Skip to main content
Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2003 Oct;74(10):1371–1381. doi: 10.1136/jnnp.74.10.1371

Neuroimaging tools to rate regional atrophy, subcortical cerebrovascular disease, and regional cerebral blood flow and metabolism: consensus paper of the EADC

G Frisoni 1, P Scheltens 1, S Galluzzi 1, F Nobili 1, N Fox 1, P Robert 1, H Soininen 1, L Wahlund 1, G Waldemar 1, E Salmon 1
PMCID: PMC1757396  PMID: 14570828

Abstract

Neuroimaging is a mainstay in the differential diagnosis of patients with cognitive impairment. The often equivocal clinical pictures, the prognostic uncertainty of the earliest stages of mild cognitive impairment, and the subtle brain changes mean that neuroimaging techniques are of potentially great incremental diagnostic value. A number of methods, ranging from very simple subjective visual ratings to highly sophisticated computerised tools, have been developed, which allow rating of structural and functional brain changes. The choice of the method is not obvious, and current guidelines provide no indications on which tools should be preferred. In this paper, we give indications for tools with demonstrated accuracy for detecting regional atrophy, cerebrovascular disease, and regional brain function, and discuss these according to increasing technological complexity, ranging from those with high feasibility that can be used at the patient's bedside to highly technological ones that require trained personnel and specific hardware and software.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnáiz E., Jelic V., Almkvist O., Wahlund L. O., Winblad B., Valind S., Nordberg A. Impaired cerebral glucose metabolism and cognitive functioning predict deterioration in mild cognitive impairment. Neuroreport. 2001 Mar 26;12(4):851–855. doi: 10.1097/00001756-200103260-00045. [DOI] [PubMed] [Google Scholar]
  2. Ashburner J., Friston K. J. Voxel-based morphometry--the methods. Neuroimage. 2000 Jun;11(6 Pt 1):805–821. doi: 10.1006/nimg.2000.0582. [DOI] [PubMed] [Google Scholar]
  3. Ashburner John, Csernansky John G., Davatzikos Christos, Fox Nick C., Frisoni Giovanni B., Thompson Paul M. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol. 2003 Feb;2(2):79–88. doi: 10.1016/s1474-4422(03)00304-1. [DOI] [PubMed] [Google Scholar]
  4. Benson R. R., Guttmann C. R. G., Wei X., Warfield S. K., Hall C., Schmidt J. A., Kikinis R., Wolfson L. I. Older people with impaired mobility have specific loci of periventricular abnormality on MRI. Neurology. 2002 Jan 8;58(1):48–55. doi: 10.1212/wnl.58.1.48. [DOI] [PubMed] [Google Scholar]
  5. Chan D., Fox N. C., Jenkins R., Scahill R. I., Crum W. R., Rossor M. N. Rates of global and regional cerebral atrophy in AD and frontotemporal dementia. Neurology. 2001 Nov 27;57(10):1756–1763. doi: 10.1212/wnl.57.10.1756. [DOI] [PubMed] [Google Scholar]
  6. Chetelat Gaël, Baron Jean-Claude. Early diagnosis of Alzheimer's disease: contribution of structural neuroimaging. Neuroimage. 2003 Feb;18(2):525–541. doi: 10.1016/s1053-8119(02)00026-5. [DOI] [PubMed] [Google Scholar]
  7. Chételat G., Desgranges B., de la Sayette V., Viader F., Eustache F., Baron J-C. Mild cognitive impairment: Can FDG-PET predict who is to rapidly convert to Alzheimer's disease? Neurology. 2003 Apr 22;60(8):1374–1377. doi: 10.1212/01.wnl.0000055847.17752.e6. [DOI] [PubMed] [Google Scholar]
