Advertisement

Neuroradiology

, Volume 61, Issue 11, pp 1239–1249 | Cite as

Characteristic asymmetric limbic and anterior temporal atrophy in demented patients with pathologically confirmed argyrophilic grain disease

  • Keita SakuraiEmail author
  • Aya.M Tokumaru
  • Toshimasa Ikeda
  • Satoru Morimoto
  • Shohei Inui
  • Kaoru Sumida
  • Hiroshi Oba
  • Motoo Nakagawa
  • Noriyuki Matsukawa
  • Yoshio Hashizume
Diagnostic Neuroradiology

Abstract

Purpose

The purpose of this study is to clarify the characteristic structural magnetic resonance imaging (MRI) findings in demented patients with pathologically confirmed argyrophilic grain disease (AGD).

Methods

Nine pathologically confirmed AGD patients with cerebral three-dimensional T1-weighted MRI were evaluated in this study. In addition to visual rating scales of atrophic and asymmetric changes in the limbic and temporal lobes, voxel-based morphometry (VBM) was performed to assess group difference between pathologically confirmed AGD and Alzheimer’s disease (AD) patients.

Results

On visual analyses of AGD patients, the medial temporal, anterior temporal, and posterior temporal atrophy scores were 3.3 ± 0.7, 1.7 ± 0.5, and 1.0 ± 0.7, respectively. Asymmetric scores of the hippocampus and parahippocampal gyrus, amygdala and ambient gyrus, anterior temporal, and posterior temporal lobes were rated as 1.1 ± 0.7, 1.6 ± 0.5, 1.3 ± 0.8, and 0.4 ± 0.7, respectively. In spite of no statistical differences in atrophic scores, AGD patients showed the higher score and proportion of anterior temporal asymmetric score than AD (p = 0.03 and 0.02). Compared with controls, VBM analysis revealed left dominant asymmetric atrophy predominantly in the limbic and anterior temporal lobe in AGD patients. By contrast, there was no significant gray matter reduction between AGD and AD patients.

Conclusions

Asymmetric atrophy relatively localized to the anterior temporal and limbic lobes including the amygdala and ambient gyrus is a characteristic MRI finding of AGD. For the precise antemortem diagnosis, especially to differentiation from AD, it is important to pay attention to this asymmetric change.

Keywords

Argyrophilic grain disease Asymmetric atrophy Magnetic resonance imaging Visual rating scale Voxel-based morphometry 

Notes

Author contributions

1.Guarantor of integrity of the entire study: Keita Sakurai, Aya.M Tokumaru

2. Study concepts: Keita Sakurai

3. Study design: Keita Sakurai, Toshimasa Ikeda

4. Definition of intellectual content: Not applicable

5. Literature research: Keita Sakurai, Satoru Morimoto, Motoo Nakagawa

6. Clinical studies: Toshimasa Ikeda, Satoru Morimoto, Noriyuki Matsukawa, Yoshio Hashizume

7. Experimental studies: Not applicable

8. Data acquisition: Shohei Inui, Kaoru Sumida, Yoshio Hashizume

9. Data analysis: Keita Sakurai, Aya.M Tokumaru, Motoo Nakagawa

10. Statistical analysis: Keita Sakurai

11. Manuscript preparation: Keita Sakurai

12. Manuscript editing: Hiroshi Oba

13. Manuscript review: Hiroshi Oba, Aya.M Tokumaru

Funding

This study was supported by Grants-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (Kakenhi Wakate B, 16K19839: KS).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

We declare that all human and animal studies have been approved by the Ethics Committee for Clinical Research of the Fukushimura Hospital and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed consent

Informed consent by the bereaved of all patients was obtained from all the individual participants included in the study.

