Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields
Open accessAbstract
Histopathological studies and animal models suggest that different physiological and pathophysiological processes exert different subfield specific effects on the hippocampus. High‐resolution images at 4T depict details of the internal structure of the hippocampus allowing for in vivo volumetry of hippocampal subfields. The aims of this study were (1) to determine patterns of hippocampal subfield volume loss due to normal aging and Apo e4 carrier state, (2) to determine subfield specific volume losses due to preclinical (MCI) and clinical Alzheimer's disease (AD) and their modification due to age and Apo e4 carrier state. One hundred fifty seven subjects (119 cognitively healthy elderly controls, 20 MCI and 18 AD) were studied with a high resolution T2 weighted imaging sequence obtained at 4T aimed at the hippocampus. Apo e4 carrier state was known in 95 subjects (66 controls, 14 MCI, 15 AD). Subiculum (SUB), CA1, CA1‐CA2 transition zone (CA1‐2 transition), CA3‐ dentate gyrus (CA3&DG) were manually marked. Multiple linear regression analysis was used to test for effects of age, Apo e4 carrier state and effects of MCI and AD on different hippocampal subfields. Age had a significant negative effect on CA1 and CA3&DG volumes in controls ( P < 0.05). AD had significantly smaller volumes of SUB, CA1, CA1‐2 transition, and MCI had smaller CA1‐2 transition volumes than controls ( P < 0.05). Apo e4 carrier state was associated with volume loss in CA3&DG compared to non‐Apo e4 carriers in healthy controls and AD. Based on these findings, we conclude that subfield volumetry provides regional selective information that allows to distinguish between different normal and pathological processes affecting the hippocampus and thus for an improved differential diagnosis of neurodegenerative diseases affecting the hippocampus. © 2009 Wiley‐Liss, Inc.
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Written from the paper’s full text.
TL;DR
High-resolution 4T MRI subfield volumetry detected selective hippocampal subfield effects of age, Apo e4 carrier state, and Alzheimer’s disease/MCI. The authors conclude that subfield volumetry provides regional information beyond total hippocampal volume for differentiating normal and pathological processes.
Key findings
- In cognitively intact controls, age had a significant negative effect on CA1 (β = −1.02, P < 0.0001) and CA3&DG (β = −1.15, P < 0.001); CA1 was stable until the 6th decade and CA3&DG until the 5th decade before declining.
- AD had significantly smaller SUB (94.9 ± 31.4 vs. 119.2 ± 23.96), CA1 (165.6 ± 38.6 vs. 203.3 ± 29.3), and CA1–2 transition volumes (8.5 ± 2.0 vs. 12.1 ± 3.3) than controls, while CA3&DG was not different; MCI showed significant volume loss only in CA1–2 transition (9.02 ± 1.64 vs. controls).
- Apo e4 carrier state was associated with smaller CA3&DG volumes in healthy controls (Apo e4 negative 146 ± 24.1 vs. positive 134.06 ± 25.1) and in AD (Apo e4 negative 159.0 ± 29.6 vs. positive 124.8 ± 26.8); MCI Apo e4 carriers also had smaller CA3&DG (132.0 ± 12.5 vs. 141.9 ± 35.3) but not significantly.
Methods
- One hundred fifty-seven subjects were studied: 119 cognitively healthy elderly controls, 20 MCI, and 18 AD; Apo e4 carrier state was known in 95 subjects (66 controls, 14 MCI, 15 AD).
- High-resolution T2-weighted fast spin echo images were acquired at 4T; SUB, CA1, CA1–CA2 transition zone, and CA3&DG were manually marked, with intracranial volume used as a covariate.
- Multiple linear regression tested effects of age, Apo e4, and disease group; post hoc analyses used Duncan’s tests or Mann–Whitney tests.
Limitations
- The paper states that the AD and MCI samples were relatively small, that findings in the small Apo e4 subgroup are preliminary and need confirmation in a larger population, and that histopathological correlation studies are necessary to verify the subfield findings.
