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The association of neuropsychiatric symptoms with regional brain volumes from patients in a tertiary multi-disciplinary memory clinic

Published online by Cambridge University Press:  28 February 2020

Milap A. Nowrangi*
Affiliation:
The Departments of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA The Johns Hopkins Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Christopher Marano
Affiliation:
Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USA
Kenichi Oishi
Affiliation:
The Johns Hopkins Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA The Departments of Radiology, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Susumu Mori
Affiliation:
The Departments of Radiology, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Haris I. Sair
Affiliation:
The Departments of Radiology, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
John Outen
Affiliation:
The Departments of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Jeannie Leoutsakos
Affiliation:
The Departments of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA The Johns Hopkins Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Constantine Lyketsos
Affiliation:
The Departments of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA The Johns Hopkins Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
Paul B. Rosenberg
Affiliation:
The Departments of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA The Johns Hopkins Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine and Johns Hopkins Bayview Medical Center, Baltimore, MD, USA
*
Correspondence should be addressed to: Milap A. Nowrangi, M.D., M.Be., Department of Psychiatry, Johns Hopkins Bayview Medical Center, 5300 Alpha Commons Drive, 4th Floor, Baltimore, MD 21224, USA. Phone: +410-550-2294; Fax: +410-550-1407. Email: mnowran1@jhmi.edu.

Abstract

Background:

To examine the interaction between structural brain volume measures derived from a clinical magnetic resonance imaging (MRI) and occurrence of neuropsychiatric symptoms (NPS) in outpatient memory clinic patients.

Methods:

Clinical and neuroimaging data were collected from the medical records of outpatient memory clinic patients who were seen by neurologists, geriatric neuropsychiatrists, and geriatricians. MRI scan acquisition was carried out on a 3 T Siemens Verio scanner at Johns Hopkins Bayview Medical Center. Image analyses used an automated multi-label atlas fusion method with a geriatric atlas inventory to generate 193 anatomical regions from which volumes were measured. Regions of interest were generated a priori based on previous literature review of NPS in dementia. Regional volumes for agitation, apathy, and delusions were carried forward in a linear regression analysis.

Results:

Seventy-two patients had clinical and usable neuroimaging data that were analyzed and grouped by Mini-Mental State Exam (MMSE). Neuropsychiatric Inventory Questionnaire (NPI-Q) agitation was inversely associated with rostral anterior cingulate cortex (ACC) bilaterally and left subcallosal ACC volumes in the moderate severity group. Delusions were positively associated with left ACC volumes in both severe and mild groups but inversely associated with the right dorsolateral prefrontal cortex (DLPFC) in the moderate subgroup.

Conclusions:

Agitation, apathy, and delusions are associated with volumes of a priori selected brain regions using clinical data and clinically acquired MRI scans. The ACC is an anatomic region common to these symptoms, particularly agitation and delusions, which closely mirror the findings of research-quality studies and suggest its importance as a behavioral hub.

Type
Original Research Article
Copyright
© International Psychogeriatric Association 2020

