Journal of Integrative Natural Science (통합자연과학논문집)

The Basic Science Institute Chosun University (조선대학교 기초과학연구원)
권호 표지
DOI QR코드

DOI QR Code

Asymmetrical Volume Loss in Hippocampal Subfield During the Early Stages of Alzheimer Disease: A Cross Sectional Study

  • Received : 2018.08.30
  • Accepted : 2018.09.07
  • Published : 2018.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Hippocampal atrophy is a well-established imaging biomarker of Alzheimer disease (AD). However, hippocampus is a non-homogenous structure with cytoarchitecturally and functionally distinct sub-regions or subfield, with each region performing distinct functions. Certain regions of the subfield have shown selective vulnerability to AD. Here, we are interested in studying the effects of normal aging and mild cognitive impairment on these sub-regional volumes. With a reliable automated segmentation technique, we segmented these subregions of the hippocampus in 101 cognitively normal (CN), 135 early mild cognitive impairment (EMCI), 67 late mild cognitive impairment (LMCI) and 48 AD subjects. Thereby, dividing the hippocampus into hippocampal tail (tail), subiculum (SUB), cornu ammonis 1 (CA1), hippocampal fissure (fissure), presubiculum (PSUB), parasubiculum (ParaSUB), molecular layer (ML), granule cells/molecular layer/dentate gyrus (GCMLDG), cornu ammonis 3(CA3), cornu ammonis 4(CA4), fimbria and hippocampal-amygdala transition area (HATA). In this cross sectional study of 351 ADNI subjects, no differences in terms of age, gender, and years of education were observed among the groups. Though, the groups had statistically significant differences (p < 0.05 after the multiple comparison correction) in the Mini-Mental State Examination (MMSE) scores. There was asymmetrical volume loss in the early stages of AD with the left hemisphere showing volume loss in regions that were unaffected in the right hemisphere. Bilateral parasubiculum, right cornu ammonis 1, 3 and 4, right fimbria and right HATA regions did not show any volume loss till the late MCI stages. Our findings suggest that the hippocampal subfield regions are selectively vulnerable to AD and also that these vulnerabilities are asymmetrical especially during the early stages of AD.

