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Hippocampal Volumes in Amnestic and Non-Amnestic Mild Cognitive Impairment Types Using Two Common Methods of MCI Classification

Published online by Cambridge University Press:  16 June 2021

Natalie A. Emmert Open the ORCID record for Natalie A. Emmert [Opens in a new window] ,
Katherine E. Reiter ,
Alissa Butts ,
Julie K Janecek ,
Mohit Agarwal ,
Malgorzata Franczak ,
James Reuss ,
Andrew Klein ,
Yang Wang  and
Laura Glass Umfleet Open the ORCID record for Laura Glass Umfleet [Opens in a new window]
Natalie A. Emmert
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Katherine E. Reiter
Affiliation:
Lou Ruvo Center for Brain Health, Neurological Institute, Cleveland Clinic, Cleveland, OH
Alissa Butts
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Julie K Janecek
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Mohit Agarwal
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Malgorzata Franczak
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
James Reuss
Affiliation:
Prism Clinical Imaging, Inc., Elm Grove, WI
Andrew Klein
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Yang Wang
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
Laura Glass Umfleet*
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, WI
*
*Correspondence and reprint requests to: Laura Glass Umfleet. PsyD, ABPP-CN, Division of Neuropsychology, Department of Neurology, Medical College of Wisconsin, 8701 Watertown Plank Rd., Milwaukee, WI 53226, USA. E-mail: lumfleet@mcw.edu
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Abstract

Objectives:

Mild cognitive impairment (MCI) types may have distinct neuropathological substrates with hippocampal atrophy particularly common in amnestic MCI (aMCI). However, depending on the MCI classification criteria applied to the sample (e.g., number of abnormal test scores considered or thresholds for impairment), volumetric findings between MCI types may change. Additionally, despite increased clinical use, no prior research has examined volumetric differences in MCI types using the automated volumetric software, Neuroreader™.

Methods:

The present study separately applied the Petersen/Winblad and Jak/Bondi MCI criteria to a clinical sample of older adults (N = 82) who underwent neuropsychological testing and brain MRI. Volumetric data were analyzed using Neuroreader™ and hippocampal volumes were compared between aMCI and non-amnestic MCI (naMCI).

Results:

T-tests revealed that regardless of MCI classification criteria, hippocampal volume z-scores were significantly lower in aMCI compared to naMCI (p’s < .05), and hippocampal volume z-scores significantly differed from 0 (Neuroreader™ normative mean) in the aMCI group only (p’s < .05). Additionally, significant, positive correlations were found between measures of delayed recall and hippocampal z-scores in aMCI using either MCI classification criteria (p’s < .05).

Conclusions:

We provide evidence of correlated neuroanatomical changes associated with memory performance for two commonly used neuropsychological MCI classification criteria. Future research should investigate the clinical utility of hippocampal volumes analyzed via Neuroreader™ in MCI.

Keywords

Mild cognitive impairmentDiagnosisHippocampal volumeMemoryNeuroimagingNeuroReader™

Information

Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 4 , April 2022 , pp. 391 - 400
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

