Dementia in Down’s syndrome: an MRI comparison with Alzheimer’s disease in the general population

Journal of Neurodevelopmental Disorders

Volumn 5, Issue 1, 2013, Pages

  Mullins, Diane ^a,b   Daly, Eileen ^a   Simmons, Andrew ^a,c   Beacher, Felix ^a   Foy, Catherine ML ^a   Lovestone, Simon ^a,c   Hallahan, Brian ^d   Murphy, Kieran C ^b   Murphy, Declan G ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b BEAUMONT HOSPITAL   (Ireland)

^c SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Dementia; Imaging; Intellectual disability

Indexed keywords

EID: 84894031575     PISSN: 18661947     EISSN: 18661955     Source Type: Journal    
DOI: 10.1186/1866-1955-5-19     Document Type: Article

References (96)

1. Evans DA, Funkenstein HH, Albert MS, Scherr PA, Cook NR, Chown MJ, Helbert LE, Hennekens CH, Taylor JO: Prevalence of Alzheimer’s disease in a community population of older persons. Higher than previously reported. JAMA 1989, 262:2551–2556.
2. Mann DMA: Alzheimer’s disease and Down syndrome. Histopathology 1988, 13:125–137.
3. Prasher VP, Farrer MJ, Kessling AM, Fisher EM, West RJ, Barber PC, Butler AC: Molecular mapping of Alzheimer-type dementia in Down’s syndrome. Ann Neurol 1998, 43:380–383.
4. Folin M, Baiguera S, Conconi MT, Pati T, Grandi C, Parnigotto PP, Nussdorfer GG: The impact of risk factors of Alzheimer’s disease in the Down syndrome. Int J Mol Med 2003, 11:267–270.
5. Beacher F, Simmons A, Daly E, Prasher V, Adams C, Margallo-Lana ML, Morris R, Lovestone S, Murphy K, Murphy DG: Hippocampal myo-inositol and cognitive ability in adults with Down syndrome. An in vivo proton magnetic resonance spectroscopy study. Arch Gen Psychiatry 2005, 62:1360–1365.
6. Giesel FL, Hahn HK, Thomann PA, Widjaja E, Wignall E, von Tengg-Kobligk H, Pantel J, Griffiths PD, Peitgen HO, Schroder J, Essig M: Temporal horn index and volume of medial temporal lobe atrophy using a new semiautomated method for rapid and precise assessment. Am J Neuroradiol 2006, 27:1454–1458.
7. McLaurin J, Franklin T, Chakrabartty A, Fraser PE: Phosphatidylinositol and inositol involvement in Alzheimer amyloid-beta fibril growth and arrest. J Mol Biol 1998, 278:183–194.
8. Foy CML, Daly E, Glover A, O’Gorman R, Simmons A, Murphy DGM, Lovestone S: Hippocampal proton MR spectroscopy in early Alzheimer’s Disease and mild cognitive impairment. Brain Topogr 2001, 24:316–322.
9. Lamar M, Foy CML, Beacher F, Daly E, Poppe M, Archer N, Prasher V, Murphy KC, Morris RG, Simmons A, Lovestone S, Murphy DG: Down syndrome with and without dementia: an in vivo proton magnetic resonance spectroscopy study with implications for Alzheimer’s disease. Neuroimage 2011, 57:63–69.
10. Katzman R, Terry R, DeTeresa R, Brown T, Davies P, Fuld P, Renbing X, Peck A: Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol 1988, 23:138–144.
11. Setern Y: What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002, 8:448–460.
12. Stern YP: Cognitive reserve and Alzheimer’s disease. Alzheimer’s Dis Assoc Disord 2006, 20:69–74.
13. Melzer D, Ely M, Brayne C: Cognitive impairment in elderly people: population based estimate of the future in England. Scotland and Wales. BMJ 1997, 315:462.
14. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM: Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDS Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 1984, 34:939–944.