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References

Balthazar, M.L. et al. (2014). Neuropsychiatric symptoms in Alzheimer’s disease are related to functional connectivity alterations in the salience network. Human Brain Mapping, 35, 12371246.CrossRefGoogle ScholarPubMed
Bernard, J.A., Orr, J.M. and Mittal, V.A. (2017). Cerebello-thalamo-cortical networks predict positive symptom progression in individuals at ultra-high risk for psychosis. Neuroimage Clinical, 14, 622628.10.1016/j.nicl.2017.03.001CrossRefGoogle ScholarPubMed
Canevelli, M. et al. (2013). Behavioral and psychological subsyndromes in Alzheimer’s disease using the Neuropsychiatric Inventory. International Journal of Geriatric Psychiatry, 28, 795803.10.1002/gps.3904CrossRefGoogle ScholarPubMed
Cao, H. et al. (2018). Cerebello-thalamo-cortical hyperconnectivity as a state-independent functional neural signature for psychosis prediction and characterization. Nature Communications, 9, 3836.CrossRefGoogle ScholarPubMed
Ceritoglu, C. et al. (2009). Multi-contrast large deformation diffeomorphic metric mapping for diffusion tensor imaging. Neuroimage, 47, 618627.10.1016/j.neuroimage.2009.04.057CrossRefGoogle ScholarPubMed
Crum, R.M. et al. (1993). Population-based norms for the Mini-Mental State Examination by age and educational level. JAMA, 269, 23862391.10.1001/jama.1993.03500180078038CrossRefGoogle ScholarPubMed
Cummings, J.L. et al. (1994). The neuropsychiatric inventory: comprehensive assessment of psychopathology in dementia. Neurology, 44, 2308–14.10.1212/WNL.44.12.2308CrossRefGoogle ScholarPubMed
Cummings, J.L. (1997). The Neuropsychiatric Inventory: assessing psychopathology in dementia patients. Neurology, 48, S10S10.10.1212/WNL.48.5_Suppl_6.10SCrossRefGoogle ScholarPubMed
Dandash, O. et al. (2014). Altered striatal functional connectivity in subjects with an at-risk mental state for psychosis. Schizophrenia Bulletin, 40, 904913.10.1093/schbul/sbt093CrossRefGoogle ScholarPubMed
de Medeiros, K. et al. (2010). The Neuropsychiatric Inventory-Clinician rating scale (NPI-C): reliability and validity of a revised assessment of neuropsychiatric symptoms in dementia. International Psychogeriatrics, 22, 984994.10.1017/S1041610210000876CrossRefGoogle ScholarPubMed
de Vugt, M.E. et al. (2006). Impact of behavioural problems on spousal caregivers: a comparison between Alzheimer’s disease and frontotemporal dementia. Dementia and Geriatric Cognitive Disorders, 22, 3541.10.1159/000093102CrossRefGoogle ScholarPubMed
Djamanakova, A. et al. (2013). Diffeomorphic brain mapping based on T1-weighted images: improvement of registration accuracy by multichannel mapping. Journal of Magnetic Resonance Imaging, 37, 7684.10.1002/jmri.23790CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E. and McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198.CrossRefGoogle ScholarPubMed
Fusar-Poli, P. et al. (2011). Altered brain function directly related to structural abnormalities in people at ultra high risk of psychosis: longitudinal VBM-fMRI study. Journal of Psychiatric Research, 45, 190198.CrossRefGoogle ScholarPubMed
Gallagher, D., Fischer, C.E. and Iaboni, A. (2017). Neuropsychiatric symptoms in mild cognitive impairment. The Canadian Journal of Psychiatry, 62, 161169.10.1177/0706743716648296CrossRefGoogle ScholarPubMed
Goodglass, H (1983). The Assessment of Aphasia and Related Disorders (2nd ed) Williams & Wilkins.Google Scholar
Hentschel, F. et al. (2005). The clinical utility of structural neuroimaging with MRI for diagnosis and differential diagnosis of dementia: a memory clinic study. International Journal of Geriatric Psychiatry, 20, 645650.10.1002/gps.1333CrossRefGoogle ScholarPubMed
Hu, X. et al. (2015). Anatomical correlates of the neuropsychiatric symptoms in Alzheimer’s disease. Current Alzheimer Research, 12, 266–77.CrossRefGoogle ScholarPubMed
Ismail, Z. et al. (2017). The Mild Behavioral Impairment Checklist (MBI-C): a rating scale for neuropsychiatric symptoms in pre-dementia populations. Journal of Alzheimer’s Disease, 56, 929938.10.3233/JAD-160979CrossRefGoogle ScholarPubMed
Koppel, J. et al. (2012). Relationships between behavioral syndromes and cognitive domains in Alzheimer disease: the impact of mood and psychosis. The American Journal of Geriatric Psychiatry, 20, 9941000.CrossRefGoogle ScholarPubMed
Koppel, J. et al. (2018). Association between psychosis in elderly patients with Alzheimer disease and impaired social cognition. JAMA Psychiatry, 75, 652653.10.1001/jamapsychiatry.2018.0482CrossRefGoogle ScholarPubMed
Lezak, M.D. (2004c). Verbal functions and language skills. In Lezak, M.D. (ed.), Neuropsychological Assessment. Oxford: Oxford University Pressitor.Google Scholar
McLachlan, E. et al. (2018). Reduced parahippocampal volume and psychosis symptoms in Alzheimer’s disease. International Journal of Geriatric Psychiatry, 33, 389395.CrossRefGoogle ScholarPubMed