  8. De Santi S., de Leon M. J., Rusinek H., Convit A., Tarshish C. Y., Roche A., Tsui W. H., Kandil E., Boppana M., Daisley K. Hippocampal formation glucose metabolism and volume losses in MCI and AD. Neurobiol Aging. 2001 Jul-Aug;22(4):529–539. doi: 10.1016/s0197-4580(01)00230-5. [DOI] [PubMed] [Google Scholar]
  9. DeCarli C., Maisog J., Murphy D. G., Teichberg D., Rapoport S. I., Horwitz B. Method for quantification of brain, ventricular, and subarachnoid CSF volumes from MR images. J Comput Assist Tomogr. 1992 Mar-Apr;16(2):274–284. doi: 10.1097/00004728-199203000-00018. [DOI] [PubMed] [Google Scholar]
  10. DeCarli C., Miller B. L., Swan G. E., Reed T., Wolf P. A., Carmelli D. Cerebrovascular and brain morphologic correlates of mild cognitive impairment in the National Heart, Lung, and Blood Institute Twin Study. Arch Neurol. 2001 Apr;58(4):643–647. doi: 10.1001/archneur.58.4.643. [DOI] [PubMed] [Google Scholar]
  11. DeCarli C., Murphy D. G., Tranh M., Grady C. L., Haxby J. V., Gillette J. A., Salerno J. A., Gonzales-Aviles A., Horwitz B., Rapoport S. I. The effect of white matter hyperintensity volume on brain structure, cognitive performance, and cerebral metabolism of glucose in 51 healthy adults. Neurology. 1995 Nov;45(11):2077–2084. doi: 10.1212/wnl.45.11.2077. [DOI] [PubMed] [Google Scholar]
  12. Denihan A., Wilson G., Cunningham C., Coakley D., Lawlor B. A. CT measurement of medial temporal lobe atrophy in Alzheimer's disease, vascular dementia, depression and paraphrenia. Int J Geriatr Psychiatry. 2000 Apr;15(4):306–312. doi: 10.1002/(sici)1099-1166(200004)15:4<306::aid-gps111>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  13. Du A. T., Schuff N., Amend D., Laakso M. P., Hsu Y. Y., Jagust W. J., Yaffe K., Kramer J. H., Reed B., Norman D. Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease. J Neurol Neurosurg Psychiatry. 2001 Oct;71(4):441–447. doi: 10.1136/jnnp.71.4.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Erkinjuntti T., Inzitari D., Pantoni L., Wallin A., Scheltens P., Rockwood K., Roman G. C., Chui H., Desmond D. W. Research criteria for subcortical vascular dementia in clinical trials. J Neural Transm Suppl. 2000;59:23–30. doi: 10.1007/978-3-7091-6781-6_4. [DOI] [PubMed] [Google Scholar]
  15. Fazekas F., Kleinert R., Offenbacher H., Schmidt R., Kleinert G., Payer F., Radner H., Lechner H. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology. 1993 Sep;43(9):1683–1689. doi: 10.1212/wnl.43.9.1683. [DOI] [PubMed] [Google Scholar]
  16. Fox N. C., Cousens S., Scahill R., Harvey R. J., Rossor M. N. 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 Mar;57(3):339–344. doi: 10.1001/archneur.57.3.339. [DOI] [PubMed] [Google Scholar]
  17. Fox N. C., Crum W. R., Scahill R. I., Stevens J. M., Janssen J. C., Rossor M. N. Imaging of onset and progression of Alzheimer's disease with voxel-compression mapping of serial magnetic resonance images. Lancet. 2001 Jul 21;358(9277):201–205. doi: 10.1016/S0140-6736(01)05408-3. [DOI] [PubMed] [Google Scholar]
  18. Fox N. C., Freeborough P. A. Brain atrophy progression measured from registered serial MRI: validation and application to Alzheimer's disease. J Magn Reson Imaging. 1997 Nov-Dec;7(6):1069–1075. doi: 10.1002/jmri.1880070620. [DOI] [PubMed] [Google Scholar]