ADNI Procedures Manual (n.d). Retrieved from http://adni.loni.usc.edu/.Google Scholar
Ahdidan, J., Raji, C.A., DeYoe, E.A., Mathis, J, Noe, K., Rimestad, J…. Lopez, O. (2016). Quantitative neuroimaging software for clinical assessment of hippocampal volumes on MRI. Journal of Alzheimer’s Disease, 49, 723–732.CrossRefGoogle Scholar
Apostolova, L.G., Dutton, R.A., Dinov, I.D., Hayashi, K.M., Toga, A.W., Cummings, J.L., & Thompson, P.M. (2006). Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. Archives of Neurology, 63, 693–699.CrossRefGoogle ScholarPubMed
Apostolova, L.G., Green, A.E., Babakchanian, S., Hwang, K.S., Chou, Y., Toga, A.W., & Thompson, P.M. (2012). Hippocampal atrophy and ventricular enlargement in normal aging, mild cognitive impairment (MCI), and Alzheimer disease. Alzheimer Disease & Associated Disorders, 26, 17–27.CrossRefGoogle Scholar
American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th ed.. Washington, DC: Author.Google Scholar
Arlt, S., Buchert, R., Spies, L, Eichenlaub, M., Lehmbeck, J.T., & Jahn, H. (2013). Association between fully automated MRI-based volumetry of different brain regions and neuropsychological test performance in patients with amnestic mild cognitive impairment and Alzheimer’s disease. European Archives of Psychiatry & Clinical Neuroscience, 263, 335–344.CrossRefGoogle ScholarPubMed
Benedict, R.H. (1997). Brief Visuospatial Memory Test—Revised: Professional Manual. Odessa, Florida: PAR.Google Scholar
Bickel, H, Mösch, E, Seigerschmidt, E, Siemen, M, & Förstl, H. (2006). Prevalence and persistence of Mild Cognitive Impairment among elderly patients in general hospitals. Dement & Geriatric Cognitive Disorders, 21(4), 242–250.CrossRefGoogle ScholarPubMed
Bonner-Jackson, A., Mahmoud, S., Miller, J., & Banks, S.J. (2015). Verbal and non-verbal memory and hippocampal volumes in a memory clinic population. Alzheimer’s Research & Therapy, 7, 61.CrossRefGoogle Scholar
Boutet, C., Chupin, M., Colliot, O., Sarazin, M., Mutlu, G., Drier, A. … the Alzheimer’s Disease Neuroimaging Initiative. (2012). Is radiological evaluation as good as computer-based volumetry to assess hippocampal atrophy in Alzheimer’s disease? Neuroradiology, 54, 1321–1330. doi: 10.1007/s00234-012-1058-0.CrossRefGoogle ScholarPubMed
Brandt, J. & Benedict, R.H. (2001). Hopkins Verbal Learning Test—Revised: Professional Manual. Odessa, Florida: Psychological Assessment Resources.Google Scholar
Broadhouse, K.M., Mowszowski, L., Duffy, S., Leung, I., Cross, N., Valenzuela, M.J., & Naismith, S.L. (2019). Memory performance correlates of hippocampal subfield volume in mild cognitive impairment subtype. Frontiers in Behavioral Neuroscience, 13, 259.CrossRefGoogle ScholarPubMed
Brooks, B.L., Iverson, G.L., Holdnack, J.A., & Feldman, H.H. (2008). Potential for misclassification of mild cognitive impairment: a study of memory scores on the Wechsler Memory Scale-III in healthy older adults. Journal of the International Neuropsychological Society, 14(3), 463–478. doi: 10.1017/S1355617708080521.CrossRefGoogle ScholarPubMed
Busse, A., Hensel, A., Guhne, U., Angermeyer, M.C., & Riedel-Heller, S.G. (2006). Mild cognitive impairment: long term course of four clinical subtypes. Neurology, 67(12): 2176–2185.CrossRefGoogle ScholarPubMed
Clark, L.R., Delano-Wood, L., Libon, D.J., McDonald, C.R., Nation, D.A., Bangen, K.J. … Bondi, M.W. (2013). Are empirically-derived subtypes of Mild Cognitive Impairment consistent with conventional subtypes? Journal of the International Neuropsychological Society, 19(6), 635–645. doi: 10.1017/S1355617713000313.CrossRefGoogle ScholarPubMed