15. Jack CR Jr, Petersen RC, Xu YC, Waring SC, O’Brien PC, Tangalos EG, Smith GE, Ivnik RJ, Kokmen E: Medial temporal atrophy on MRI in normal aging and very mild Alzheimer’s disease. Neurology 1997, 49:786–794.
16. Leinsinger G, Teipel S, Wismuller A, Born C, Meindl T, Flatz W, Schonberg S, Pruessner J, Hampel H, Reiser M: Volumetric MRI for evaluation of regional pattern and progression of neocortical degeneration in Alzheimer’s disease. Radiologe 2003, 43:537–542.
17. Jack CR Jr, Shiung MM, Gunter JL, O’Brien PC, Weigand SD, Knopman DS, Boeve BF, Invik RJ, Smith GE, Cha RH, Tangalos EG, Petersen RC: Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology 2004, 62:591–600.
18. Devanand DP, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, Stern Y, Tabert MH, de Leon ML: Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 2007, 68:828–836.
19. Fox NC, Freeborough PA: Brain atrophy progression measured from registered serial MRI: validation and application to Alzheimer’s disease. JMRI 1997, 7:1069–1075.
20. Fox NC, Cousens S, Scahill R, Harvey RJ, Rossor MN: Using serial registered brain magnetic resonance imaging to measure disease progression in Alzheimer disease: power calculations and estimates of sample size to detect treatment effects. Arch Neurol 2000, 57:339–344.
21. Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, De Stefano N: Accurate, robust, and automated longitudinal and crosssectional brain change analysis. Neuroimage 2002, 17:479–489.
22. Schott JM, Price SL, Frost C, Whitwell JL, Rossor MN, Fox NC: Measuring atrophy in Alzheimer disease: a serial MRI study over 6 and 12 months. Neurology 2005, 65:119–124.
23. Westman E, Wahlund LO, Foy C, Poppe M, Cooper A, Murphy D, Spenger C, Lovestone S, Simmons A: Combining MRS and MRI measures to distinguish between Alzheimer’s disease and healthy controls. J Alzheimer’s Disease 2010, 22:171–181.
24. Westman E, Wahlund LO, Foy C, Poppe M, Cooper A, Murphy D, Spenger C, Lovestone S, Simmons A: Magnetic resonance imaging and magnetic resonance spectroscopy for detection of early Alzheimer’s disease. J Alzheimer’s Disease 2001, 26:307–319.
25. Bradley KM, Bydder GM, Budge MM, Hajnal JV, White SJ, Ripley BD, Smith AD: Serial brain MRI at 3–6 month intervals as a surrogate marker for Alzheimer’s disease. Br J Radiol 2002, 75:506–513.
26. Wang D, Chalk JB, Rose SE, de Zubicaray G, Cowin G, Galloway GJ, Barnes D, Spooner D, Doddrell MD, Semple J: MR image-based measurement of rates of change in volumes of brain structures part II: application to a study of Alzheimer’s disease and normal aging. Magn Reson Imaging 2002, 20:41–48.
27. Silbert LC, Quinn JF, Moore MM, Corbridge E, Ball MJ, Murdoch G, Sexton G, Kaye JA: Changes in premorbid brain volume predict Alzheimer’s disease pathology. Neurology 2003, 61:487–492.
28. Thompson PM, Hayashi KM, De Zubicaray GI, Janke AL, Rose SE, Semple J, Kong MS, Herman DH, Gravano D, Doddrell DM, Toga AW: Mapping hippocampal and ventricular change in Alzheimer disease. Neuroimage 2004, 22:1754–1766.
29. Carmichael OT, Kuller LH, Lopez OL, Thompson PM, Dutton RA, Lu A, Lee SE, Lee YJ, Aizenstein HJ, Meltzer CC, Liu Y, Toga AW, Becker JT: Ventricular volume and dementia progression in the cardiovascular health study. Neurobiol Aging 2007, 28:389–397.