  19. Fox N. C., Freeborough P. A., Rossor M. N. Visualisation and quantification of rates of atrophy in Alzheimer's disease. Lancet. 1996 Jul 13;348(9020):94–97. doi: 10.1016/s0140-6736(96)05228-2. [DOI] [PubMed] [Google Scholar]
  20. Fox N. C., Scahill R. I., Crum W. R., Rossor M. N. Correlation between rates of brain atrophy and cognitive decline in AD. Neurology. 1999 May 12;52(8):1687–1689. doi: 10.1212/wnl.52.8.1687. [DOI] [PubMed] [Google Scholar]
  21. Fox N. C., Warrington E. K., Freeborough P. A., Hartikainen P., Kennedy A. M., Stevens J. M., Rossor M. N. Presymptomatic hippocampal atrophy in Alzheimer's disease. A longitudinal MRI study. Brain. 1996 Dec;119(Pt 6):2001–2007. doi: 10.1093/brain/119.6.2001. [DOI] [PubMed] [Google Scholar]
  22. Frisoni G. B., Beltramello A., Weiss C., Geroldi C., Bianchetti A., Trabucchi M. Linear measures of atrophy in mild Alzheimer disease. AJNR Am J Neuroradiol. 1996 May;17(5):913–923. [PMC free article] [PubMed] [Google Scholar]
  23. Frisoni G. B. Structural imaging in the clinical diagnosis of Alzheimer's disease: problems and tools. J Neurol Neurosurg Psychiatry. 2001 Jun;70(6):711–718. doi: 10.1136/jnnp.70.6.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Frisoni Giovanni B., Geroldi Cristina, Beltramello Alberto, Bianchetti Angelo, Binetti Giuliano, Bordiga Giovanni, DeCarli Charles, Laakso Mikko P., Soininen Hilkka, Testa Cristina. Radial width of the temporal horn: a sensitive measure in Alzheimer disease. AJNR Am J Neuroradiol. 2002 Jan;23(1):35–47. [PMC free article] [PubMed] [Google Scholar]
  25. Frisoni Giovanni B., Rossi Roberta, Beltramello Alberto. The radial width of the temporal horn in mild cognitive impairment. J Neuroimaging. 2002 Oct;12(4):351–354. doi: 10.1111/j.1552-6569.2002.tb00143.x. [DOI] [PubMed] [Google Scholar]
  26. Gao F. Q., Black S. E., Leibovitch F. S., Callen D. J., Lobaugh N. J., Szalai J. P. A reliable MR measurement of medial temporal lobe width from the Sunnybrook Dementia Study. Neurobiol Aging. 2003 Jan-Feb;24(1):49–56. doi: 10.1016/s0197-4580(02)00013-1. [DOI] [PubMed] [Google Scholar]
  27. Ge Yulin, Grossman Robert I., Babb James S., Rabin Marcie L., Mannon Lois J., Kolson Dennis L. Age-related total gray matter and white matter changes in normal adult brain. Part I: volumetric MR imaging analysis. AJNR Am J Neuroradiol. 2002 Sep;23(8):1327–1333. [PMC free article] [PubMed] [Google Scholar]
  28. Goethals Ingeborg, Van De Wiele Christophe, Slosman Daniel, Dierckx Rudi. Brain SPET perfusion in early Alzheimer's disease: where to look? Eur J Nucl Med Mol Imaging. 2002 Aug;29(8):975–978. doi: 10.1007/s00259-002-0872-8. [DOI] [PubMed] [Google Scholar]
  29. Herholz K., Salmon E., Perani D., Baron J. C., Holthoff V., Frölich L., Schönknecht P., Ito K., Mielke R., Kalbe E. Discrimination between Alzheimer dementia and controls by automated analysis of multicenter FDG PET. Neuroimage. 2002 Sep;17(1):302–316. doi: 10.1006/nimg.2002.1208. [DOI] [PubMed] [Google Scholar]
  30. Hillman B. J. Medical imaging in the 21st century. Lancet. 1997 Sep 6;350(9079):731–733. doi: 10.1016/S0140-6736(97)04570-4. [DOI] [PubMed] [Google Scholar]
  31. Holloway Frank. Outcome measurement in mental health--welcome to the revolution. Br J Psychiatry. 2002 Jul;181:1–2. doi: 10.1192/bjp.181.1.1. [DOI] [PubMed] [Google Scholar]
  32. Jack C. R., Jr, Bentley M. D., Twomey C. K., Zinsmeister A. R. MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. Radiology. 1990 Jul;176(1):205–209. doi: 10.1148/radiology.176.1.2353093. [DOI] [PubMed] [Google Scholar]