Csukly, G., Sirály, E., Fodor, Z., Horváth, A., Salacz, P., Hidasi, Z. … Szabó, Á. (2016). The differentiation of amnestic type MCI from the non-amnestic types by structural MRI. Frontiers in Aging Neuroscience, 8(52), 1–10. doi: 10.3389/fnagi.2016.00052.CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). California Verbal Learning Test–Second Edition (CVLT-II). San Antonio, TX: The Psychological Corporation.Google Scholar
Eckerström, C., Olsson, E., Borga, M., Ekholm, S., Ribbelin, S, Rolstad, S. … Malmgren, H.(2008). Small baseline volume of left hippocampus is associated with subsequent conversion of MCI into dementia: the Göteborg MCI study. Journal of the Neurological Sciences, 272, 48–59. doi: 10.1016/j.jns.2008.04.024.CrossRefGoogle ScholarPubMed
Edmonds, E.C., Delano-Wood, L., Clark, L.R., Jak, A.J., Nation, D.A., McDonald, C.R. … for the Alzheimer’s Disease Neuroimaging Initiative. (2015). Susceptibility of the conventional criteria for MCI to false positive diagnostic errors. Alzheimer’s & Dementia, 11(4), 415–424. doi: 10.1016/j.jalz.2014.03.005.CrossRefGoogle ScholarPubMed
Eskildsen, S.F., Coupé, P., Fonov, V.S., Pruessner, J.C., Collins, D.L., & Alzheimer’s Disease Neuroimaging Initiative. (2015). Structural imaging biomarkers of Alzheimer’s disease: predicting disease progression. Neurobiology of Aging, 36, S23–S31.CrossRefGoogle ScholarPubMed
Ferman, T.J., Smith, G.E., Kantarci, K., Boeve, B.F., Pankratz, V.S., Dickson, D.W. … Petersen, R.C. (2013). Nonamnestic mild cognitive impairment progresses to dementia with lewy bodies. Neurology, 81, 2032–2038.CrossRefGoogle ScholarPubMed
Fritzsche, K.H., Stieltjes, B., Schlindwein, S., van Bruggen, T., Essig, M., & Meinzer, H. (2010). Automated MR morphometry to predict Alzheimer’s disease in mild cognitive impairment. International Journal of Computer Assisted Radiology and Surgery, 5, 623–632.CrossRefGoogle Scholar
Ganguli, M., Dodge, H.H., Shen, C., & DeKosky, S.T. (2004). Mild cognitive impairment, amnestic type: an epidemiologic study. Neurology, 63, 115–121.CrossRefGoogle Scholar
Ganguli, M., Snitz, B.E., Saxton, J.A., Chang, C-C.H., Lee, C-W., Vander Bilt, J. … Petersen, R.C. (2011). Outcomes of mild cognitive impairment depend on definition: a population study. Archives of Neurology, 68 (6), 761–767. doi: 10.1001/archneurol.2011.101.CrossRefGoogle Scholar
Geffen, G., Hoar, K.J., O’Hanlon, A.P., Clark, C.R., & Geffen, L.B. (1990). Performance measures of 16–86- year-old males and females on the Auditory Verbal Learning Test. Clinical Neuropsychologist, 4, 45–63.CrossRefGoogle Scholar
Jack, C.R., Petersen, R.C., O’Brien, P.C., & Tangalos, E.G. (1992). MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology, 42, 183–188.CrossRefGoogle ScholarPubMed
Jack, C.R., Therneau, R.M., Wiste, H.J., Weigand, S.D., Knopman, D.S., Lowe, V.J. … Petersen, R.C. (2016). Transition rates between amyloid and neurodegeneration biomarker states and to dementia: a population-based, longitudinal cohort study. Lancet Neurology, 15, 56–64.CrossRefGoogle ScholarPubMed
Jak, A.J., Bondi, M.W., Delano-Wood, L., Wierenga, C.E., Corey-Bloom, J., Salmon, D.P., & Delis, D. (2009a). Quantification of five neuropsychological approaches to defining mild cognitive impairment. American Journal of Geriatric Psychiatry, 17, 368–375.CrossRefGoogle ScholarPubMed
Jak, A.J., Preis, S.R., Beiser, A.S., Seshadri, S., Wolf, P.A., Bondi, M.W., & Au, R. (2016). Neuropsychological criteria for Mild Cognitive Impairment and dementia risk in the Framingham Heart Study. Journal of the International Neuropsychological Society, 22, 1–7. doi: 10.1017/S1355617716000199.CrossRefGoogle ScholarPubMed