30. Fleisher AS, Sun S, Taylor C, Ward CP, Gamst AC, Petersen RC, Jack CR Jr, Aisen PS, Thal LJ: Volumetric MRI vs clinical predictors of Alzheimer disease in mild cognitive impairment. Neurology 2008, 70:191–199.
31. Xanthakos S, Krishnan KR, Kim DM, Charles HC: Magnetic resonance imaging of Alzheimer’s disease. Prog Neuropsychopharmacol Biol Psychiatry 1996, 20:597–626.
32. Kesslak JP, Nagata SF, Lott I, Nalciogly O: MRI analysis of age-related changes in the brains of individuals with Down’s syndrome. Neurology 1994, 44:1039–1045.
33. Pearlson GD, Breiter SN, Aylward EH, Warren AC, Grygorcewicz M, Frangou S, Barta PE, Pulsifer MB: MRI brain changes in subjects with Down syndrome with and without dementia. Dev Med Child Neurol 1998, 40:326–334.
34. Aylward EH, Li Q, Honeycutt NA, Warren AC, Pulsifer MB, Barta PE, Chan MD, Smith PD, Jerram M, Pearlson GD: MRI volumes of the hippocampus and amygdala in adults with Down’s syndrome with and without dementia. Am J Psychiatry 1990, 156:564–568.
35. Prasher V, Cumella S, Natarajan K, Rolfe E, Shah S, Haque MS: Magnetic resonance imaging, Down’s syndrome and Alzheimer’s disease: research and clinical implications. JIDR 2003, 47:90–100.
36. Beacher F, Daly E, Simmons A, Prasher V, Morris R, Robinson C, Lovestone S, Murphy K, Murphy DG: Alzheimer’s disease and Down’s syndrome: an in vivo MRI study. Psychol Med 2009, 39:675–683.
37. Hon J, Huppert F, Holland A, Watson P: Neuropsychological assessment of older adults with Down’s syndrome: an epidemiological study using the Cambridge Cognitive Examination (CAMCOG). Br J Clin Psych 1999, 38:155–165.
38. Blessed G, Black SE, Butler T, Kay DW: The diagnosis of dementia in the elderly. A comparison of CAMCOG (the cognitive section of CAMDEX), the AGECAT program, DSM-III, the Mini-Mental State Examination and some short rating scales. Br J Psychiatry 1991, 159:193–198.
39. Simmons A, Arridge SR, Barker GJ, Williams SC: Stimulation of MRI cluster plots and application to neurological segmentation. Magn Reson Imaging 1996, 14:73–92.
40. Simmons A, Westman E, Muehlboeck S, Mecocci P, Vellas B, Tsolaki M, Kloszewska I, Wahlund LO, Soininen H, Lovestone S, Evans A, Spenger C: AddNeuroMed Consortium. MRI measures of Alzheimer’s disease and the AddNeuroMed study. Ann NY Acad Sci 2009, 1180:47–55.
41. Simmons A, Westman E, Muehlboeck S, Mecocci P, Vellas B, Tsolaki M, Kloszewska I, Wahlund LO, Soininen H, Lovestone S, Evans A, Spenger C: The AddNeuroMed framework for multi-centre MRI assessment of Alzheimer’s disease: experience from the first 24 months. Int J Geriatr Psychiatry 2011, 26:75–82.
42. Barta PE, Dhingra L, Royall R, Schwartz E: Efficient estimates for the volume of structures identified in three-dimensional arrays of spatial data. J Neurosci Methods 1997, 75:111–118.
43. Murphy DGM, DeCarli C, McIntosh AR, Daly E, Mentis MJ, Pietrini P, Szcepanik J, Schapiro MB, Grady CL, Horowitz B, Rapoport SI: Sex differences in human brain morphometry and metabolism: an in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. Arch Gen Psychiatry 1996, 53:585–594.