- The paper notes that manual subfield labeling is time-consuming and requires an experienced rater, limiting usefulness for large studies; automated methods have their own sensitivity to shape variants, intensity changes, and image quality.
- Evident from the text: the study is cross-sectional, Apo e4 genotype was available only in a subset, and no direct histopathological validation was performed.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
0 of 11 cited sources checked · 0 supported · 0 flagged
- Findingown data
Elderly controls (60-85 years) with Apo e4 have smaller CA3&DG volumes than those without (127.0 ± 24.7 vs 144.0 ± 24.8).
“as did the group of elderly (60–85 yrs) controls (127.0 ± 24.7 vs. 144.0 ± 24.8).”
Quote in the paperSubstantial claim - Findingown data
In controls with known Apo e4 status, the interaction between Apo e4 and age on CA3&DG is not significant.
“however, the interaction between Apo e4 and age was not significant.”
Quote in the paperNot a substantial claim - Findingown data
In controls with known Apo e4 status, CA1 volume is not influenced by Apo e4 carrier state (P = 0.81).
“CA1 volume was not influenced by Apo e4 carrier state (P = 0.81)”
Quote in the paperSubstantial claim - Findingown data
In controls with known Apo e4 status, age has a significant negative effect on CA3&DG volume (β = −0.78, P = 0.02).
“Similarly as in the total population, there was also a significant effect for age on CA3&DG (β = −0.78, P = 0.02)”
Quote in the paperSubstantial claim - Findingown data
In the subgroup with known Apo e4 carrier state, CA3&DG has a significant Apo e4 effect (Apo e4 negative β = 15.7, P = 0.0031).
“and Apo e4 effect (Apo e4 negative β = 15.7, P = 0.0031).”
Quote in the paperSubstantial claim
- Findingown data
AD does not have significantly different CA3&DG volumes compared to controls.
“whereas CA3&DG volumes were not different (137.1 ± 29.9 vs. 141.0 ± 26.2).”
Quote in the paperSubstantial claim - Findingown data
In controls with known Apo e4 status, Apo e4 carrier state is associated with smaller CA3&DG volumes (non-carriers 146 ± 24.1 vs carriers 134.06 ± 25.1).
“There was significant effect for Apo e4 (β = 9.45, P = 0.042) on CA3&DG, indicating that subjects without Apo e4 had larger CA3&DG volumes (146 ± 24.1) than subjects with Apo e4 (134.06 ± 25.1).”
Quote in the paperSubstantial claim - Findingown data
There are no significant differences in subfield volumes between AD and MCI.
“There were no significant differences between AD and MCI”
Quote in the paperSubstantial claim - Findingown data
Age has a significant negative effect on CA3&DG volume in cognitively healthy controls.
“A significant negative age effect was found for CA1 (β = −1.02, P < 0.0001) and CA3&DG (β = −1.15, P < 0.001).”
Quote in the paperSubstantial claim - Findingown data
MCI has significantly reduced CA1-2 transition volume compared to controls.
“In contrast, the atrophy was more restricted in MCI who showed significant volume losses in CA1–2 transition (9.02 ± 1.64) compared to controls”
Quote in the paperSubstantial claim - Findingown data
AD has significantly reduced SUB, CA1, and CA1-2 transition volumes compared to controls.
“Post-hoc analyses showed that AD had significantly reduced SUB (94.9 ± 31.4 vs. 119.2 ± 23.96), CA1 (165.6 ± 38.6 vs. 203.3 ± 29.3), and CA1–2 transition volumes (8.5 ± 2.0 vs.12.1 ± 3.3) compared to controls”
Quote in the paperSubstantial claim - Findingown data
In controls with known Apo e4 status, CA1 volume shows a significant negative age effect (β = −1.69, P = 0.0002).
“but showed a significant age effect (β = −1.69; P = 0.0002) as in the previous analysis”
Quote in the paperSubstantial claim - Findingown data
In the subgroup with known Apo e4 carrier state, MCI has smaller CA1-2 transition volume than controls.
