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@ARTICLE{Richter:1040638,
author = {Richter, Nils and Breidenbach, Laura and Schmieschek,
Maximilian HT and Heiss, Wolf-Dieter and Fink, Gereon Rudolf
and Onur, Özgür},
title = {{A}lzheimer-typical temporo-parietal atrophy and
hypoperfusion are associated with a more significant
cholinergic impairment in amnestic neurodegenerative
syndromes},
journal = {Journal of Alzheimer's disease},
volume = {104(4)},
issn = {1387-2877},
address = {Amsterdam},
publisher = {IOS Press},
reportid = {FZJ-2025-01978},
year = {2025},
note = {J Alzheimers Dis 2025 Apr;104(4):1290-1300. The authors
disclosed receipt of the following financial support for the
research, authorship, and/or publication of this article:
This work was supported by a grant from the Marga and Walter
Boll Foundation (Nr. 210-08-13), Kerpen, Germany, to GRF and
OO.},
abstract = {BackgroundTo date, cholinomimetics remain central in the
pharmacotherapy of Alzheimer's disease (AD) dementia.
However, postmortem investigations indicate that the
AD-typical progressive amnestic syndrome may also result
from predominantly limbic non-AD neuropathology such as
TDP-43 proteinopathy and argyrophilic grain disease.
Experimental evidence links a beneficial response to
cholinomimetics in early AD to reduced markers of
cholinergic neurotransmission. However, the cholinergic
impairment varies among patients with a clinical AD
presentation, likely due to non-AD
(co)-pathologies.ObjectiveThis study examines whether
AD-typical atrophy and hypoperfusion can provide information
about the cholinergic system in clinically diagnosed
AD.MethodsThirty-two patients with amnestic mild cognitive
impairment or mild dementia due to AD underwent positron
emission tomography (PET) with the tracer
N-methyl-4-piperidyl-acetate (MP4A) to estimate
acetylcholinesterase (AChE) activity, neurological
examinations, cerebral magnetic resonance imaging (MRI) and
neuropsychological assessment. The ‘cholinergic deficit’
was computed as the deviation of AChE activity from
cognitively normal controls across the cerebral cortex and
correlated gray matter (GM) and perfusion of
temporo-parietal cortices typically affected by AD and basal
forebrain (BF) GM.ResultsTemporo-parietal perfusion and GM,
as well as the inferior temporal to medial temporal ratio of
perfusion correlated negatively with the ‘cholinergic
deficit’. A smaller Ch4p area of the BF was associated
with a more significant ‘cholinergic deficit’, albeit to
a lesser degree than cortical measures.ConclusionsIn
clinically diagnosed AD, temporo-parietal GM and perfusion
are more closely associated with the ‘cholinergic
deficit’ than BF volumes, making them possible markers for
cholinergic treatment response in amnestic
neurodegeneration.IntroductionAlzheimer's disease (AD),
biologically characterized by the accumulation of amyloid
and tau pathologies and subsequent neurodegeneration,1
typically first presents with slowly progressive memory
impairment. The observation of particularly severe
degeneration of the cholinergic basal forebrain in AD led to
the use of cholinomimetics, which to date are central to AD
pharmacotherapy.2,3 However, the effects of these
medications are limited and vary considerably across
patients, while side-effects often limit their use.
Nonetheless, cholinergic pharmacotherapy is likely to remain
relevant despite the introduction of anti-amyloid
medications, given the moderate effects, side-effects, and
contraindications of current anti-amyloid therapies and the
lack of alternatives.4 Given the enormous burden of AD and
other amnestic neurodegenerative syndromes on patients and
caregivers and the risk of side-effects in the often
geriatric patients, it is therefore crucial to identify
factors that will allow a targeted use of cholinergic
medications and ensure an appropriate risk-benefit balance
for each patient.An explanation for the variable treatment
response and limited group level effects of cholinomimetics
may be, that a relevant ‘cholinergic deficit’ is
required for patients to benefit from these medications and
that the degree of cholinergic degeneration varies
considerably across patients. Supporting this idea, we
previously observed that even patients with mild cognitive
impairment (MCI) due to AD may benefit from cholinergic
stimulation, but the treatment response depended on the
degree of cholinergic impairment.5 Interestingly, even in
this relatively homogenous group, the cortical levels of
acetylcholinesterase (AChE), a critical enzyme of
cholinergic neurotransmission, varied substantially between
patients.6 There is also evidence for more severe
cholinergic impairment in patients with early-onset than
late-onset AD.6–8A cause of the variability in cholinergic
degeneration and, consequently, response to cholinergic
treatment could be the heterogeneity of underlying
neuropathology. Trials examining the efficacy of cholinergic
medications recruited patients based purely on a clinical AD
diagnosis.9–11 However, it has become clear, that the
AD-typical amnestic syndrome may also be caused by non-AD
pathologies.12 Non-AD pathological change is common and can
be observed as co-pathology in up to half of the patients
with molecular evidence of AD-pathology, especially with
increasing age.12–14 It remains unclear, how limbic
predominant non-AD pathologies, such as limbic-predominant
age-associated TDP-43 encephalopathy (LATE) and argyrophilic
grain disease, affect the cholinergic system. Basal
forebrain atrophy has been linked to amyloid and Lewy-body
pathology rather than LATE.15 Furthermore, the basal
forebrain does not appear particularly susceptible to the
TDP-43 pathology observed in frontotemporal lobar
degeneration,16 and total basal forebrain volumes measured
using MRI did not differ between patients with pure-AD and
pure LATE neuropathological change.17Specific molecular
markers of cholinergic neurotransmission, such as the
activity of critical enzymes, transporters, and receptors,
can be quantified in vivo using positron emission tomography
(PET).18–20 However, these techniques are
resource-intensive, and their use, hence, remains restricted
to specialized centers, limiting their utility in
large-scale studies of treatment response. However, AD and
non-AD (co)-pathologies are associated with specific
hypometabolism and atrophy patterns:13,21–25 The common
non-AD pathologies predominantly affect the medial temporal
lobe, whereas AD also affects lateral temporal and parietal
cortices. Furthermore, the volume of basal forebrain
structures, which are the source of cholinergic input to the
cerebral cortex, can be assessed with MRI methods similar to
those routinely used in the clinical setting.6,26,27
Therefore, these markers, thought to reflect different
underlying pathologies, might be suitable for indirectly
assessing the degree of cholinergic dysfunction in
vivo.Hence, we here examined putative structural (MRI) and
metabolic (PET) imaging markers that could provide insights
regarding the integrity of the cortical cholinergic system
in patients with a clinical diagnosis of AD. Specifically,
based on our prior work, we hypothesized (1) that the volume
of the posterior basal forebrain (Ch4p region) would be more
closely correlated with levels of cortical AChE activity
than that of the whole basal forebrain. Furthermore, we
hypothesized (2) that the inferior temporal gyrus to medial
temporal (ITM) ratio of cerebral perfusion, which contrasts
perfusion in areas of AD- and non-AD-degeneration,13,21 and
perfusion of temporo-parietal cortices, serving as markers
of AD-specific degeneration, would also be correlated with
cortical AChE activity.},
cin = {INM-3},
ddc = {610},
cid = {I:(DE-Juel1)INM-3-20090406},
pnm = {5251 - Multilevel Brain Organization and Variability
(POF4-525)},
pid = {G:(DE-HGF)POF4-5251},
typ = {PUB:(DE-HGF)16},
doi = {10.1177/13872877251324080},
url = {https://juser.fz-juelich.de/record/1040638},
}