  33. Jack C. R., Jr, Petersen R. C., Xu Y. C., O'Brien P. C., Smith G. E., Ivnik R. J., Boeve B. F., Waring S. C., Tangalos E. G., Kokmen E. Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology. 1999 Apr 22;52(7):1397–1403. doi: 10.1212/wnl.52.7.1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jagust W., Thisted R., Devous M. D., Sr, Van Heertum R., Mayberg H., Jobst K., Smith A. D., Borys N. SPECT perfusion imaging in the diagnosis of Alzheimer's disease: a clinical-pathologic study. Neurology. 2001 Apr 10;56(7):950–956. doi: 10.1212/wnl.56.7.950. [DOI] [PubMed] [Google Scholar]
  35. Jobst K. A., Smith A. D., Barker C. S., Wear A., King E. M., Smith A., Anslow P. A., Molyneux A. J., Shepstone B. J., Soper N. Association of atrophy of the medial temporal lobe with reduced blood flow in the posterior parietotemporal cortex in patients with a clinical and pathological diagnosis of Alzheimer's disease. J Neurol Neurosurg Psychiatry. 1992 Mar;55(3):190–194. doi: 10.1136/jnnp.55.3.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Jobst K. A., Smith A. D., Szatmari M., Esiri M. M., Jaskowski A., Hindley N., McDonald B., Molyneux A. J. Rapidly progressing atrophy of medial temporal lobe in Alzheimer's disease. Lancet. 1994 Apr 2;343(8901):829–830. doi: 10.1016/s0140-6736(94)92028-1. [DOI] [PubMed] [Google Scholar]
  37. Jobst K. A., Smith A. D., Szatmari M., Molyneux A., Esiri M. E., King E., Smith A., Jaskowski A., McDonald B., Wald N. Detection in life of confirmed Alzheimer's disease using a simple measurement of medial temporal lobe atrophy by computed tomography. Lancet. 1992 Nov 14;340(8829):1179–1183. doi: 10.1016/0140-6736(92)92890-r. [DOI] [PubMed] [Google Scholar]
  38. Johnson K. A., Jones K., Holman B. L., Becker J. A., Spiers P. A., Satlin A., Albert M. S. Preclinical prediction of Alzheimer's disease using SPECT. Neurology. 1998 Jun;50(6):1563–1571. doi: 10.1212/wnl.50.6.1563. [DOI] [PubMed] [Google Scholar]
  39. Klunk William E., Wang Yanming, Huang Guo-feng, Debnath Manik L., Holt Daniel P., Shao Li, Hamilton Ronald L., Ikonomovic Milos D., DeKosky Steven T., Mathis Chester A. The binding of 2-(4'-methylaminophenyl)benzothiazole to postmortem brain homogenates is dominated by the amyloid component. J Neurosci. 2003 Mar 15;23(6):2086–2092. doi: 10.1523/JNEUROSCI.23-06-02086.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Knopman D. S., DeKosky S. T., Cummings J. L., Chui H., Corey-Bloom J., Relkin N., Small G. W., Miller B., Stevens J. C. Practice parameter: diagnosis of dementia (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2001 May 8;56(9):1143–1153. doi: 10.1212/wnl.56.9.1143. [DOI] [PubMed] [Google Scholar]
  41. Laakso M. P., Frisoni G. B., Könönen M., Mikkonen M., Beltramello A., Geroldi C., Bianchetti A., Trabucchi M., Soininen H., Aronen H. J. Hippocampus and entorhinal cortex in frontotemporal dementia and Alzheimer's disease: a morphometric MRI study. Biol Psychiatry. 2000 Jun 15;47(12):1056–1063. doi: 10.1016/s0006-3223(99)00306-6. [DOI] [PubMed] [Google Scholar]
  42. Laakso M. P., Partanen K., Riekkinen P., Lehtovirta M., Helkala E. L., Hallikainen M., Hanninen T., Vainio P., Soininen H. Hippocampal volumes in Alzheimer's disease, Parkinson's disease with and without dementia, and in vascular dementia: An MRI study. Neurology. 1996 Mar;46(3):678–681. doi: 10.1212/wnl.46.3.678. [DOI] [PubMed] [Google Scholar]