“The results regarding group effect remained unchanged, that is, AD had smaller SUB, CA1, CA1–2 transition volumes and MCI had smaller CA1–2 transition volumes than controls.”
Quote in the paperSubstantial claim - Findingown data
AD subjects with Apo e4 have smaller CA3&DG volumes than AD subjects without Apo e4 (124.8 ± 26.8 vs 159.0 ± 29.6).
“Posthoc tests showed that AD with Apo e4 had smaller CA3&DG than those without (124.8 ± 26.8 vs. 159.0 ± 29.6)”
Quote in the paperSubstantial claim - Findingown data
In the subgroup with known Apo e4 carrier state, CA3&DG has a significant negative age effect (β = −1.58, P = 0.024).
“CA3&DG had a significant age effect (β = −1.58, P = 0.024)”
Quote in the paperSubstantial claim - Findingown data
In the subgroup with known Apo e4 carrier state, AD has smaller SUB, CA1, and CA1-2 transition volumes than controls.
“The results regarding group effect remained unchanged, that is, AD had smaller SUB, CA1, CA1–2 transition volumes and MCI had smaller CA1–2 transition volumes than controls.”
Quote in the paperSubstantial claim - Findingown data
Age has a significant negative effect on CA1 volume in cognitively healthy controls.
“A significant negative age effect was found for CA1 (β = −1.02, P < 0.0001)”
Quote in the paperSubstantial claim - Interpretationreasoning
Neuroimaging methods able to obtain subfield-specific information might allow for a better differentiation of different disease processes than total hippocampal volume, which is currently the gold standard for in vivo assessment of hippocampal structural damage.
“These findings suggest that neuroimaging methods able to obtain subfield specific information might allow for a better differentiation of different disease processes than total hippocampal volume that is currently the gold standard for the in vivo assessment of hippocampal structural damage.”
Quote in the paperSubstantial claim - Interpretationown data
In vivo subfield volumetry using high-resolution MR images and a manual parcellation scheme can identify regional selective effects of age, Apo e4, and AD on the hippocampus.
“The most important finding of this study was that in vivo subfield volumetry obtained using high resolution MR images and a manual parcellation scheme was able to identify regional selective effects of age and Apo e4 and AD on the hippocampus.”
Quote in the paperSubstantial claim
- May combine two claims. 12
- The quote only partly states this claim. 1
- Classified as probably not a substantial claim. 10
May combine two claims.
Findingown dataIn the analysis of AD and MCI with age- and gender-matched controls, disease group has significant effects on SUB, CA1, and CA1-2 transition volumes but not on CA3&DG.
“Multiple regression analysis showed significant effects for disease group (defined as control, MCI, and AD) for SUB (P = 0.003), CA1 (P = 0.0001), and CA1–2 transition (P < 0.0001) but not for CA3&DG.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataIn controls, CA1 volumes are stable until the 6th decade, after 60 years they become increasingly smaller.
“CA1 volumes were stable until the 6th decade, after 60 yrs of age; CA1 volumes started getting increasingly smaller.”
Quote in the paperSubstantial claimThe quote only partly states this claim.
Findingown dataIn controls, CA3&DG volumes are stable up to the 5th decade and then become increasingly smaller.
“CA3&DG volumes stayed stable up to the 5th decade and then became increasingly smaller”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataMCI subjects with Apo e4 have smaller CA3&DG volumes than those without (132.0 ± 12.5 vs 141.9 ± 35.3), but the difference is not significant.
“MCI with the Apo e4 also had smaller CA3&DG than those without (132.0 ± 12.5 vs. 141.9 ± 35.3); however, the difference was not significant”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataMCI does not have significantly reduced SUB, CA1, or CA3&DG volumes compared to controls.
“but not in SUB (112.9 ± 23.4), CA1 (181.2 ± 30.3), or CA3&DG (140.9 ± 24.4).”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductown dataThe findings in the small AD and MCI sample are preliminary and need confirmation in a larger population.