44. Murphy DGM, DeCarli C, Daly E, Haxby JV, Allen G, White BJ, McIntosh AR, Powell CM, Horowitz B, Rapoport SI, Schapiro MB: X-chromosome effects on female brain: a magnetic resonance imaging study of Turner’s syndrome. Lancet 1993, 342:1197–2000.
45. Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A, Olivier A, Melnson D, Leroux G: Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992, 42:1743–1750.
46. Bartko JJ, Carpenter WT: On the methods and theory of reliability. J Nervous Ment Disease 1986, 163:307–317.
47. Wisniewski KE, Dalton AJ, McLachlan C, Wen GY, Wisniewski HM: Alzheimer’s disease in Down’s syndrome: clinicopathologic studies. Neurology 1985, 35:957–961.
48. Oliver C, Holland AJ: Down’s syndrome and Alzheimer’s disease: a review. Psychol Med 1986, 16:307–322.
49. Lott IT, Head E: Down syndrome and Alzheimer’s disease: a link between development and aging. Ment Retard Dev Disabil Res Rev 2001, 7:172–178.
50. Raz N, Torres IJ, Briggs SD, Spencer WD, Thornton AE, Loken WJ, Gunning FM, McQuain JD, Driesen NR, Acker JD: Selective neuroanatomic abnormalities in Down’s syndrome and their cognitive correlates: evidence from MRI morphometry. Neurology 1995, 45:356–366.
51. Aylward EH, Qiang L, Honeycutt NA, Warren AC, Pulsifer MB, Barta PE, Chan MD, Smith PD, Jerram M, Pearlson GD: MRI volumes of the hippocampus and amygdala in adults with Down’s syndrome with and without dementia. Am J Psychiatry 1999, 156:564–568.
52. Beacher F, Daly E, Simmons A, Prasher V, Morris R, Robinson C, Lovestone S, Murphy K, Murphy DG: Brain anatomy and ageing in non-demented adults with Down’s syndrome: an in vivo MRI study. Psychol Med 2010, 40:611–619.
53. Double KL, Halliday GM, Kril JJ, Harasty JA, Cullen K, Brooks WS, Creasey H, Broe GA: Topography of brain atrophy during normal ageing and AD. Neurobiol Aging 1996, 17:513–521.
54. Karas GB, Burton EJ, Rombouts SA, van Schijndel RA, O’Brien JT, Scheltens P, McKeith IG, Williams D, Ballard C, Barkhof F: A comprehensive study of gray matter loss in patients with Alzheimer’s disease using optimized voxel-based morphometry. Neuroimage 2003, 18:895–907.
55. Pennanen C, Kivipelto M, Tuomainen S, Hartikainen P, Hanninen T, Laakso MP, Hallikainen M, Vanhanen M, Nissinen A, Helkala EL, Vainio P, Vanninen R, Partanen K, Soininen H: Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiol Aging 2004, 25:303–310.
56. Hessl D, Rivera S, Koldewyn K, Cordeiro L, Adams J, Tassone F, Hagerman PJ, Hagerman RJ: Amygdala dysfunction in men with the fragile X premutation. Brain 2007, 130:404–416.
57. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss A, Amaral DG: The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neuroscience 2004, 24:6392–6401.
58. Krasuski JS, Alexander GE, Horwitz B, Rapoport SI, Schapiro MB: Relation of medial temporal lobe volumes to age and memory function in nondemented adults with Down’s syndrome: implications for the prodromal phase of Alzheimer’s disease.Am J Psychiatry 2002, 159:74–81.
59. Pinter JD, Brown WE, Eliez S, Schmitt JE, Capone GT, Reiss AL: Amygdala and hippocampal volumes in children with Down Syndrome: a highresolution MRI study. Neurology 2001, 56:972–974.
60. Teipel SJ, Schapiro MB, Alexander GE, Krasuski JS, Horwitz B, Hoehne C, Moller HJ, Rapoport SI, Hampel H: Relation of corpus callosum and hippocampal size to age in non-demented adults with Down’s syndrome. Am J Psychiatry 2003, 160:1870–1878.