  43. Laakso M. P., Soininen H., Partanen K., Lehtovirta M., Hallikainen M., Hänninen T., Helkala E. L., Vainio P., Riekkinen P. J., Sr MRI of the hippocampus in Alzheimer's disease: sensitivity, specificity, and analysis of the incorrectly classified subjects. Neurobiol Aging. 1998 Jan-Feb;19(1):23–31. doi: 10.1016/s0197-4580(98)00006-2. [DOI] [PubMed] [Google Scholar]
  44. Lobotesis K., Fenwick J. D., Phipps A., Ryman A., Swann A., Ballard C., McKeith I. G., O'Brien J. T. Occipital hypoperfusion on SPECT in dementia with Lewy bodies but not AD. Neurology. 2001 Mar 13;56(5):643–649. doi: 10.1212/wnl.56.5.643. [DOI] [PubMed] [Google Scholar]
  45. Lopez O. L., Becker J. T., Jungreis C. A., Rezek D., Estol C., Boller F., DeKosky S. T. Computed tomography--but not magnetic resonance imaging--identified periventricular white-matter lesions predict symptomatic cerebrovascular disease in probable Alzheimer's disease. Arch Neurol. 1995 Jul;52(7):659–664. doi: 10.1001/archneur.1995.00540310029012. [DOI] [PubMed] [Google Scholar]
  46. Lopez O. L., Becker J. T., Klunk W., Saxton J., Hamilton R. L., Kaufer D. I., Sweet R. A., Cidis Meltzer C., Wisniewski S., Kamboh M. I. Research evaluation and diagnosis of possible Alzheimer's disease over the last two decades: II. Neurology. 2000 Dec 26;55(12):1863–1869. doi: 10.1212/wnl.55.12.1863. [DOI] [PubMed] [Google Scholar]
  47. Lopez O. L., Becker J. T., Klunk W., Saxton J., Hamilton R. L., Kaufer D. I., Sweet R. A., Cidis Meltzer C., Wisniewski S., Kamboh M. I. Research evaluation and diagnosis of probable Alzheimer's disease over the last two decades: I. Neurology. 2000 Dec 26;55(12):1854–1862. doi: 10.1212/wnl.55.12.1854. [DOI] [PubMed] [Google Scholar]
  48. Matsuda H. Cerebral blood flow and metabolic abnormalities in Alzheimer's disease. Ann Nucl Med. 2001 Apr;15(2):85–92. doi: 10.1007/BF02988596. [DOI] [PubMed] [Google Scholar]
  49. Messa C., Perani D., Lucignani G., Zenorini A., Zito F., Rizzo G., Grassi F., Del Sole A., Franceschi M., Gilardi M. C. High-resolution technetium-99m-HMPAO SPECT in patients with probable Alzheimer's disease: comparison with fluorine-18-FDG PET. J Nucl Med. 1994 Feb;35(2):210–216. [PubMed] [Google Scholar]
  50. Middelkoop H. A., van der Flier W. M., Burton E. J., Lloyd A. J., Paling S., Barber R., Ballard C., McKeith I. G., O'Brien J. T. Dementia with Lewy bodies and AD are not associated with occipital lobe atrophy on MRI. Neurology. 2001 Dec 11;57(11):2117–2120. doi: 10.1212/wnl.57.11.2117. [DOI] [PubMed] [Google Scholar]
  51. Nobili Flavio, Koulibaly Malick, Vitali Paolo, Migneco Octave, Mariani Giuliano, Ebmeier Klaus, Pupi Alberto, Robert Philippe H., Rodriguez Guido, Darcourt Jacques. Brain perfusion follow-up in Alzheimer's patients during treatment with acetylcholinesterase inhibitors. J Nucl Med. 2002 Aug;43(8):983–990. [PubMed] [Google Scholar]
  52. O'Brien J. T., Ames D., Desmond P., Lichtenstein M., Binns D., Schweitzer I., Davis S., Tress B. Combined magnetic resonance imaging and single-photon emission tomography scanning in the discrimination of Alzheimer's disease from age-matched controls. Int Psychogeriatr. 2001 Jun;13(2):149–161. doi: 10.1017/s1041610201007554. [DOI] [PubMed] [Google Scholar]
