Hormonal factors moderate the associations between vascular risk factors and white matter hyperintensities

Springer Science and Business Media LLC - Tập 17 - Trang 172-184 - 2022
Abdullah Alqarni1,2, Wei Wen1,3, Ben C. P. Lam1, John D. Crawford1, Perminder S. Sachdev1,3, Jiyang Jiang1
1Centre for Healthy Brain Ageing (CHeBA), Discipline of Psychiatry and Mental Health, Faculty of Medicine, University of New South Wales, Sydney, Australia
2Radiology and Medical Imaging Department, College of Applied Medical Sciences, Prince Sattam bin Abdulaziz University, Al-Kharj, Saudi Arabia
3Neuropsychiatric Institute, Prince of Wales Hospital, Randwick, Australia

Tóm tắt

To examine the moderation effects of hormonal factors on the associations between vascular risk factors and white matter hyperintensities in men and women, separately. White matter hyperintensities were automatically segmented and quantified in the UK Biobank dataset (N = 18,294). Generalised linear models were applied to examine (1) the main effects of vascular and hormonal factors on white matter hyperintensities, and (2) the moderation effects of hormonal factors on the relationship between vascular risk factors and white matter hyperintensities volumes. In men with testosterone levels one standard deviation higher than the mean value, smoking was associated with 27.8% higher white matter hyperintensities volumes in the whole brain. In women with a shorter post-menopause duration (one standard deviation below the mean), diabetes and higher pulse wave velocity were associated with 28.8% and 2.0% more deep white matter hyperintensities, respectively. These findings highlighted the importance of considering hormonal risk factors in the prevention and management of white matter hyperintensities.