Jak, A.J., Urban, S., McCauley, A., Bangen, K. J., Delano-Wood, L., Corey-Bloom, J., & Bondi, M.W. (2009b). Profile of hippocampal volumes and stroke risk varies by neuropsychological definition of mild cognitive impairment. Journal of the International Neuropsychological Society, 15(6), 890–897.CrossRefGoogle ScholarPubMed
Kantarci, K., Petersen, R.C., Przybelski, S.A., Weigand, S.D., Shiung, M.M., Whitwell, J. L. … Jack, C. R. Jr (2008). Hippocampal volumes, proton magnetic resonance spectroscopy metabolites, and cerebrovascular disease in mild cognitive impairment subtypes. Archives of Neurology, 65(12), 1621–1628.CrossRefGoogle ScholarPubMed
Landis, J.R. & Koch, G.G. (1977). The measurement of observer agreement for categorical data. Biometrics, 33, 159–174.CrossRefGoogle ScholarPubMed
Liu, Y., Paajanen, T., Zhang, Y., Westman, E., Wahlund, L., Simmons, A., … & the AddNeuroMed Consortium. (2010). Analysis of regional MRI volumes and thicknesses as predictors of conversion from mild cognitive impairment to Alzheimer’s disease. Neurobiology of Aging, 31(8), 1375–1385.CrossRefGoogle ScholarPubMed
Neuroreader™ Medical Imaging Processing Software User manual [V8.03. March 2, 2020]. (2020).Google Scholar
Nordlund, A., Rolstad, S., Hellström, P., Sjögren, M., Hansen, S., & Wallin, A. (2005). The Goteborg MCI study: Mild cognitive impairment is a heterogenous condition. Journal of Neurology, Neurosurgery, & Psychiatry, 76, 1485–1490. doi: 10.1136/jnnp.2004.050385.CrossRefGoogle Scholar
Palmer, B.W., Boone, K.B., Lesser, I.M. & Wohl, M.A. (1998). Base rates of “impaired” neuropsychological test performance among healthy older adults. Archives of Clinical Neuropsychology, 13(6), 503–511.Google ScholarPubMed
Peng, G., Feng, Z., He, F., Chen, Z., Liu, X, Liu, P., & Luo, B. (2015). Correlation of hippocampal volume and cognitive performances in patients with either Mild Cognitive Impairment or Alzheimer’s disease. CNS Neurosciences & Therapeutics, 21, 15–22.CrossRefGoogle ScholarPubMed
Petersen, R.C. (2000). Mild cognitive impairment: transition between aging and Alzheimer’s disease. Neurologia, 15, 93–101.Google ScholarPubMed
Petersen, R.C. Mild cognitive impairment as a diagnostic entity. (2004). Journal of Internal Medicine, 256, 183–194.CrossRefGoogle ScholarPubMed
Petersen, R.C., Doody, R., Kurz, A., Mohs, R.C., Morris, J.C., Rabins, P.V., Ritchie, K., Rossor, M., Thal, L., & Winblad, B. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992.CrossRefGoogle ScholarPubMed
Petersen, R.C. & Morris, J.C. (2003). Clinical features. In Petersen’s, RC (Ed.) Mild cognitive impairment: aging to Alzheimer’s disease (pp. 15–40). New York: Oxford University Press, Inc.Google Scholar
Petersen, R.C. & Negash, S. (2008). Mild cognitive impairment: an overview. CNS Spectrums, 13, 45–53.CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Kokmen, E., & Tangelos, E.G. (1997). Aging, memory, and mild cognitive impairment. International Psychogeriatrics, 9(51), 65–69.CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56, 303–308.CrossRefGoogle ScholarPubMed
Raji, C.A., Eyre, H., Wei, S.H., Bredesen, D.E., Moylan, S., Law, M. … Vernooij, M.W. (2015). Hot topics in research: preventive neuroradiology in brain aging and cognitive decline. American Journal of Neuroradiology, 36(10), 1803–1809. doi: 10.3174/ajnr.A4409.CrossRefGoogle ScholarPubMed
Risacher, S.L., Saykin, A.J., West, J.D., Shen, L., Firpi, H.A., McDonald, B.C., & Alzheimer’s Disease Neuroimaging Initiative (ADNI). (2009). Baseline MRI predictors of conversion from MCI to probable AD in the ADNI cohort. Current Alzheimer Research, 6(4), 347–361.CrossRefGoogle ScholarPubMed