“The findings in this small sample therefore have to be considered preliminary and have to be confirmed in a larger population.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationDifferent physiological and pathophysiological processes exert different subfield-specific effects on the hippocampus.
“Histopathological studies and animal models suggest that different physiological and pathophysiological processes exert different subfield specific effects on the hippocampus.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationApo e4 is the best documented genetic risk factor for sporadic AD, although it is insufficient to explain all cases of sporadic late onset AD as only 40-80% of all AD patients carry the Apo e4 allele.
“The best documented genetic risk factor for sporadic AD is apolipoprotein E4 (Apo e4), although it is insufficient to explain all cases of sporadic late onset AD as only 40–80% of all AD patients carry the Apo e4 allele (Waring and Rosenberg, 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Waring and Rosenberg, 2008
Not checked in the free run.
May combine two claims.
Study design and conductreasoningThe sample size of the AD and MCI group was relatively small, so it cannot be excluded that the study lacked statistical power to differentiate between strong AD effects and more subtle Apo e4 effects.
“But again, the sample size of the AD and MCI group was relatively small and thus it cannot be excluded that we lacked the statistical power to differentiate between the strong AD effects active in CA1, CA1–2, SUB and ERC, and the probably more subtle effect of Apo e4.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationThe hippocampus is not a homogeneous structure but consists of several histologically and functionally specialized but tightly interconnected subfields: the subiculum (SUB), the cornu ammonis sectors (CA) 1-3, and the dentate gyrus (DG).
“However, the hippocampus is not a homogeneous structure but consists of several histologically and functionally specialized but tightly interconnected subfields: the subiculum (SUB), the cornu ammonis sectors (CA) 1–3, and the dentate gyrus (DG) (Duvernoy, 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Duvernoy, 2005 source
Not checked in the free run.
May combine two claims.
PremisecitationAnimal and histopathological studies have shown that different pathological conditions exert regional selective effects on hippocampal subfields, for example, AD and hypoxia damage preferentially CA1, schizophrenia CA2, and post-traumatic stress syndrome CA3.
“Animal and histopathological studies have shown that different pathological conditions exert regional selective effects on hippocampal subfields, for example, AD and hypoxia damage preferentially CA1 (West et al., 2004), schizophrenia CA2 (Harrison, 2004), and post-traumatic stress syndrome CA3 (McEwen and Magarinos, 1997), and so forth.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites West et al., 2004
Not checked in the free run.
- cites Harrison, 2004
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- cites McEwen and Magarinos, 1997
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationAmnestic MCI is the most relevant subtype for AD, characterized by subjective and objective memory deficits but otherwise intact cognitive functions.
“The most relevant subtype for AD is amnestic MCI, which is characterized by subjective and objective memory deficits but otherwise intact cognitive functions.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Petersen et al., 1999
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationMCI is a clinical concept defining the transition from normal aging to possible AD; subjects with MCI are not demented but have significant deficits in one or several cognitive domains and an increased risk to develop dementia.
“The concept of mild cognitive impairment (MCI) is an attempt to clinically define this transition from normal aging to possible AD. Subjects diagnosed with MCI are not demented, but have significant deficits in one or several cognitive domains and an increased risk to develop dementia.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Petersen et al., 1999
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationMolecular pathomechanisms leading to AD are active several years before the patient becomes cognitively impaired.
“There is increasing evidence that the molecular pathomechanisms leading to AD are active several years before the patient becomes cognitively impaired (DeKosky and Marek, 2003).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites DeKosky and Marek, 2003
Not checked in the free run.
May combine two claims.
Interpretationown dataSubfield volumetry provides regional selective information that allows distinguishing between different normal and pathological processes affecting the hippocampus and thus improves differential diagnosis of neurodegenerative diseases affecting the hippocampus.
