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Basal Forebrain Volume, but Not Hippocampal Volume, Is a Predictor of Global Cognitive Decline in Patients with Alzheimer’S Disease

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Basal Forebrain Volume, but Not Hippocampal Volume, Is a Predictor of Global Cognitive Decline in Patients with Alzheimer’S Disease ORIGINAL RESEARCH published: 14 August 2018 doi: 10.3389/fneur.2018.00642 Basal Forebrain Volume, but Not Hippocampal Volume, Is a Predictor of Global Cognitive Decline in Patients With Alzheimer’s Disease Edited by: Treated With Cholinesterase Lars Ersland, Haukeland University Hospital, Inhibitors Norway Reviewed by: Stefan J. Teipel 1,2*, Enrica Cavedo 3,4,5,6,7, Harald Hampel 3,4,5,6 and Michel J. Grothe 1 for Elizabeth J. Coulson, the Alzheimer’s Disease Neuroimaging Initiative† and Alzheimer Precision Medicine The University of Queensland, Initiative (APMI) Australia Karsten Specht, 1 German Center for Neurodegenerative Diseases-Rostock/Greifswald, Rostock, Germany, 2 Department of Psychosomatic University of Bergen, Norway Medicine, University of Rostock, Rostock, Germany, 3 AXA Research Fund and Sorbonne University Chair, Paris, France, *Correspondence: 4 Sorbonne University, GRC n◦ 21, Alzheimer Precision Medicine, AP-HP, Pitié-Salpêtrière Hospital, Boulevard de l’Hôpital, Stefan J. Teipel Paris, France, 5 Brain and Spine Institute (ICM), INSERM U 1127, CNRS UMR 7225, Boulevard de l’Hôpital, Paris, France, [email protected] 6 Department of Neurology, Institute of Memory and Alzheimer’s Disease (IM2A), Pitié-Salpêtrière Hospital, AP-HP, Boulevard de l’Hôpital, Paris, France, 7 IRCCS Istituto Centro San Giovanni di Dio-Fatebenefratelli, Brescia, Italy †Data used in preparation of this article were obtained from the Alzheimer’s Disease Neuroimaging Background: Predicting the progression of cognitive decline in Alzheimer’s disease Initiative (ADNI) database (AD) is important for treatment selection and patient counseling. Structural MRI markers (adni.loni.usc.edu/). As such, the investigators within the ADNI such as hippocampus or basal forebrain volumes might represent useful instruments contributed to the design and for the prediction of cognitive decline. The primary objective was to determine the implementation of ADNI and/or provided data but did not participate predictive value of hippocampus and basal forebrain volumes for global and domain in analysis or writing of this report. A specific cognitive decline in AD dementia during cholinergic treatment. complete listing of ADNI investigators can be found at: http://adni.loni.usc. Methods: We used MRI and cognitive data from 124 patients with the clinical diagnosis edu/wp-content/uploads/ of AD dementia, derived from the ADNI-1 cohort, who were on standard of care how_to_apply/ cholinesterase inhibitor treatment during a follow-up period between 0.4 and 3.1 years. ADNI_Acknowledgement_List.pdf We used linear mixed effects models with cognitive function as outcome to assess Specialty section: the main effects as well as two-way interactions between baseline volumes and time This article was submitted to controlling for age, sex, and total intracranial volume. This model accounts for individual Applied Neuroimaging, a section of the journal variation in follow-up times. Frontiers in Neurology Results: Basal forebrain volume, but not hippocampus volume, was a significant Received: 10 November 2017 Accepted: 17 July 2018 predictor of rates of global cognitive decline. Larger volumes were associated with smaller Published: 14 August 2018 rates of cognitive decline. Left hippocampus volume had a modest association with rates Citation: of episodic memory decline. Baseline performance in global cognition and memory was Teipel SJ, Cavedo E, Hampel H and significantly associated with hippocampus and basal forebrain volumes; in addition, basal Grothe MJ (2018) Basal Forebrain Volume, but Not Hippocampal forebrain volume was associated with baseline performance in executive function. Volume, Is a Predictor of Global Conclusions: Our findings indicate that in AD dementia patients, basal forebrain volume Cognitive Decline in Patients With Alzheimer’s Disease Treated With may be a useful marker to predict subsequent cognitive decline during cholinergic Cholinesterase Inhibitors. treatment. Front. Neurol. 