  53. O'Brien J., Ames D., Chiu E., Schweitzer I., Desmond P., Tress B. Severe deep white matter lesions and outcome in elderly patients with major depressive disorder: follow up study. BMJ. 1998 Oct 10;317(7164):982–984. doi: 10.1136/bmj.317.7164.982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Okamura Nobuyuki, Arai Hiroyuki, Maruyama Masahiro, Higuchi Makoto, Matsui Toshifumi, Tanji Haruko, Seki Takashi, Hirai Hisao, Chiba Hiroshi, Itoh Masatoshi. Combined Analysis of CSF Tau Levels and [(123)I]Iodoamphetamine SPECT in Mild Cognitive Impairment: Implications for a Novel Predictor of Alzheimer's Disease. Am J Psychiatry. 2002 Mar;159(3):474–476. doi: 10.1176/appi.ajp.159.3.474. [DOI] [PubMed] [Google Scholar]
  55. Pantoni L., Leys D., Fazekas F., Longstreth W. T., Jr, Inzitari D., Wallin A., Filippi M., Scheltens P., Erkinjuntti T., Hachinski V. Role of white matter lesions in cognitive impairment of vascular origin. Alzheimer Dis Assoc Disord. 1999 Oct-Dec;13 (Suppl 3):S49–S54. [PubMed] [Google Scholar]
  56. Pearlson G. D., Harris G. J., Powers R. E., Barta P. E., Camargo E. E., Chase G. A., Noga J. T., Tune L. E. Quantitative changes in mesial temporal volume, regional cerebral blood flow, and cognition in Alzheimer's disease. Arch Gen Psychiatry. 1992 May;49(5):402–408. doi: 10.1001/archpsyc.1992.01820050066012. [DOI] [PubMed] [Google Scholar]
  57. Perani D. The role of emission tomography in dementia. Ital J Neurol Sci. 1999;20(5 Suppl):S254–S257. doi: 10.1007/s100729970007. [DOI] [PubMed] [Google Scholar]
  58. Petrella Jeffrey R., Coleman R. Edward, Doraiswamy P. Murali. Neuroimaging and early diagnosis of Alzheimer disease: a look to the future. Radiology. 2003 Feb;226(2):315–336. doi: 10.1148/radiol.2262011600. [DOI] [PubMed] [Google Scholar]
  59. Reiman E. M., Caselli R. J., Chen K., Alexander G. E., Bandy D., Frost J. Declining brain activity in cognitively normal apolipoprotein E epsilon 4 heterozygotes: A foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3334–3339. doi: 10.1073/pnas.061509598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Riemenschneider M., Lautenschlager N., Wagenpfeil S., Diehl J., Drzezga A., Kurz A. Cerebrospinal fluid tau and beta-amyloid 42 proteins identify Alzheimer disease in subjects with mild cognitive impairment. Arch Neurol. 2002 Nov;59(11):1729–1734. doi: 10.1001/archneur.59.11.1729. [DOI] [PubMed] [Google Scholar]
  61. Rockwood K., Parhad I., Hachinski V., Erkinjuntti T., Rewcastle B., Kertesz A., Eastwood M. R., Phillips S. Diagnosis of vascular dementia: Consortium of Canadian Centres for Clinical Cognitive Research concensus statement. Can J Neurol Sci. 1994 Nov;21(4):358–364. doi: 10.1017/s0317167100040968. [DOI] [PubMed] [Google Scholar]
  62. Román G. C., Tatemichi T. K., Erkinjuntti T., Cummings J. L., Masdeu J. C., Garcia J. H., Amaducci L., Orgogozo J. M., Brun A., Hofman A. Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology. 1993 Feb;43(2):250–260. doi: 10.1212/wnl.43.2.250. [DOI] [PubMed] [Google Scholar]
  63. Sackett D. L., Haynes R. B. The architecture of diagnostic research. BMJ. 2002 Mar 2;324(7336):539–541. doi: 10.1136/bmj.324.7336.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Salmon Eric. Functional brain imaging applications to differential diagnosis in the dementias. Curr Opin Neurol. 2002 Aug;15(4):439–444. doi: 10.1097/00019052-200208000-00006. [DOI] [PubMed] [Google Scholar]
