Association of Osteoarthritis With Changes in Structural Neuroimaging Markers Over Time Among Non-demented Older Adults

Lichuang Wu, Xiang Wang, Yiheng Ye, Cailong Liu, Lichuang Wu, Xiang Wang, Yiheng Ye, Cailong Liu

Abstract

Objective: Although emerging evidence suggests that both osteoarthritis (OA) and brain atrophy (as assessed by structural neuroimaging markers) are associated with the risk of dementia, little is known about the association between OA and structural neuroimaging markers. This study aimed to examine the association of OA with changes in structural neuroimaging markers among non-demented older people. Methods: We examined the cross-sectional and longitudinal associations between OA and structural neuroimaging markers (hippocampal volume, entorhinal volume, ventricular volume, and volume of gray matter of the whole brain) among non-demented older people. We categorized our participants as those without OA (OA-) and those with OA (OA+). At baseline, we included 1,281 non-demented older adults, including 1,050 without OA and 231 with OA. Results: In the cross-sectional analysis, we did not observe any significant difference in structural neuroimaging markers between the two OA groups. In the longitudinal analysis, we found that compared to participants without OA, those with OA showed a steeper decline in volumes of the gray matter of the whole brain among non-demented older adults. Conclusions: OA was associated with a steeper decline in volumes of the gray matter of the whole brain over time among non-demented older people.

Keywords: MRI; dementia; longitudinal study; neuroimaging; osteoarthritis.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Wu, Wang, Ye and Liu.

Figures

Figure 1
Figure 1
Association of OA status with changes in cognition over time among non-demented older adults. The OA status was not associated with the change in ADAS-Cog 13 over time among non-demented older adults (coefficient = −0.13, p = 0.08). Abbreviations: OA, Osteoarthritis; ADAS-Cog 13, the 13-item Alzheimer’s Disease Assessment Scale-Cognitive subscale.
Figure 2
Figure 2
Association of OA status with changes in MRI markers over time among non-demented older adults. Panel (A) shows that OA status was not associated with the change in HVR. Panel (B) shows that compared with participants without OA, those with OA showed a significantly steeper decline in WVR. Panel (C) shows that OA status was not associated with a change in VVR. Panel (D) shows that OA status was not associated with the change in EVR. Abbreviations: OA, Osteoarthritis; HVR, Hippocampal volume ratio; WVR, Whole brain volume ratio; VVR, Ventricles volume ratio; EVR, Entorhinal volume ratio.

