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Brain age estimation reveals older adults’ accelerated senescence after traumatic brain injury

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Abstract

Adults aged 60 and over are most vulnerable to mild traumatic brain injury (mTBI). Nevertheless, the extent to which chronological age (CA) at injury affects TBI-related brain aging is unknown. This study applies Gaussian process regression to T1-weighted magnetic resonance images (MRIs) acquired within \(\sim\)7 days and again \(\sim\)6 months after a single mTBI sustained by 133 participants aged 20–83 (CA \(\mu \pm \sigma\) = 42.6 ± 17 years; 51 females). Brain BAs are estimated, modeled, and compared as a function of sex and CA at injury using a statistical model selection procedure. On average, the brains of older adults age by 15.3 ± 6.9 years after mTBI, whereas those of younger adults age only by 1.8 ± 5.6 years, a significant difference (Welch’s t32 =  − 9.17, p ≃ 9.47 × 10−11). For an adult aged \(\sim\)30 to \(\sim\)60, the expected amount of TBI-related brain aging is \(\sim\)3 years greater than in an individual younger by a decade. For an individual over \(\sim\)60, the respective amount is \(\sim\)7 years. Despite no significant sex differences in brain aging (Welch’s t108 = 0.78, p > 0.78), the statistical test is underpowered. BAs estimated at acute baseline versus chronic follow-up do not differ significantly (t264 = 0.41, p > 0.66, power = 80%), suggesting negligible TBI-related brain aging during the chronic stage of TBI despite accelerated aging during the acute stage. Our results indicate that a single mTBI sustained after age \(\sim\)60 involves approximately \(\sim\)10 years of premature and lasting brain aging, which is MRI detectable as early as \(\sim\)7 days post-injury.

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Abbreviations

AG:

Age gap

BA:

Biological age

CA:

Chronological age

HC:

Healthy control

MRI:

Magnetic resonance imaging

mTBI:

Mild traumatic brain injury

OA:

Older adult

YA:

Younger adult

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Acknowledgements

The authors are thankful to Michelle Y. Ha, Dylan Overby, and Chur Tam for their comments, suggestions, assistance with literature search, and figure preparation. This study was supported by the National Institutes of Health grant R01 NS 100973 to A.I., by the US Department of Defense contract W81XWH-18-1-0413 to A.I., by a Hanson-Thorell Family Research Scholarship, and by the James J. and Sue Femino Foundation. The funding sources had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

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Author notes

  1. Anar Amgalan and Alexander S. Maher contributed equally to this work.

Authors and Affiliations

  1. Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USA

    Anar Amgalan, Alexander S. Maher, Satyaki Ghosh & Andrei Irimia

  2. Department of Electronics and Electrical Engineering, Indian Institute of Technology, Guwahati, Assam, India

    Satyaki Ghosh

  3. Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    Helena C. Chui

  4. Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA

    Paul Bogdan

  5. Corwin D. Denney Research Center, Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA

    Andrei Irimia

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  1. Anar Amgalan
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  2. Alexander S. Maher
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Correspondence to Andrei Irimia.

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Amgalan, A., Maher, A.S., Ghosh, S. et al. Brain age estimation reveals older adults’ accelerated senescence after traumatic brain injury. GeroScience 44, 2509–2525 (2022). https://doi.org/10.1007/s11357-022-00597-1

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