61. Ball MJ, Schapiro MB, Rapoport SI: Neuropathological relationships between Down syndrome and senile dementia Alzheimer type. In Neurobiology of Down syndrome. Edited by Epstein C. New York: Raven Press; 1986:45–58.
62. Mann DMA, Esiri MM: The pattern of acquisition of plaques and tangles in the brains of patients under 50 years of age with Down’s syndrome. J Neurol Sci 1989, 89:169–179.
63. Hof PR, Bouras C, Perl DP, Sparks L, Mehta N, Morrison JH: Age-related distribution of neuropathologic changes in the cerebral cortex of patients with Down’s syndrome: quantative regional analysis and comparison with Alzheimer’s disease. Arch Neurol 1995, 52:379–391.
64. Hyman BT, West HL, Rebeck GW, Lai F, Mann DMA: Neuropathological changes in Down’s syndrome hippocampal formation: effect of age and apolipoprotein E genotype. Arch Neurol 1995, 52:373–378.
65. Laakso MP, Soininen H, Partanen K, Helkala EL, Hartikainen P, Vainio P, Hallikainen M, Hanninen T, Riekkinen PJ Sr: Volumes of hippocampus, amygdala and frontal lobes in the MRI-based diagnosis of early Alzheimer’s disease: correlation with memory functions. J Neural Transm 1995, 9:73–86.
66. Yamaguchi S, Meguro K, Shimada M, Ishizaki J, Yamadori A, Sekita Y: Five year retrospective changes in hippocampal atrophy and cognitive screening test performances in very mild Alzheimer’s disease: the Tajiri project. Neuroradiology 2002, 44:43–48.
67. Seab JB, Jagust WJ, Wong STS, Roos MS, Reed BR, Budinger TF: Quantitative NMR measurements of hippocampal atrophy in Alzheimer’s disease. Magn Reson Med 1988, 8:200–208.
68. Mega MS, Thompson PM, Toga AW, Cummings JL: Brain mapping in dementia. In Brain mapping: the disorders. Edited by Mazziotta J, Frackowiak RSJ, Toga A. San Diego: Academic Press; 2000:217–239.
69. Fox NC, Rossor MN: Diagnosis of early Alzheimer’s disease. Rev Neurol 1999, 155(suppl 4):S33–S37.
70. Celsis P: Age-related cognitive decline, mild cognitive impairment or preclinical Alzheimer’s disease? Ann Med 2000, 32:6–14.
71. Scheltens P: Early diagnosis of dementia: neuroimaging. J Neurol 1999, 246:16–20.
72. Jack CR Jr, Dickson DW, Parisi JE, Xu YC, Cha RH, O’Brien PC, Edland SD, Smith GE, Boeve BF, Tangalos EG, Kokmen E, Petersen RC: Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 2002, 58:750–757.
73. Riekkinen P Jr, Kejonen K, Laakso MP, Soininen H, Partanen K, Riekkinen M: Hippocampal atrophy is related to impaired memory, but not frontal functions in non-demented Parkinson’s disease patients. Neuroreport 1998, 9:1507–1511.
74. Gosche KM, Mortimer JA, Smith CD, Markesbery WR, Snowdon DA: Hippocampal volume as an index of Alzheimer neuropathology: findings from the Nun study. Neurology 2002, 58:1476–1482.
75. Kesslak JP, Nalcioglu O, Cotman CW: Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer’s disease. Neurology 1991, 41:51–54.
76. Pearlson GD, Harris GJ, Powers RE: Quantitative changes in mesial temporal volume, regional cerebral blood flow, and cognition in Alzheimer’s disease. Arch Gen Psychiatry 1992, 49:402–408.
77. Jack CR Jr, Petersen RC, O’Brien PC, Tangalos EG: MR-based hippocampal volumetry in the diagnosis of Alzheimer’sdisease.Neurology 1992, 42:183–188.
78. Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, Jolesz F: Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer’s disease. Arch Neurol 1993, 50:949–954.
79. Convit A, de Leon MJ, Golomb J, George AE, Tarshish CY, Bobinski M, Tsui W, De Santi S, Wegiel J, Wisniewski H: Hippocampal atrophy in early Alzheimer’s disease, anatomic specificity and validation. Psychiatr Q 1993, 64:371–387.
80. Lehericy S, Baulac M, Chiras J, Pierot L, Martin N, Pillon B, Deweer B, Dubois B, Marsault C: Amygdalohippocampal MR volume measurements in the early stages of Alzheimer disease. Am J Neuroradiol 1994, 15:929–937.
81. Squire LR, Zola-Morgan S: The medial temporal lobe memory system. Science 1991, 20:1380–1386.
82. Rombouts S, Machielsen W, Witter M, Barkhof F, Lindeboom J, Scheltens P: Visual association encoding activates the medial temporal lobe: a functional magnetic resonance imaging study. Hippocampus 1997, 7:594–601.
83. Storandt M, Hill R: Very mild senile dementia of the Alzheimer type-II Psychometric test performance. Arch Neurol 1989, 46:383–386.
84. Petersen RC, Smith GE, Ivnik RJ, Tangalos EG: Memory function in very early Alzheimer’s disease. Neurology 1994, 44:867–872.
85. Storandt M, Hill R: Very mild senile dementia of the Alzheimer type-II Psychometric test performance. Arch Neurol 1989, 46:383–386.
86. Tierney M, Szalai J, Snow W: Prediction of probable Alzheimer’s disease in memory impaired patients. Neurology 1996, 46:661–665.
87. Bowen J, Teri L, Kukull W, McCormick W, McCurry S, Larson E: Progression to dementia in patients with isolated memory loss. Lancet 1997, 349:763–765.
88. De Leon M, George A, Convit A, Tarshish CY, McRae T, De Santi S, Smith G, Ferris SH, Noz M, Rusinek H: The radiologic prediction of Alzheimer disease: the atrophic hippocampal formation. Am J Neuroradiol 1993, 14:897–906.
89. Kaye JA, Swihart T, Howieson D, Dame A, Moore MM, Karnost T, Camicioli R, Ball M, Oken B, Sexton G: Volume loss of the hippocampus and temporal lobe in healthy elderly persons destined to develop dementia. Neurology 1997, 48:1297–1304.
90. Fox NC, Freeborough PA, Rossor MN: Visualisation and quantification of rates of atrophy in Alzeheimer’s disease. Lancet 1996, 348:94–97.
91. Meng X, D’Arch C: Education and Dementia in the context of the cognitive research hypothesis: a systematic review with meta-analysis and qualitative analyses. PLoS One 2012, 7:e38268.
92. Temple V, Jozsvai E, Konstantareas MM, Hewitt TA: Alzheimer’s dementia in Down’s syndrome: the relevance of cognitive ability. J Intell Dis Res 2001, 45:47–55.
93. Golomb J, Kluger A, de Leon M, Ferris SH, Mittelman M, Cohen J, George AE: Hippocampal formation size predicts declining memory performance in normal aging. Neurology 1996, 47:810–813.
94. Aylward EH, Li Q, Habbak QR, Warren A, Pulsifer MB, Barta PE, Jerram M, Pearlson G: Basal ganglia volume in adults with Down syndrome. Psychiatry Res 1997, 74:73–82.
95. Teipel SJ, Alexander GE, Schapiro MB, Moller HJ, Rapoport SI, Hampel H: Age-related cortical grey matter reductions in non-demented Down’s syndrome adults determined by MRI with voxel-based morphometry. Brain 2004, 127:811–824.
96. Coppus A, Evenhuis H, Verberne GJ, Visser F, van Gool P, Eikelenboom P, van Duijin C: Dementia and mortality in persons with Down’s syndrome. JIDR 2006, 50:768–777.