References

    1. Blondell S. J., Hammersley-Mather R., Veerman J. L. (2014). Does physical activity prevent cognitive decline and dementia?: a systematic review and meta-analysis of longitudinal studies. BMC Public Health 14:510. 10.1186/1471-2458-14-510
    1. Buchman A. S., Boyle P. A., Yu L., Shah R. C., Wilson R. S., Bennett D. A. (2012). Total daily physical activity and the risk of AD and cognitive decline in older adults. Neurology 78, 1323–1329. 10.1212/WNL.0b013e3182535d35
    1. Cardenas V. A., Chao L. L., Studholme C., Yaffe K., Miller B. L., Madison C., et al. . (2011). Brain atrophy associated with baseline and longitudinal measures of cognition. Neurobiol. Aging. 32, 572–580. 10.1016/j.neurobiolaging.2009.04.011
    1. Chen K. T., Chen Y. C., Fan Y. H., Lin W. X., Lin W. C., Wang Y. H., et al. . (2018). Rheumatic diseases are associated with a higher risk of dementia: a nation-wide, population-based, case-control study. Int. J. Rheum. Dis. 21, 373–380. 10.1111/1756-185X.13246
    1. Cunningham C., Campion S., Lunnon K., Murray C. L., Woods J. F., Deacon R. M., et al. . (2009). Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol. Psychiatry 65, 304–312. 10.1016/j.biopsych.2008.07.024
    1. Cunningham C., Wilcockson D. C., Boche D., Perry V. H. (2005). Comparison of inflammatory and acute-phase responses in the brain and peripheral organs of the ME7 model of prion disease. J. Virol. 79, 5174–5184. 10.1128/JVI.79.8.5174-5184.2005
    1. Erickson K. I., Leckie R. L., Weinstein A. M. (2014). Physical activity, fitness and gray matter volume. Neurobiol. Aging. 35, S20–S28. 10.1016/j.neurobiolaging.2014.03.034
    1. Folstein M. F., Folstein S. E., Mchugh P. R. (1975). "Mini-mental state". a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189–198. 10.1016/0022-3956(75)90026-6
    1. Fox N. C., Scahill R. I., Crum W. R., Rossor M. N. (1999). Correlation between rates of brain atrophy and cognitive decline in AD. Neurology 52, 1687–1689. 10.1212/wnl.52.8.1687
    1. Ghivizzani S. C., Kang R., Georgescu H. I., Lechman E. R., Jaffurs D., Engle J. M., et al. (1997). Constitutive intra-articular expression of human IL-1 beta following gene transfer to rabbit synovium produces all major pathologies of human rheumatoid arthritis. J. Immunol. 159, 3604–3612.
    1. Huang S.-W., Wang W.-T., Chou L.-C., Liao C.-D., Liou T.-H., Lin H.-W. (2015). Osteoarthritis increases the risk of dementia: a nationwide cohort study in taiwan. Sci. Rep. 5:10145. 10.1038/srep10145
    1. Hunter D. J., Bierma-Zeinstra S. (2019). Osteoarthritis. Lancet 393, 1745–1759. 10.1016/S0140-6736(19)30417-9
    1. Jack C. R., Jr, Bernstein M. A., Borowski B. J., Gunter J. L., Fox N. C., Thompson P. M., et al. (2010). Update on the magnetic resonance imaging core of the Alzheimer’s disease neuroimaging initiative. Alzheimers Dement. 6, 212–220. 10.1016/j.jalz.2010.03.004
    1. Jack C. R., Jr, Shiung M. M., Gunter J. L., O’brien P. C., Weigand S. D., Knopman D. S., et al. . (2004). Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology 62, 591–600. 10.1212/01.wnl.0000110315.26026.ef
    1. Josephs K. A., Whitwell J. L., Ahmed Z., Shiung M. M., Weigand S. D., Knopman D. S., et al. (2008). β-amyloid burden is not associated with rates of brain atrophy. Ann. Neurol. 63, 204–212. 10.1002/ana.21223
    1. Kyrkanides S., Tallents R. H., Jen-Nie H. M., Olschowka M. E., Johnson R., Yang M., et al. . (2011). Osteoarthritis accelerates and exacerbates Alzheimer’s disease pathology in mice. J. Neuroinflammation 8:112. 10.1186/1742-2094-8-112
    1. Lawlor K. E., Campbell I. K., O’donnell K., Wu L., Wicks I. P. (2001). Molecular and cellular mediators of interleukin-1-dependent acute inflammatory arthritis. Arthritis Rheum. 44, 442–450. 10.1002/1529-0131(200102)44:2<442::AID-ANR63>;2-M
    1. Mckhann G. M., Knopman D. S., Chertkow H., Hyman B. T., Jack C. R., Jr, Kawas C. H., et al. . (2011). The diagnosis of dementia due to Alzheimer’s disease: recommendations from the national institute on Aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement. 7, 263–269. 10.1016/j.jalz.2011.03.005
    1. Mohs R. C., Knopman D., Petersen R. C., Ferris S. H., Ernesto C., Grundman M., et al. . (1997). Development of cognitive instruments for use in clinical trials of antidementia drugs: additions to the Alzheimer’s disease assessment scale that broaden its scope. the Alzheimer’s disease cooperative study. Alzheimer Dis. Assoc. Disord. 11, S13–S21.
    1. Morris J. C. (1993). The clinical dementia rating (CDR): current version and scoring rules. Neurology 43, 2412–2414. 10.1212/wnl.43.11.2412-a
    1. Ridha B. H., Anderson V. M., Barnes J., Boyes R. G., Price S. L., Rossor M. N., et al. (2008). Volumetric MRI and cognitive measures in Alzheimer disease : comparison of markers of progression. J. Neurol. 255, 567–574. 10.1007/s00415-008-0750-9
    1. Schott J. M., Crutch S. J., Frost C., Warrington E. K., Rossor M. N., Fox N. C. (2008). Neuropsychological correlates of whole brain atrophy in Alzheimer’s disease. Neuropsychologia 46, 1732–1737. 10.1016/j.neuropsychologia.2008.02.015
    1. Sluimer J. D., Bouwman F. H., Vrenken H., Blankenstein M. A., Barkhof F., Van Der Flier W. M., et al. . (2010). Whole-brain atrophy rate and CSF biomarker levels in MCI and AD: a longitudinal study. Neurobiol. Aging. 31, 758–764. 10.1016/j.neurobiolaging.2008.06.016
    1. Sluimer J. D., Van Der Flier W. M., Karas G. B., Fox N. C., Scheltens P., Barkhof F., et al. . (2008). Whole-brain atrophy rate and cognitive decline: longitudinal MR study of memory clinic patients. Radiology 248, 590–598. 10.1148/radiol.2482070938
    1. Staite N. D., Richard K. A., Aspar D. G., Franz K. A., Galinet L. A., Dunn C. J. (1990). Induction of an acute erosive monarticular arthritis in mice by interleukin-1 and methylated bovine serum albumin. Arthritis Rheum. 33, 253–260. 10.1002/art.1780330215
    1. Sundermann E. E., Biegon A., Rubin L. H., Lipton R. B., Mowrey W., Landau S., et al. . (2016). Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy. Neurology 86, 1368–1376. 10.1212/WNL.0000000000002570
    1. Team R. C. (2013). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
    1. Weber A., Hung Mak S., Berenbaum F., Sellam J., Zheng Y.-P., Han Y., et al. . (2019). Association between osteoarthritis and increased risk of dementia: a systemic review and meta-analysis. Medicine (Baltimore) 98:e14355. 10.1097/MD.0000000000014355
    1. Weiner M. W., Veitch D. P., Aisen P. S., Beckett L. A., Cairns N. J., Cedarbaum J., et al. . (2015). 2014 Update of the Alzheimer’s disease neuroimaging initiative: a review of articles published since its inception. Alzheimers Dement. 11, e1–e120. 10.1016/j.jalz.2014.11.001

Source: PubMed

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