9:642. doi: 10.3389/fneur.2018.00642 Keywords: cholinergic treatment, MRI, prediction, memory, executive function, basal forebrain, hippocampus Frontiers in Neurology | www.frontiersin.org 1 August 2018 | Volume 9 | Article 642 Teipel et al. Predicting Cognitive Decline in AD INTRODUCTION Initiative (ADNI-1) database, all receiving cholinergic treatment. Based on the previous evidence on the potential predictive A prediction of the individual course of cognitive change value of these brain regions in AD, we determined the in Alzheimer’s disease (AD) would help adequate resource association of hippocampus and basal forebrain volume with allocation, patient care, and counseling. Evidence suggests rates of global and domain-specific cognitive decline during that the hippocampus supports the consolidation of long- cholinergic treatment. We expected that lower basal forebrain term declarative memory (1, 2), showing neurodegeneration in (hippocampus) volume would predict a faster rate of global autopsy data and atrophy in in vivo MRI scans as early as in and executive (global and episodic memory) function. Secondly, predementia stages of AD (3, 4). Its measurement is standardized, we determined the predictive use of basal forebrain and robust, accessible and feasible for in vivo studies using established hippocampus volumes for the identification of cognitively stable volumetric protocols, with the most recent advance being an vs. cognitively declining patients, where we expected that internationally harmonized protocol for a consistent delineation cognitively stable patients would have larger basal forebrain and of the hippocampus’ anatomical borders on MRI scans (5). The hippocampus volumes at baseline. These data help to assess cholinergic basal forebrain is the main source of neocortical the potential usefulness of volumetric MRI to identify people acetylcholine (6), and is involved in attentional processes, such with a more rapid disease progression; such data would support as immediate recall and executive function (7). Autopsy studies clinical decision making on allocation of treatment resources found degeneration of cholinergic basal forebrain neurons in and care. early clinical stages of AD (8, 9), and the resulting reduction of cholinergic cortical activity represents the rationale for the use of cholinergic treatment in AD dementia. The hippocampus METHODS represents a key input area of cholinergic projections from the basal forebrain (10). In recent years, MRI based protocols for an Study Population automated measurement of cholinergic basal forebrain volumes Data used in the preparation of this article were obtained have been established that make use of stereotactic information from the Alzheimer’s Disease Neuroimaging Initiative (ADNI) derived from combined post mortem MRI and histology (11– database (adni.loni.usc.edu). The ADNI was launched in 2003 13). Based on these protocols, several MRI volumetric studies as a public-private partnership, led by Principal Investigator have shown consistent pattern of hippocampus and cholinergic Michael W. Weiner, MD. The primary goal of ADNI has basal forebrain atrophy in AD dementia (11, 14) and prodromal been to test whether serial magnetic resonance imaging (MRI), at-risk stages of AD dementia, such as amnestic mild cognitive positron emission tomography (PET), other biological markers, impairment (MCI) (15, 16) or individuals with amyloid positive and clinical and neuropsychological assessment can be combined MCI (17). to measure the progression of mild cognitive impairment (MCI) Based on these findings, hippocampus and cholinergic basal and early Alzheimer’s disease (AD). A fuller description of ADNI forebrain volumes may help to predict cognitive change and and up-to-date information is available at www.adni-info.org. response to cholinergic treatment in patients with AD dementia We retrieved data of participants of the ADNI-1 study who had or prodromal AD. A previous study found that the thickness of a clinical diagnosis of AD dementia at baseline, a baseline MRI the substantia innominata, a potential proxy of cholinergic basal scan, neuropsychological testing at baseline and follow-up and forebrain integrity (18), was associated with rates of cognitive documented treatment with any cholinesterase inhibitor during change in 82 AD dementia patients during 9 months of treatment follow-up time. We retrieved 124 cases, 56 women, fulfilling these with a cholinesterase inhibitor, with smaller rates of cognitive conditions. We included only people with a clinical diagnosis of decline in people with a lower thickness of the substantia AD dementia, because cholinesterase inhibitor treatment is only innominata (19). In people with MCI, hippocampus volume was approved for this diagnosis, but not for MCI or other diagnoses. associated with rates of cognitive decline with a moderate effect size (20–24). In 37 AD dementia cases, smaller hippocampus Neuropsychological Tests volume was associated with faster global cognitive decline during We used ADAScog11 as measure of global cognitive decline cholinergic treatment (25). In a recent randomized controlled (27–29). ADAScog 11 has frequently been used in clinical trial of donepezil, we found that hippocampus volume, but efficacy trials of cholinesterase inhibitors in AD as primary not basal forebrain volume, was a predictor of subsequent endpoint (30, 31). In addition, we used composite measures for cognitive decline in 216 MCI cases (26); this effect, however, memory and executive
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