human brain. J. Neurochem. 1958, 3:41-51.
26. Halliwell B. Iron and damage to biomolecules. Iron and Human Disease 1992, 209-236. CRC Press, Roca Baton (FL). Lauffer (Ed.).
27. Hare D., Ayton S., Bush A., Lei P. A delicate balance: iron metabolism and diseases of the brain. Front. Aging Neurosci. 2013, 5:34.
28. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11(3):298-300.
29. Hayes A.F., Scharkow M. The relative trustworthiness of inferential tests of the indirect effect in statistical mediation analysis: does method really matter?. Psychol. Sci. 2013, 24:1918-1927.
30. Hertzog C., Lindenberger U., Ghisletta P., von Oertzen T. On the power of multivariate latent growth curve models to detecting correlated change. Psychol. Methods 2006, 11(3):244-252.
31. Horn J.L., McArdle J.J. A practical and theoretical approach to measurement invariance in aging research. Exp. Aging Res. 1992, 18:117-144.
32. Jack C.R., Twomey C.K., Zinsmeister A.R., Sharbrough F.W., Petersen R.C., Cascino G.D. Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 1989, 172:549-554.
33. Janaway B.M., Simpson J.E., Hoggard N., Highley J.R., Forster G., Drew D., Gebril O.H., Matthews F.E., Bryane C., Wharton S.B., Ince P.G., MRC Cognitive Function and Ageing Neuropathology Study Brain haemosiderin in older people: pathological evidence for an ischemic origin of magnetic resonance imaging (MRI) microbleeds. Neuropathol. Appl. Neurobiol. 2014, 40(3):258-269.
34. Langkammer C., Schweser F., Krebs N., Deistung A., Goessler W., Scheurer E., Sommer K., Reishofer G., Yen K., Fazekas F., Ropele S., Reichenbach J.R. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. NeuroImage 2012, 62:1593-1599.
35. Larsen R. Missing data imputation versus full information maximum likelihood with second-level dependencies. Struct. Equ. Model. 2011, 18(4):649-662.
36. Lehmann D.J., Worwood M., Ellis R., Wimhurst V.L.J., Merryweather-Clarke A.T., Warden D.R., Smith A.D., Robson K.J.H. Iron genes, iron load and risk of Alzheimer's disease. J. Med. Genet. 2006, 43.
37. Li W., Yu B., Batrachenko A., Bancroft-Wu V., Morey R.A., Shashi V., Langkammer C., De Bellis M.D., Ropele S., Song A.W., Liu C. Differential developmental trajectories of magnetic susceptibility in human brain gray and white matter over the lifespan. Hum. Brain Mapp. 2014, 35(6):2698-2713.
38. Lindenberger U., von Oertzen T., Ghisletta P., Hertzog C. Cross-sectional age variance extraction: what's change got to do with it?. Psychol. Aging 2011, 26(1):34-47.
39. Liu C., Li W., Johnson A., Wu B. High-field (9.4T) MRI of brain dysmyelination by quantitative mapping of magnetic susceptibility. NeuroImage 2011, 56:930-938.
40. Loitfelder M., Seiler S., Schwingenschuh P., Schmidt R. Cerebral microbleeds: a review. Panminerva Med. 2012, 54(3):149-160.
41. Maxwell S.E., Cole D.A. Bias in cross-sectional analyses of longitudinal mediation. Psychol. Methods 2007, 12(1):23-44.
42. Mills E., Dong X., Wang F., Xu H. Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future Med. Chem. 2010, 2(1):51-72.
43. Morita R., Yoshii M., Nakajima K., Kohsaka T., Miki M., Torizuka K. Clinical evaluation of serum ferritin to iron ratio in malignant diseases. Eur. J. Nucl. Med. 1981, 6(7):331-336.
44. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417(1):1-13.
45. Muthén B., Kaplan D., Hollis M. On structural equation modeling with data that are not missing completely at random. Psychometrika 1987, 52:431-462.
46. Naderi S., Colakoglu Z., Lüleci G. Calcification of basal ganglia associated with pontine calcification in four cases: a radiologic and genetic study. Clin. Neurol. Neurosurg. 1993, 95:155-157.
47. Nandar W., Connor J.R. HFE gene variants affect iron in the brain. J. Nutr. 2011, 141:729S-739S.
48. Oldfield R.C. The assessment and analysis of handedness. Neuropsychologica 1971, 9:97-113.
49. Pearl J. Interpretation and identification of causal mediation. Psychol. Methods 2014, 19:459-481.
50. Pearl J. Reply to commentary by Imai, Keele, Tingley, and Yamamoto, concerning causal mediation analysis. Psychol. Methods 2014, 19:488-492.
51. Penke L., Hernandéz M.C.V., Maniega S.M., Gow A.J., Murray C., Starr J.M., Bastin M.E., Deary I.J., Wardlaw J.M. Brain iron deposits are associated with general cognitive ability and cognitive aging. Neurobiol. Aging 2012, 33:510-517.
52. Peran P., Cherubini A., Luccichenti G., Hagberg G., Démont J.-F., Rascol O., Celsis P., Caltagirone C., Spalletta G., Sabatini U. Volume and iron content in the basal ganglia and thalamus. Hum. Brain Mapp. 2009, 30:2667-2675.
53. Pfefferbaum A., Adalsteinsson E., Rohlfing T., Sullivan E.V. Diffusion tensor imaging of deep gray matter brain structures: effects of age and iron concentration. Neurobiol. Aging 2010, 31(3):482-500.