Ross, D.E., Ochs, A.L., Seabaugh, J.M., Shrader, C.R. & the Alzheimer’s Disease Neuroimaging Initiative. (2013). Man versus machine: comparison of radiologists’ interpretations and NeuroQuant® volumetric analyses of brain MRIs in patients with traumatic brain injury. The Journal of Neuropsychiatry & Clinical Neurosciences, 25, 32–39.CrossRefGoogle ScholarPubMed
Rountree, S.D., Waring, S.C., Chan, W.C., Lupo, P.J., Darby, E.J., & Doody, R.S. (2007). Importance of subtle amnestic and nonamnestic deficits in Mild Cognitive Impairment: prognosis and conversion to dementia. Dementia & Geriatric Cognitive Disorders, 24(6), 476–482.CrossRefGoogle ScholarPubMed
Salmon, D.P. (2000). Disorders of memory in Alzheimer’s disease. In Cermak’s, LS (Ed.) Handbook of Neuropsychology: Memory and Its Disorders (2nd ed., Vol. 2, pp. 155–195). Amsterdam: Elsevier.Google Scholar
Salmon, D.P. & Bondi, M.W. (2009). Neuropsychological assessment of dementia. Annual Review of Psychology, 60, 257–282. doi: 10.1146/annurev.psych.57.102904.190024.CrossRefGoogle ScholarPubMed
Schinka, J.A., Loewenstein, D.A., Raj, A., Schoenberg, M.R., Banko, J.L., Potter, H., & Duara, R. (2010). Defining mild cognitive impairment: impact of varying decision criteria on neuropsychological diagnostic frequencies and correlates. The American Journal of Geriatric Psychiatry, 18(8), 684–691. doi: 10.1097/JGP.0b013e3181e56d5a.CrossRefGoogle ScholarPubMed
Suppa, P., Hampel, H., Keppb, T., Langea, C., Spies, L., Fiebach, J. B. … Ralph Bucherta for the Alzheimer’s Disease Neuroimaging Initiative. (2016). Performance of hippocampus volumetry with FSL-FIRST for prediction of Alzheimer’s Disease dementia in at risk subjects with Amnestic Mild Cognitive Impairment. Journal of Alzheimer’s Disease, 51, 867–873. doi: 10.3233/JAD-150804.CrossRefGoogle ScholarPubMed
Tanpitukpongse, T.P., Mazurowski, M.A., Ikhena, J., & Petrella, J.R. (2017). Predictive utility of marketed volumetric software tools in subjects at risk for Alzheimer’s disease: do regions outside the hippocampus matter? American Journal of Neuroradiology, 38(3), 546–552. doi: https://doi.org/10.3174/ajnr.A5061.CrossRefGoogle ScholarPubMed
Trittschuh, E.H., Crane, P.K., Larson, E., Cholerton, B., McCormick, W.C., McCurry, S.M. … Craft, S. (2011). Effects of varying diagnostic criteria on prevalence of Mild Cognitive Impairment in a community based sample. Journal of Alzheimer’s Disease, 25(1), 163–173. doi: 10.3233/JAD-2011-101821.CrossRefGoogle Scholar
Vos, S.J.B., van Rossum, I.A., Verhey, F., Knol, D.L., Soininen, H., Wahlund, L. … Visser, P.J. (2013). Prediction of Alzheimer disease in subjects with amnestic and nonamnestic MCI. Neurology, 80, 1124–1132.CrossRefGoogle ScholarPubMed
Wechsler, D. (2009). WMS-IV: Wechsler Memory Scale. San Antonio, Texas: Pearson.Google Scholar
Whitwell, J.L., Shiung, M. M., Przybelski, S.A., Weigand, S.D., Knopman, D.S., Boeve, B.F., Petersen, R.C., & Jack, C.R. (2008). MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology, 70, 512–520. doi: 10.1212/01.wnl.0000280575.77437.a2.CrossRefGoogle ScholarPubMed
Wilkinson, G.S. & Robertson, G.J. (2006). Wide Range Achievement Test (WRAT4). Lutz, FL: Psychological Assessment Resources.Google Scholar
Yi, H.A., Moller, C., Dieleman, N., Bouwman, F., Barkhof, F., Scheltens, P. … Vrenken, H. (2016). Relation between subcortical grey matter atrophy and conversion from mild cognitive impairment to Alzheimer’s disease. Journal of Neurology, Neurosurgery, & Psychiatry, 87, 425–432.CrossRefGoogle ScholarPubMed
Zhang, H., Sachdev, P.S., Wen, W., Kochan, N.A, Crawford, J.D., Brodaty, H. … Trollor, J. N. (2012). Gray matter atrophy patterns of mild cognitive impairment subtypes. Journal of the Neurological Sciences, 315, 26–32. doi: 10.1016/j.jns.2011.12.0.CrossRefGoogle ScholarPubMed