References

  1. 1.
    Braak H, Braak E (1987) Argyrophilic grains: characteristic pathology of cerebral cortex in cases of adult onset dementia without Alzheimer changes. Neurosci Lett 76(1):124–127CrossRefGoogle Scholar
  2. 2.
    Irwin DJ, Cohen TJ, Grossman M, Arnold SE, McCarty-Wood E, Van Deerlin VM, Lee VM, Trojanowski JQ (2013) Acetylated tau neuropathology in sporadic and hereditary tauopathies. Am J Pathol 183(2):344–351CrossRefGoogle Scholar
  3. 3.
    Saito Y, Nakahara K, Yamanouchi H, Murayama S (2002) Severe involvement of ambient gyrus in dementia with grains. J Neuropathol Exp Neurol 61(9):789–796CrossRefGoogle Scholar
  4. 4.
    Ilieva EV, Kichev A, Naudí A, Ferrer I, Pamplona R, Portero-Otín M (2011) Mitochondrial dysfunction and oxidative and endoplasmic reticulum stress in argyrophilic grain disease. J Neuropathol Exp Neurol 70(4):253–263CrossRefGoogle Scholar
  5. 5.
    Martinez-Lage P, Munoz DG (1997) Prevalence and disease associations of argyrophilic grains of Braak. J Neuropathol Exp Neurol 56(2):157–164CrossRefGoogle Scholar
  6. 6.
    Rodriguez RD, Grinberg LT (2015) Argyrophilic grain disease: an underestimated tauopathy. Dement Neuropsychol 9(1):2–8CrossRefGoogle Scholar
  7. 7.
    Ding ZT, Wang Y, Jiang YP, Yoshida M, Mimuro M, Inagaki T, Iwase T, Hashizume Y (2006) Argyrophilic grain disease: frequency and neuropathology in centenarians. Acta Neuropathol 111(4):320–328CrossRefGoogle Scholar
  8. 8.
    Josephs KA, Whitwell JL, Parisi JE, Knopman DS, Boeve BF, Geda YE, Jack CR Jr, Petersen RC, Dickson DW (2008) Argyrophilic grains: a distinct disease or an additive pathology? Neurobiol Aging 29(4): 566–573CrossRefGoogle Scholar
  9. 9.
    Jicha GA, Petersen RC, Knopman DS, Boeve BF, Smith GE, Geda YE, Johnson KA, Cha R, Delucia MW, Braak H, Dickson DW, Parisi JE (2006) Argyrophilic grain disease in demented subjects presenting initially with amnestic mild cognitive impairment. J Neuropathol Exp Neurol 65(6):602–609CrossRefGoogle Scholar
  10. 10.
    Saito Y, Murayama S (2007) Neuropathology of mild cognitive impairment. Neuropathology 27(6):578–584CrossRefGoogle Scholar
  11. 11.
    Rodriguez RD, Suemoto CK, Molina M, Nascimento CF, Leite RE, de Lucena Ferretti-Rebustini RE, Farfel JM, Heinsen H, Nitrini R, Ueda K, Pasqualucci CA, Jacob-Filho W, Yaffe K, Grinberg LT (2016) Argyrophilic grain disease: demographics, clinical, and neuropathological features from a large autopsy study. J Neuropathol Exp Neurol 75(7): 628–635CrossRefGoogle Scholar
  12. 12.
    Barkhof F, Polvikoski TM, van Straaten EC, Kalaria RN, Sulkava R, Aronen HJ, Niinistö L, Rastas S, Oinas M, Scheltens P, Erkinjuntti T (2007) The significance of medial temporal lobe atrophy: a postmortem MRI study in the very old. Neurology 69(15):1521–1527CrossRefGoogle Scholar
  13. 13.
    Adachi T, Saito Y, Hatsuta H, Funabe S, Tokumaru AM, Ishii K, Arai T, Sawabe M, Kanemaru K, Miyashita A, Kuwano R, Nakashima K, Murayama S (2010) Neuropathological asymmetry in argyrophilic grain disease. J Neuropathol Exp Neurol 69(7):737–744CrossRefGoogle Scholar
  14. 14.
    Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y, Yamanouchi H, Murayama S (2004) Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 63(9):911–918CrossRefGoogle Scholar
  15. 15.
    Hyman BT, Trojanowski JQ (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J Neuropathol Exp Neurol 56(10):1095–1097CrossRefGoogle Scholar
  16. 16.
    McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor JP, Weintraub D, Aarsland D, Galvin J, Attems J, Ballard CG, Bayston A, Beach TG, Blanc F, Bohnen N, Bonanni L, Bras J, Brundin P, Burn D, Chen-Plotkin A, Duda JE, El-Agnaf O, Feldman H, Ferman TJ, Ffytche D, Fujishiro H, Galasko D, Goldman JG, Gomperts SN, Graff-Radford NR, Honig LS, Iranzo A, Kantarci K, Kaufer D, Kukull W, Lee VMY, Leverenz JB, Lewis S, Lippa C, Lunde A, Masellis M, Masliah E, McLean P, Mollenhauer B, Montine TJ, Moreno E, Mori E, Murray M, O'Brien JT, Orimo S, Postuma RB, Ramaswamy S, Ross OA, Salmon DP, Singleton A, Taylor A, Thomas A, Tiraboschi P, Toledo JB, Trojanowski JQ, Tsuang D, Walker Z, Yamada M, Kosaka K (2017) Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology 89(1):88–100CrossRefGoogle Scholar
  17. 17.
    Litvan I, Hauw JJ, Bartko JJ, Lantos PL, Daniel SE, Horoupian DS, McKee A, Dickson D, Bancher C, Tabaton M, Jellinger K, Anderson DW (1996) Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and related disorders. J Neuropathol Exp Neurol 55(1):97–105CrossRefGoogle Scholar
  18. 18.
    Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82(4):239–259CrossRefGoogle Scholar
  19. 19.