“Based on these findings, we conclude that subfield volumetry provides regional selective information that allows to distinguish between different normal and pathological processes affecting the hippocampus and thus for an improved differential diagnosis of neurodegenerative diseases affecting the hippocampus.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductcitationThe method used for subfield marking, including assessment of measurement reliability, has been described in detail previously.
“The method used for subfield marking including assessment of measurement reliability has been described in detail previously (Mueller et al., 2007, 2008).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Mueller et al., 2007
Not checked in the free run.
- cites Mueller et al., 2008
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationAge is the most consistent epidemiological risk factor for sporadic AD, with prevalence increasing from 1% at age 65 to 40-50% by age 95.
“Age is the most consistent epidemiological risk factor with the prevalence of the disease increasing from 1% at age 65 to 40–50% by the age of 95 (Wang and Ding, 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Wang and Ding, 2008
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Classified as probably not a substantial claim.
Study design and conductreasoningICV was used as a covariate in all analyses to account for volumetric differences due to different head sizes.
“ICV in ccm was used as a covariate in all these analyses to account for volumetric differences due to different head sizes.”
Quote in the paperSubstantial claim
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The CA1 region is one of the earliest and more affected brain regions in AD patients.
“In contrast to 5xFAD, other FAD mouse models show clear intraneuronal Aβ accumulation and neuronal loss in the CA1 region [7, 16, 88], which has also been shown to be one of the earliest and more affected brain regions in AD patients [4, 27, 68, 82].”
From Senescence-related impairment of autophagy induces toxic intraneuronal amyloid-β accumulation in a mouse model of amyloid pathology (2023) · cites this paper as [82]
Controversial data were obtained particularly in studies that relied on manual versus automated segmentation methods.
“As for the second point of concern, controversial data were obtained particularly in studies that relied on manual versus automated segmentation methods.”
From Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease (2015) · cites this paper as [35]
The volume of the subiculum was reported to be normal in MCI in a manual segmentation study and an automated segmentation study but significantly reduced in two other studies using manual or automated segmentation.
“Thus, for example, the volume of the subiculum was reported to be normal in MCI in a study that relied on manual segmentation [35] and in another study that used an automated segmentation method [38] but was significantly reduced in two other studies that also used a method of manual [39] or automated segmentation [40].”
From Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease (2015) · cites this paper as [35]
The most critical issues explaining contrasting data regard the diagnostic criteria adopted in sample selection and the reliability of segmentation techniques for discriminating between individual hippocampal subfields.
“Probably, the most critical issues regard the diagnostic criteria adopted in sample selection and the reliability of the segmentation techniques used for discriminating between individual hippocampal subfields.”
From Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease (2015) · cites this paper as [35]
Literature on individuals with MCI is more controversial, with discrepant data resulting from adoption of the same subfield segmentation procedure.
“Analogous literature on individuals with MCI is still more controversial, with discrepant data resulting from adoption of the same subfield segmentation procedure.”
From Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease (2015) · cites this paper as [35]
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- Authors
- Mueller, S. G., & Weiner, M. W.
- Affiliations
- San Francisco VA Medical Center (US)
- Corresponding author
- Mueller, Susanne G.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2009-04-29
- Volume
- 19
- Issue
- 6
- Pages
- 558-564
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC2802542
- OpenAlex
- W1984748043
- Cited by
- 248
- References
- 43
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 6 · 2023: 12 · 2022: 10 · 2021: 15 · 2020: 16 · 2019: 13 · 2018: 12 · 2017: 17 · 2016: 17 · 2015: 25 · 2014: 27 · 2013: 22 · 2012: 14
- FWCI
- 8.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (P01AG 12435, R01AG010897, P01AG012435)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal subfields, Alzheimer's disease, mild cognitive impairment, APOE ε4, normal aging, CA1, CA3, dentate gyrus, subiculum, differential diagnosis of neurodegenerative diseases
- MeSH terms
- Adult, Age Factors, Aged, Aged, 80 and over, Aging, Alzheimer Disease, Cognition Disorders, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Organ Size, Linear Models, Sequence Analysis, DNA, Apolipoprotein E4, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.
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