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Understanding brain resilience in superagers: a systematic review

  • Diagnostic Neuroradiology
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Abstract

Purpose

Superagers are older adults presenting excellent memory performance that may reflect resilience to the conventional pathways of aging. Our contribution aims to shape the evidence body of the known distinctive biomarkers of superagers and their connections with the Brain and Cognitive Reserve and Brain Maintenance concepts.

Methods

We performed a systematic literature search in PubMed and ScienceDirect with no limit on publication date for studies that evaluated potential biomarkers in superagers classified by validated neuropsychological tests. Methodological quality was assessed using the QUADAS-2 tool.

Results

Twenty-one studies were included, the majority in neuroimaging, followed by histological, genetic, cognition, and a single one on blood plasma analysis. Superagers exhibited specific regions of cortical preservation, rather than global cortical maintenance, standing out the anterior cingulate and hippocampus regions. Both superagers and controls showed similar levels of amyloid deposition. Moreover, the functional oscillation patterns in superagers resembled those described in young adults. Most of the quality assessment for the included studies showed medium risks of bias.

Conclusion

This systematic review supports selective cortical preservation in superagers, comprehending regions of the default mode, and salience networks, overlapped by stronger functional connectivity. In this context, the anterior cingulate cortex is highlighted as an imaging and histologic signature of these subjects. Besides, the biomarkers included pointed out that the Brain and Cognitive Reserve and Brain Maintenance concepts are independent and complementary in the superagers’ setting.

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Abbreviations

ACC:

Anterior cingulate cortex

AMC:

Age-matched controls

DMN:

Default mode network

MAC:

Middle-age controls

PiB:

Pittsburgh Compound B

SA:

Superagers

SN:

Salience network

y:

Years old

YC:

young controls

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Acknowledgments

We thank Charlesworth, Author Services, for scientific language editing.

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No funding was received for this study.

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Authors and Affiliations

  1. The National Hospital of Neurology and Neurosurgery, University College London, London, UK

    Laiz Laura de Godoy & Sotirios Bisdas

  2. Department of Radiology and Oncology, Hospital das Clínicas, Faculdade de Medicina da Universidade de São Paulo, Sao Paulo, Brazil

    Laiz Laura de Godoy, Adalberto Studart-Neto, Ricardo Nitrini & Claudia da Costa Leite

  3. Division of Neuroradiology, Department of Radiology, The Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Cesar Augusto Pinheiro Ferreira Alves & Juan Sebastian Martin Saavedra

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  1. Laiz Laura de Godoy
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  2. Cesar Augusto Pinheiro Ferreira Alves
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Correspondence to Laiz Laura de Godoy.

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Key Points

• Superagers showed selective cortical preservation in some DMN and SN regions, overlapped by stronger functional connectivity akin to young adults (Cognitive Reserve and Brain Maintenance).

• The anterior cingulate cortex is a key structure of superagers in different biomarkers' sources (structural and functional MRI and histological studies).

• Levels of amyloid deposition were not related to the superager subjects, pointing out that brain resilience may be partially independent of neurodegeneration (Brain and Cognitive Reserve).

• Brain and Cognitive Reserve and Brain Maintenance concepts tend to exert independent and complementary roles in the setting of superagers.

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de Godoy, L.L., Alves, C.A.P.F., Saavedra, J.S.M. et al. Understanding brain resilience in superagers: a systematic review. Neuroradiology 63, 663–683 (2021). https://doi.org/10.1007/s00234-020-02562-1

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