  65. Scheltens P., Erkinjunti T., Leys D., Wahlund L. O., Inzitari D., del Ser T., Pasquier F., Barkhof F., Mäntylä R., Bowler J. White matter changes on CT and MRI: an overview of visual rating scales. European Task Force on Age-Related White Matter Changes. Eur Neurol. 1998;39(2):80–89. doi: 10.1159/000007921. [DOI] [PubMed] [Google Scholar]
  66. Scheltens P., Launer L. J., Barkhof F., Weinstein H. C., Jonker C. The diagnostic value of magnetic resonance imaging and technetium 99m-HMPAO single-photon-emission computed tomography for the diagnosis of Alzheimer disease in a community-dwelling elderly population. Alzheimer Dis Assoc Disord. 1997 Jun;11(2):63–70. doi: 10.1097/00002093-199706000-00002. [DOI] [PubMed] [Google Scholar]
  67. Scheltens P., Leys D., Barkhof F., Huglo D., Weinstein H. C., Vermersch P., Kuiper M., Steinling M., Wolters E. C., Valk J. Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry. 1992 Oct;55(10):967–972. doi: 10.1136/jnnp.55.10.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Scheltens Philip, Fox Nick, Barkhof Frederik, De Carli Charles. Structural magnetic resonance imaging in the practical assessment of dementia: beyond exclusion. Lancet Neurol. 2002 May;1(1):13–21. doi: 10.1016/s1474-4422(02)00002-9. [DOI] [PubMed] [Google Scholar]
  69. Shoghi-Jadid Kooresh, Small Gary W., Agdeppa Eric D., Kepe Vladimir, Ercoli Linda M., Siddarth Prabha, Read Stephen, Satyamurthy Nagichettiar, Petric Andrej, Huang Sung-Cheng. Localization of neurofibrillary tangles and beta-amyloid plaques in the brains of living patients with Alzheimer disease. Am J Geriatr Psychiatry. 2002 Jan-Feb;10(1):24–35. [PubMed] [Google Scholar]
  70. Signorini M., Paulesu E., Friston K., Perani D., Colleluori A., Lucignani G., Grassi F., Bettinardi V., Frackowiak R. S., Fazio F. Rapid assessment of regional cerebral metabolic abnormalities in single subjects with quantitative and nonquantitative [18F]FDG PET: A clinical validation of statistical parametric mapping. Neuroimage. 1999 Jan;9(1):63–80. doi: 10.1006/nimg.1998.0381. [DOI] [PubMed] [Google Scholar]
  71. Silverman D. H., Small G. W., Chang C. Y., Lu C. S., Kung De Aburto M. A., Chen W., Czernin J., Rapoport S. I., Pietrini P., Alexander G. E. Positron emission tomography in evaluation of dementia: Regional brain metabolism and long-term outcome. JAMA. 2001 Nov 7;286(17):2120–2127. doi: 10.1001/jama.286.17.2120. [DOI] [PubMed] [Google Scholar]
  72. Skovronsky D. M., Zhang B., Kung M. P., Kung H. F., Trojanowski J. Q., Lee V. M. In vivo detection of amyloid plaques in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7609–7614. doi: 10.1073/pnas.97.13.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Small Gary W., Agdeppa Eric D., Kepe Vladimir, Satyamurthy Nagichettiar, Huang Sung-Cheng, Barrio Jorge R. In vivo brain imaging of tangle burden in humans. J Mol Neurosci. 2002 Dec;19(3):323–327. doi: 10.1385/jmn:19:3:321. [DOI] [PubMed] [Google Scholar]
  74. Smith Stephen M., Zhang Yongyue, Jenkinson Mark, Chen Jacqueline, Matthews P. M., Federico Antonio, De Stefano Nicola. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage. 2002 Sep;17(1):479–489. doi: 10.1006/nimg.2002.1040. [DOI] [PubMed] [Google Scholar]
  75. Snowdon D. A., Greiner L. H., Mortimer J. A., Riley K. P., Greiner P. A., Markesbery W. R. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA. 1997 Mar 12;277(10):813–817. [PubMed] [Google Scholar]