54. Preacher K.J., Wichman A.L., MacCallum R.C., Briggs N.E. Latent Growth Curve Modeling 2008, SAGE Publications, Inc., Thousand Oaks (CA).
55. Pujol J., Junque C., Vendrell P., Grau J.M., Marti-Vilalta J.L., Olivé C., Gili J. Biological significance of iron-related magnetic resonance imaging changes in the brain. Arch. Neurol. 1992, 49(7):711-717.
56. Radloff L.S. The CES-D scale: a self-report depression scale for research in the general population. J. Struct. Biol. 1977, 153:42-54.
57. Raykov T., Marcoulides G.A. A First Course in Structural Equation Modeling 2006, Lawrence Erlbaum, Mahwah (NJ). second ed.
58. Raz N., Kennedy K.M. A systems approach to the aging brain: Neuroanatomic changes, their modifiers, and cognitive correlates. Imaging the Aging Brain 2009, 43-70. Oxford University Press, New York (NY). W. Jagust, M. D'Esposito (Eds.).
59. Raz N., Lindenberger U. News of cognitive cure for age-related brain shrinkage is premature: a comment on burgmans et al., (2009). Neuropsychology 2011, 24(2):255-257.
60. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., Dahle C., Gerstorf D., Acker J.D. Regional brain changes in aging healthy adults: general trends, individual differences, and modifiers. Cereb. Cortex 2005, 15:1676-1689.
61. Raz N., Rodrigue K., Head D., Kennedy K., Acker J. Differential aging of the medial temporal lobe: a study of a five-year change. Neurology 2004, 62:433-439.
62. Raz N., Rodrigue K.M., Haacke E.M. Brain aging and its modifiers: insights from in vivo neuromophometry and susceptibility weighted imaging. Ann. NY Acad. Sci. 2007, 1097:84-93.
63. Rodrigue K.M., Daugherty A.M., Haacke E.M., Raz N. The role of hippocampal iron content and hippocampal volume in age-related differences in memory. Cereb. Cortex 2013, 23(7):1533-1541.
64. Rubin D.B. Causal inference using potential outcomes: design, modeling, decisions. J. Am. Stat. Assoc. 2005, 100:322-331.
65. Salgado J.C., Olivera-Nappa A., Gerdtzen Z.P., Tapia V., Theil E.C., Conca C., Nuñez M.T. Mathematical modeling of the dynamic storage of iron in ferritin. BMC Syst. Biol. 2010, 4:147.
66. Schenck J.F., Zimmerman E.A. High-field magnetic resonance imaging of brain iron: birth of a biomarker?. NMR Biomed. 2004, 17:433-445.
67. Serroyen J., Molenberghs G., Verbeke G., Davidian M. Non-linear models for longitudinal data. Am. Stat. 2009, 63(4):378-388.
68. Shrout P.E., Fleiss J.L. Intraclass correlations: uses in assessing raters reliability. Psychol. Bull. 1979, 86:420-428.
69. Sohal R.S., Orr W.C. The redox stress hypothesis of aging. Free Radic. Biol. Med. 2012, 52(3):539-555.
70. Sullivan E.V., Adalsteinsson E., Rohlfing T., Pfefferbaum A. Relevance of iron deposition in deep gray matter brain structures of cognitive and motor performance in healthy elderly men and women: exploratory findings. Brain Imaging Behav. 2009, 3:167-175.
71. Thomas L.O., Boyko O.B., Anthony D.C., Burger P.C. MR detection of brain iron. Am. J. Neuroradiol. 1993, 14(5):1043-1048.
72. Ulla M., Bonny J.M., Ouchchane L., Rieu I., Claise B., Durif F. Is R2* a new MRI biomarker for the progression of Parkinson's disease? A longitudinal follow-up. PLoS ONE 2013, 8(3):e57904.
73. Urrutia P.J., Mena N.P., Núñez M.T. The interplay between iron accumulation, mitochondrial dysfunction, and inflammation during the execution step of neurodegenerative disorders. Front. Pharmacol. 2014, 5. (article 38).
74. Walsh A.J., Belvins G., Lebel R.M., Seres P., Emery D.J., Wilman A.H. Longitudinal MR imaging of iron in multiple sclerosis: an imaging marker of disease. Radiology 2014, 270(1):186-196.
75. Ward R.J., Zucca F.A., Duyn J.H., Crichton R.R., Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014, 13:1045-1060.
76. Wessling-Resnick M. Iron homeostasis and the inflammatory response. Annu. Rev. Nutr. 2010, 30:105-122.
77. Winship C., Morgan S.L. The estimation of causal effects from observational data. Annu. Rev. Sociol. 1999, 26:659-706.
78. Xu X., Wang Q., Zhang M. Age, gender, and hemispheric differences in iron deposition in the human brain: an in vivo MRI study. NeuroImage 2008, 40:35-42.
79. Yates P.A., Villemagne V.L., Ellis K.A., Desmond P.M., Masters C.L., Rowe C.C. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Front. Neurosci. 2014, 4:205.
80. Zecca L., Youdim M.B.H., Riederer P., Connor J.R., Crichton R.R. Iron, brain ageing and neurodegenerative disorders. Nat. Rev. 2004, 5:863-873.
81. Zhang S., Wang J., Song N., Xie J., Hiang H. Up-regulation of divalent metal transporter 1 is involved in 1-methyl-4-phenylpyridinium (MPP+)-induced apoptosis in MES23.5 cells. Neurobiol. Aging 2009, 30:1466-1476.