Miotto, E.C. et al. (2012). Hopkins verbal learning test-revised and brief visuospatial memory test-revised: preliminary normative data for the Brazilian population. Arquivos de Neuro-Psiquiatria, 70, 962965.10.1590/S0004-282X2012001200014CrossRefGoogle ScholarPubMed
Nakaaki, S. et al. (2013). Neuroanatomical abnormalities before onset of delusions in patients with Alzheimer’s disease: a voxel-based morphometry study. Neuropsychiatric Disease and Treatment, 9, 18.Google ScholarPubMed
Nilsson, F.M. (2007). Mini Mental State Examination (MMSE) – probably one of the most cited papers in health science. Acta Psychiatrica Scandinavica, 116, 156157.CrossRefGoogle ScholarPubMed
Oishi, K. et al. (2009). Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer’s disease participantstlas. Neuroimage, 46, 486499.CrossRefGoogle Scholar
Peters, M.E. et al. (2012). Prevalence of neuropsychiatric symptoms in CIND and its subtypes: the Cache County Study. The American Journal of Geriatric Psychiatry, 20, 416424.CrossRefGoogle ScholarPubMed
Pfeffer, R.I. et al. (1982). Measurement of functional activities in older adults in the community. The Journals of Gerontology, 37, 323329.CrossRefGoogle Scholar
Poulin, S.P. et al. (2017). Risk factors, neuroanatomical correlates, and outcome of neuropsychiatric symptoms in Alzheimer’s disease. Journal of Alzheimer’s Disease, 60, 483493.CrossRefGoogle ScholarPubMed
Rafii, M.S. et al. (2014). Neuropsychiatric symptoms and regional neocortical atrophy in mild cognitive impairment and Alzheimer’s disease. American Journal of Alzheimer's Disease & Other Dementias, 29, 159165.10.1177/1533317513507373CrossRefGoogle ScholarPubMed
Reitan, R.M. (1955). The relation of the trail making test to organic brain damage. Journal of Consulting and Clinical Psychology, 19, 393394.CrossRefGoogle ScholarPubMed
Rosenberg, P.B., Nowrangi, M.A. and Lyketsos, C.G. (2015). Neuropsychiatric symptoms in Alzheimer’s disease: What might be associated brain circuits? Molecular Aspects of Medicine, 43–44, 2537.10.1016/j.mam.2015.05.005CrossRefGoogle ScholarPubMed
Ruff, R.M. et al. (1996). Benton controlled oral word association test: reliability and updated norms. Archives of Clinical Neuropsychology, 11, 329338.CrossRefGoogle ScholarPubMed
Shin, I.S. et al. (2005). Neuropsychiatric symptoms and quality of life in Alzheimer disease. The American Journal of Geriatric Psychiatry, 13, 469474.CrossRefGoogle ScholarPubMed
Steinberg, M. et al. (2004). The persistence of neuropsychiatric symptoms in dementia: the Cache County Study. International Journal of Geriatric Psychiatry, 19, 1926.10.1002/gps.1025CrossRefGoogle ScholarPubMed
Steinberg, M. et al. (2008). Point and 5-year period prevalence of neuropsychiatric symptoms in dementia: the Cache County Study. International Journal of Geriatric Psychiatry, 23, 170177.10.1002/gps.1858CrossRefGoogle ScholarPubMed
Tan, L.L., Wong, H.B. and Allen, H. (2005). The impact of neuropsychiatric symptoms of dementia on distress in family and professional caregivers in Singapore. International Psychogeriatrics, 17, 253263.CrossRefGoogle Scholar
Tang, X. et al. (2013). Bayesian parameter estimation and segmentation in the multi-atlas random orbit model. PLoS One, 8, e65591.Google ScholarPubMed
Tariot, P.N. et al. (1995). The behavior rating scale for dementia of the consortium to establish a registry for Alzheimer’s sisease. The behavioral pathology committee of the consortium to establish a registry for Alzheimer’s disease. The American Journal of Psychiatry, 152, 134913457.Google Scholar
Tascone, L.D.S. et al. (2017). Cortical brain volume abnormalities associated with few or multiple neuropsychiatric symptoms in Alzheimer’s disease. PLoS One, 12, e0177169.CrossRefGoogle ScholarPubMed
Tatsumi, H. et al. (2009). Neuropsychiatric symptoms predict change in quality of life of Alzheimer disease patients: a two-year follow-up study. Psychiatry and Clinical Neurosciences, 63, 374384.10.1111/j.1440-1819.2009.01955.xCrossRefGoogle ScholarPubMed
Teng, E.L. and Chui, H.C. (1987). The Modified Mini-Mental State (3MS) examination. The Journal of Clinical Psychiatry, 48, 314318.Google ScholarPubMed
Tombaugh, T.N. and McIntyre, N.J. (1992). The mini-mental state examination: a comprehensive review. Journal of the American Geriatrics Society, 40, 922–35.CrossRefGoogle ScholarPubMed
Tschanz, J.T. et al. (2011). Progression of cognitive, functional, and neuropsychiatric symptom domains in a population cohort with Alzheimer dementia: the Cache County Dementia Progression study. The American Journal of Geriatric Psychiatry, 19, 532542.CrossRefGoogle Scholar
Wu, D. et al. (2016). Resource atlases for multi-atlas brain segmentations with multiple ontology levels based on T1-weighted MRI. Neuroimage, 125, 120–30.10.1016/j.neuroimage.2015.10.042CrossRefGoogle ScholarPubMed
Yesavage, J.A. et al. (1982). Development and validation of a geriatric depression screening scale: a preliminary report. Journal of Psychiatric Research, 17, 3749.10.1016/0022-3956(82)90033-4CrossRefGoogle ScholarPubMed