  76. Tonkonogy J. M., Geller J. L. Late-onset paranoid psychosis as a distinct clinicopathologic entity: magnetic resonance imaging data in elderly patients with paranoid psychosis of late onset and schizophrenia of early onset. Neuropsychiatry Neuropsychol Behav Neurol. 1999 Oct;12(4):230–235. [PubMed] [Google Scholar]
  77. Van Laere Koenraad J., Warwick James, Versijpt Jan, Goethals Ingeborg, Audenaert Kurt, Van Heerden Ben, Dierckx Rudi. Analysis of clinical brain SPECT data based on anatomic standardization and reference to normal data: an ROC-based comparison of visual, semiquantitative, and voxel-based methods. J Nucl Med. 2002 Apr;43(4):458–469. [PubMed] [Google Scholar]
  78. Visser P. J., Verhey F. R. J., Hofman P. A. M., Scheltens P., Jolles J. Medial temporal lobe atrophy predicts Alzheimer's disease in patients with minor cognitive impairment. J Neurol Neurosurg Psychiatry. 2002 Apr;72(4):491–497. doi: 10.1136/jnnp.72.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Wahlund L. O., Barkhof F., Fazekas F., Bronge L., Augustin M., Sjögren M., Wallin A., Ader H., Leys D., Pantoni L. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001 Jun;32(6):1318–1322. doi: 10.1161/01.str.32.6.1318. [DOI] [PubMed] [Google Scholar]
  80. Wahlund L. O., Julin P., Johansson S. E., Scheltens P. Visual rating and volumetry of the medial temporal lobe on magnetic resonance imaging in dementia: a comparative study. J Neurol Neurosurg Psychiatry. 2000 Nov;69(5):630–635. doi: 10.1136/jnnp.69.5.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Waldemar G., Bruhn P., Kristensen M., Johnsen A., Paulson O. B., Lassen N. A. Heterogeneity of neocortical cerebral blood flow deficits in dementia of the Alzheimer type: a [99mTc]-d,l-HMPAO SPECT study. J Neurol Neurosurg Psychiatry. 1994 Mar;57(3):285–295. doi: 10.1136/jnnp.57.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Waldemar G., Dubois B., Emre M., Scheltens P., Tariska P., Rossor M. Diagnosis and management of Alzheimer's disease and other disorders associated with dementia. The role of neurologists in Europe. European Federation of Neurological Societies. Eur J Neurol. 2000 Mar;7(2):133–144. doi: 10.1046/j.1468-1331.2000.00030.x. [DOI] [PubMed] [Google Scholar]
  83. Woermann F. G., Free S. L., Koepp M. J., Ashburner J., Duncan J. S. Voxel-by-voxel comparison of automatically segmented cerebral gray matter--A rater-independent comparison of structural MRI in patients with epilepsy. Neuroimage. 1999 Oct;10(4):373–384. doi: 10.1006/nimg.1999.0481. [DOI] [PubMed] [Google Scholar]
  84. Zijlmans J. C., Thijssen H. O., Vogels O. J., Kremer H. P., Poels P. J., Schoonderwaldt H. C., Merx J. L., van 't Hof M. A., Thien T., Horstink M. W. MRI in patients with suspected vascular parkinsonism. Neurology. 1995 Dec;45(12):2183–2188. doi: 10.1212/wnl.45.12.2183. [DOI] [PubMed] [Google Scholar]
  85. de Leon M. J., Convit A., Wolf O. T., Tarshish C. Y., DeSanti S., Rusinek H., Tsui W., Kandil E., Scherer A. J., Roche A. Prediction of cognitive decline in normal elderly subjects with 2-[(18)F]fluoro-2-deoxy-D-glucose/poitron-emission tomography (FDG/PET). Proc Natl Acad Sci U S A. 2001 Aug 28;98(19):10966–10971. doi: 10.1073/pnas.191044198. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Neurology, Neurosurgery, and Psychiatry are provided here courtesy of BMJ Publishing Group

RESOURCES