Keywords

References

  1. 2018 Alzheimer's disease facts and figures. Alzheimer's & Dementia. 2018;14(3):367-429. https://doi.org/10.1016/j.jalz.2018.02.001
  2. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34(7):939-44. https://doi.org/10.1212/WNL.34.7.939
  3. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Kawas CH, et al. The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer's & Dementia. 2011;7(3):263-9. https://doi.org/10.1016/j.jalz.2011.03.005
  4. Fletcher E, Villeneuve S, Maillard P, Harvey D, Reed B, Jagust W, et al. ${\beta}$-amyloid, hippocampal atrophy and their relation to longitudinal brain change in cognitively normal individuals. Neurobiology of aging. 2016;40:173-80. https://doi.org/10.1016/j.neurobiolaging.2016.01.133
  5. Jack CR, Wiste HJ, Knopman DS, Vemuri P, Mielke MM, Weigand SD, et al. Rates of ${\beta}$-amyloid accumulation are independent of hippocampal neurodegeneration. Neurology. 2014;82(18):1605. https://doi.org/10.1212/WNL.0000000000000386
  6. Duvernoy HM. The human hippocampus : functional anatomy, vascularization, and serial sections with MRI. Berlin; New York: Springer; 2005.
  7. Iglesias JE, Augustinack JC, Nguyen K, Player CM, Player A, Wright M, et al. A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI. NeuroImage. 2015;115:117-37. https://doi.org/10.1016/j.neuroimage.2015.04.042
  8. Lucassen P, Heine V, Muller M, Beek E, M Wiegant V, de Kloet E, et al. Stress, Depression and Hippocampal Apoptosis 2006. 531-46 p.
  9. West MJ, Coleman PD, Flood DG, Troncoso JC. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer’s disease. The Lancet. 1994;344(8925):769-72. https://doi.org/10.1016/S0140-6736(94)92338-8
  10. Bugiani O, Constantinidis J, Ghetti B, Bouras C, Tagliavini F. Asymmetrical cerebral atrophy in Alzheimer’s disease. Clinical neuropathology. 1991; 10(2):55-60.
  11. Hou G, Yang X, Yuan TF. Hippocampal asymmetry: differences in structures and functions. Neurochemical research. 2013;38(3):453-60. https://doi.org/10.1007/s11064-012-0954-3
  12. Pedraza O, Bowers D, Gilmore R. Asymmetry of the hippocampus and amygdala in MRI volumetric measurements of normal adults. Journal of the International Neuropsychological Society : JINS. 2004;10(5):664-78. https://doi.org/10.1017/S1355617704105080
  13. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Annals of neurology. 2012; 72(4):578-86. https://doi.org/10.1002/ana.23650
  14. Petersen RC. Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine. 2004;256(3):183-94. https://doi.org/10.1111/j.1365-2796.2004.01388.x
  15. Jack CR, Jr., Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, et al. The Alzheimer's Disease Neuroimaging Initiative (ADNI): MRI methods. Journal of magnetic resonance imaging : JMRI. 2008;27(4):685-91. https://doi.org/10.1002/jmri.21049
  16. Leow AD, Klunder AD, Jack CR, Toga AW, Dale AM, Bernstein MA, et al. Longitudinal stability of MRI for mapping brain change using tensor-based morphometry. NeuroImage. 2006;31(2):627-40. https://doi.org/10.1016/j.neuroimage.2005.12.013
  17. Dale AM, Fischl B, Sereno MI. Cortical Surface-Based Analysis: I. Segmentation and Surface Reconstruction. NeuroImage. 1999;9(2):179-94. https://doi.org/10.1006/nimg.1998.0395
  18. Fischl B, Sereno MI, Dale AM. Cortical Surface-Based Analysis: II: Inflation, Flattening, and a Surface-Based Coordinate System. NeuroImage. 1999; 9(2):195-207. https://doi.org/10.1006/nimg.1998.0396
  19. Adachi M, Kawakatsu S, Hosoya T, Otani K, Honma T, Shibata A, et al. Morphology of the inner structure of the hippocampal formation in Alzheimer disease. AJNR American journal of neuroradiology. 2003;24(8):1575-81.
  20. Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Human brain mapping. 2010;31(9):1339-47. https://doi.org/10.1002/hbm.20934
  21. Mueller SG, Weiner MW. Selective effect of age, Apo e4, and Alzheimer’s disease on hippocampal subfields. Hippocampus. 2009;19(6):558-64. https://doi.org/10.1002/hipo.20614
  22. Kerchner GA, Deutsch GK, Zeineh M, Dougherty RF, Saranathan M, Rutt BK. Hippocampal CA1 apical neuropil atrophy and memory performance in Alzheimer's disease. NeuroImage. 2012;63(1):194-202. https://doi.org/10.1016/j.neuroimage.2012.06.048
  23. Thompson PM, Hayashi KM, de Zubicaray G, Janke AL, Rose SE, Semple J, et al. Dynamics of gray matter loss in Alzheimer's disease. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2003;23(3):994-1005. https://doi.org/10.1523/JNEUROSCI.23-03-00994.2003
  24. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica. 1991;82(4):239-59. https://doi.org/10.1007/BF00308809
  25. Braak E, Braak H. Alzheimer’s disease: Transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon’s horn. Acta Neuropathol. 1997;93:323-5. https://doi.org/10.1007/s004010050622
  26. Simic G, Kostovic I, Winblad B, Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. Journal of Comparative Neurology. 1997;379(4):482-94. https://doi.org/10.1002/(SICI)1096-9861(19970324)379:4<482::AID-CNE2>3.0.CO;2-Z
  27. Wang L, Khan A, Csernansky JG, Fischl B, Miller MI, Morris JC, et al. Fully-automated, multi-stage hippocampus mapping in very mild Alzheimer disease. Hippocampus. 2009;19(6):541-8. https://doi.org/10.1002/hipo.20616
  28. Devanand DP, Bansal R, Liu J, Hao X, Pradhaban G, Peterson BS. MRI hippocampal and entorhinal cortex mapping in predicting conversion to Alzheimer’s disease. NeuroImage. 2012;60(3):1622-9. https://doi.org/10.1016/j.neuroimage.2012.01.075
  29. Chow N, Aarsland D, Honarpisheh H, Beyer MK, Somme JH, Elashoff D, et al. Comparing Hippocampal Atrophy in Alzheimer’s Dementia and Dementia with Lewy Bodies. Dementia and Geriatric Cognitive Disorders. 2012;34(1):44-50. https://doi.org/10.1159/000339727
  30. Mak E, Su L, Williams GB, Watson R, Firbank M, Blamire A, et al. Differential Atrophy of Hippocampal Subfields: A Comparative Study of Dementia with Lewy Bodies and Alzheimer Disease. The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry. 2016;24(2):136-43. https://doi.org/10.1016/j.jagp.2015.06.006
  31. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science (New York, NY). 2005;309(5734):619-23. https://doi.org/10.1126/science.1114037
  32. Lee I, Kesner RP. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus. 2004;14(3):301-10. https://doi.org/10.1002/hipo.10177
  33. O'Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. Journal of Anatomy. 2005;207(3):271-82. https://doi.org/10.1111/j.1469-7580.2005.00446.x
  34. Toga AW, Thompson PM. Mapping brain asymmetry. Nature Reviews Neuroscience. 2003;4:37. https://doi.org/10.1038/nrn1009
  35. Massman PJ, Doody RS. Hemispheric asymmetry in Alzheimer's disease is apparent in motor functioning. Journal of clinical and experimental neuropsychology. 1996;18(1):110-21. https://doi.org/10.1080/01688639608408267
  36. Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Jicha GA, Cooper G, et al. Brain structural alterations before mild cognitive impairment. Neurology. 2007;68(16):1268-73. https://doi.org/10.1212/01.wnl.0000259542.54830.34
  37. Smith CD, Andersen AH, Gold BT, Alzheimer’s Disease Neuroimaging I. Structural Brain Alterations before Mild Cognitive Impairment in ADNI: Validation of Volume Loss in a Predefined Antero-Temporal Region. Journal of Alzheimer's disease : JAD. 2012;31(03):S49-S58. https://doi.org/10.3233/JAD-2012-120157
  38. Bernard C, Helmer C, Dilharreguy B, Amieva H, Auriacombe S, Dartigues JF, et al. Time course of brain volume changes in the preclinical phase of Alzheimer’s disease. Alzheimers Dement. 2014; 10(2):143-51.e1. https://doi.org/10.1016/j.jalz.2013.08.279
  39. Zahn R, Juengling F, Bubrowski P, Jost E, Dykierek P, Talazko J, et al. Hemispheric asymmetries of hypometabolism associated with semantic memory impairment in Alzheimer's disease: a study using positron emission tomography with fluorodeoxyglucose-F18. Psychiatry research. 2004;132(2):159-72. https://doi.org/10.1016/j.pscychresns.2004.07.006
  40. Loewenstein DA, Barker WW, Chang JY, Apicella A, Yoshii F, Kothari P, et al. Predominant left hemisphere metabolic dysfunction in dementia. Arch Neurol. 1989;46(2):146-52. https://doi.org/10.1001/archneur.1989.00520380046012