    Uchino A, Takao M, Hatsuta H, Sumikura H, Nakano Y, Nogami A, Saito Y, Arai T, Nishiyama K, Murayama S (2015) Incidence and extent of TDP-43 accumulation in aging human brain. Acta Neuropathol Commun 3:35CrossRefGoogle Scholar
  20. 20.
    Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The consortium to establish a registry for Alzheimer’s disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41(4):479–486CrossRefGoogle Scholar
  21. 21.
    Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P, Kuiper M, Steinling M, Wolters EC, Valk J (1992) Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 55(10):967–972CrossRefGoogle Scholar
  22. 22.
    Kipps CM, Davies RR, Mitchell J, Kril JJ, Halliday GM, Hodges JR (2007) Clinical significance of lobar atrophy in frontotemporal dementia: application of an MRI visual rating scale. Dement Geriatr Cogn Disord 23(5):334–342CrossRefGoogle Scholar
  23. 23.
    Harper L, Barkhof F, Fox NC, Schott JM (2015) Using visual rating to diagnose dementia: a critical evaluation of MRI atrophy scales. J Neurol Neurosurg Psychiatry 86(11):1225–1233CrossRefGoogle Scholar
  24. 24.
    Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38(1):95–113CrossRefGoogle Scholar
  25. 25.
    Whitwell JL, Jack CR Jr, Boeve BF, Parisi JE, Ahlskog JE, Drubach DA, Senjem ML, Knopman DS, Petersen RC, Dickson DW, Josephs KA (2010) Imaging correlates of pathology in corticobasal syndrome. Neurology 75(21): 1879–1887CrossRefGoogle Scholar
  26. 26.
    Harper L, Fumagalli GG, Barkhof F, Scheltens P, O'Brien JT, Bouwman F, Burton EJ, Rohrer JD, Fox NC, Ridgway GR, Schott JM (2016) MRI visual rating scales in the diagnosis of dementia: evaluation in 184 post-mortem confirmed cases. Brain 139(Pt 4): 1211–1225CrossRefGoogle Scholar
  27. 27.
    Wisse LEM, Butala N, Das SR, Davatzikos C, Dickerson BC, Vaishnavi SN, Yushkevich PA, Wolk DA; Alzheimer’s Disease Neuroimaging Initiative (2015) Suspected non-AD pathology in mild cognitive impairment. Neurobiol Aging 36(12): 3152–3162Google Scholar
  28. 28.
    Toledo JB, Cairns NJ, Da X, Chen K, Carter D, Fleisher A, Householder E, Ayutyanont N, Roontiva A, Bauer RJ, Eisen P, Shaw LM, Davatzikos C, Weiner MW, Reiman EM, Morris JC, Trojanowski JQ, Alzheimer’s Disease Neuroimaging Initiative (ADNI) (2013) Clinical and multimodal biomarker correlates of ADNI neuropathological findings. Acta Neuropathol Commun 1:65CrossRefGoogle Scholar
  29. 29.
    Tolnay M, Clavaguera F (2004) Argyrophilic grain disease: a late-onset dementia with distinctive features among tauopathies. Neuropathology 24(4):269–283CrossRefGoogle Scholar
  30. 30.
    Mesulam MM, Weintraub S, Rogalski EJ, Wieneke C, Geula C, Bigio EH (2014) Asymmetry and heterogeneity of Alzheimer’s and frontotemporal pathology in primary progressive aphasia. Brain 137(Pt 4): 1176–1192CrossRefGoogle Scholar
  31. 31.
    Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11(6 Pt 1):805–821CrossRefGoogle Scholar
  32. 32.
    Ikeda K, Akiyama H, Arai T, Matsushita M, Tsuchiya K, Miyazaki H (2000) Clinical aspects of argyrophilic grain disease. Clin Neuropathol 19(6):278–284PubMedGoogle Scholar
  33. 33.
    Josephs KA, Whitwell JL, Ahmed Z, Shiung MM, Weigand SD, Knopman DS, Boeve BF, Parisi JE, Petersen RC, Dickson DW, Jack CR Jr (2008) Beta-amyloid burden is not associated with rates of brain atrophy. Ann Neurol 63(2):204–212CrossRefGoogle Scholar
  34. 34.
    O'Brien JT, Holmes C, Jones M, Jones R, Livingston G, McKeith I, Mittler P, Passmore P, Ritchie C, Robinson L, Sampson EL, Taylor JP, Thomas A, Burns A (2017) Clinical practice with anti-dementia drugs: a revised (third) consensus statement from the British Association for Psychopharmacology. J Psychopharmacol 31(2):147–168CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Keita Sakurai
    • 1
    Email author
  • Aya.M Tokumaru
    • 2
  • Toshimasa Ikeda
    • 3
  • Satoru Morimoto
    • 4
  • Shohei Inui
    • 1
    • 5
  • Kaoru Sumida
    • 1
  • Hiroshi Oba
    • 1
  • Motoo Nakagawa
    • 6
  • Noriyuki Matsukawa
    • 3
  • Yoshio Hashizume
    • 7
  1. 1.Department of RadiologyTeikyo University School of MedicineTokyoJapan
  2. 2.Department of Diagnostic RadiologyTokyo Metropolitan Medical center of GerontologyTokyoJapan
  3. 3.Department of Neurology and NeuroscienceNagoya City University Graduate School of Medical SciencesNagoyaJapan
  4. 4.Department of Physiology, School of MedicineKeio UniversityTokyoJapan
  5. 5.Department of Radiology, Graduate School of MedicineThe University of TokyoTokyoJapan
  6. 6.Department of RadiologyNagoya City University Graduate School of Medical SciencesNagoyaJapan
  7. 7.Fukushimura HospitalChoju Medical InstituteTokyoJapan

Personalised recommendations