Tài liệu tham khảo

Aiken, L. S., West, S. G., & Reno, R. R. (1991). Multiple regression: testing and interpreting interactions. Sage. Alfaro-Almagro, F., Jenkinson, M., Bangerter, N. K., Andersson, J. L. R., Griffanti, L., Douaud, G., & Smith, S. M. (2018). Image processing and quality control for the first 10,000 brain imaging datasets from UK Biobank. NeuroImage, 166, 400–424. https://doi.org/10.1016/j.neuroimage.2017.10.034 Alqarni, A., Jiang, J., Crawford, J. D., Koch, F., Brodaty, H., Sachdev, P., & Wen, W. (2021). Sex differences in risk factors for white matter hyperintensities in non-demented older individuals. Neurobiology of Aging, 98, 197–204. https://doi.org/10.1016/j.neurobiolaging.2020.11.001 Armstrong, N. J., Mather, K. A., Sargurupremraj, M., Knol, M. J., Malik, R., Satizabal, C. L., & Nyquist, P. A. (2020). Common genetic variation indicates separate causes for periventricular and deep white matter hyperintensities. Stroke, 51(7), 2111–2121. https://doi.org/10.1161/STROKEAHA.119.027544 Assareh, A. A., Mather, K. A., Crawford, J. D., Wen, W., Anstey, K. J., Easteal, S., & Sachdev, P. S. (2014). Renin-angiotensin system genetic polymorphisms and brain white matter lesions in older Australians. American Journal of Hypertension, 27(9), 1191–1198. https://doi.org/10.1093/ajh/hpu035 Caughey, M. C., Qiao, Y., Meyer, M. L., Palta, P., Matsushita, K., Tanaka, H., & Heiss, G. (2021). Relationship between central artery stiffness, brain arterial dilation, and white matter hyperintensities in older adults: the ARIC study-brief report. Arteriosclerosis Thrombosis and Vascular Biology, 41(6), 2109–2116. https://doi.org/10.1161/ATVBAHA.120.315692 Cook, I. A., Morgan, M. L., Dunkin, J. J., David, S., Witte, E., Lufkin, R., & Leuchter, A. F. (2002). Estrogen replacement therapy is associated with less progression of subclinical structural brain disease in normal elderly women: a pilot study. International Journal of Geriatric Psychiatry, 17(7), 610–618. https://doi.org/10.1002/gps.644 de Kat, A. C., Dam, V., Onland-Moret, N. C., Eijkemans, M. J. C., Broekmans, F. J. M., & van der Schouw, Y. T. (2017). Unraveling the associations of age and menopause with cardiovascular risk factors in a large population-based study. BMC Medicine, 15(1), 2. https://doi.org/10.1186/s12916-016-0762-8 de Leeuw, F. E., de Groot, J. C., Achten, E., Oudkerk, M., Ramos, L. M., Heijboer, R., & Breteler, M. M. (2001). Prevalence of cerebral white matter lesions in elderly people: a population based magnetic resonance imaging study. The Rotterdam scan study. Journal of Neurology, Neurosurgery and Psychiatry, 70(1), 9–14. https://doi.org/10.1136/jnnp.70.1.9 DeCarli, C., Massaro, J., Harvey, D., Hald, J., Tullberg, M., Au, R., & Wolf, P. A. (2005). Measures of brain morphology and infarction in the framingham heart study: establishing what is normal. Neurobiology of Aging, 26(4), 491–510. https://doi.org/10.1016/j.neurobiolaging.2004.05.004 DuPont, J. J., Kenney, R. M., Patel, A. R., & Jaffe, I. Z. (2019). Sex differences in mechanisms of arterial stiffness. British Journal of Pharmacology, 176(21), 4208–4225. https://doi.org/10.1111/bph.14624 Espeland, M. A., Hayden, K. M., Lockhart, S. N., Yassine, H. N., Hoscheidt, S., & Yasar, S., … Group, f. t. A. f. H. i. D. B. M. R. I. R. (2019). Sex-related differences in brain volumes and cerebral blood flow among overweight and obese adults with type 2 diabetes: Exploratory analyses from the action for health in diabetes brain magnetic resonance imaging study. The Journals of Gerontology: Series A, 75(4),771–778. https://doi.org/10.1093/gerona/glz090 Fatemi, F., Kantarci, K., Graff-Radford, J., Preboske, G. M., Weigand, S. D., Przybelski, S. A., & Vemuri, P. (2018). Sex differences in cerebrovascular pathologies on FLAIR in cognitively unimpaired elderly. Neurology, 90(6), e466–e473. https://doi.org/10.1212/wnl.0000000000004913 Filomena, J., Riba-Llena, I., Vinyoles, E., Tovar, J. L., Mundet, X., Castane, X., … Delgado, P. (2015). Short-term blood pressure variability relates to the presence of subclinical brain small vessel disease in primary hypertension. Hypertension, 66(3), 634–640; discussion 445. https://doi.org/10.1161/hypertensionaha.115.05440 Garnier-Crussard, A., Bougacha, S., Wirth, M., André, C., Delarue, M., Landeau, B., & Chételat, G. (2020). White matter hyperintensities across the adult lifespan: relation to age, Aβ load, and cognition. Alzheimer’s Research & Therapy, 12(1), 127. https://doi.org/10.1186/s13195-020-00669-4 Geerlings, M. I., Appelman, A. P., Vincken, K. L., Algra, A., Witkamp, T. D., Mali, W. P., & van der Graaf, Y. (2010). Brain volumes and cerebrovascular lesions on MRI in patients with atherosclerotic disease. The SMART-MR study. Atherosclerosis, 210(1), 130–136. https://doi.org/10.1016/j.atherosclerosis.2009.10.039 Griffanti, L., Jenkinson, M., Suri, S., Zsoldos, E., Mahmood, A., Filippini, N., & Zamboni, G. (2018). Classification and characterization of periventricular and deep white matter hyperintensities on MRI: a study in older adults. NeuroImage, 170, 174–181. https://doi.org/10.1016/j.neuroimage.2017.03.024 Gurol, M. E., Biessels, G. J., & Polimeni, J. R. (2020). Advanced neuroimaging to unravel mechanisms of cerebral small vessel diseases. Stroke, 51(1), 29–37. https://doi.org/10.1161/STROKEAHA.119.024149 Habes, M., Sotiras, A., Erus, G., Toledo, J. B., Janowitz, D., Wolk, D. A., & Davatzikos, C. (2018). White matter lesions. Neurology, 91(10), e964. https://doi.org/10.1212/WNL.0000000000006116 Jiang, J., Liu, T., Zhu, W., Koncz, R., Liu, H., Lee, T., & Wen, W. (2018). UBO detector - A cluster-based, fully automated pipeline for extracting white matter hyperintensities. NeuroImage, 174, 539–549. https://doi.org/10.1016/j.neuroimage.2018.03.050 Jongen, C., van der Grond, J., Kappelle, L. J., Biessels, G. J., Viergever, M. A., Pluim, J. P. W., on behalf of the Utrecht Diabetic Encephalopathy Study. (2007). Automated measurement of brain and white matter lesion volume in type 2 diabetes mellitus. Diabetologia, 50(7), 1509–1516. https://doi.org/10.1007/s00125-007-0688-y Kim, K. W., MacFall, J. R., & Payne, M. E. (2008). Classification of white matter lesions on magnetic resonance imaging in elderly persons. Biological Psychiatry, 64(4), 273–280. https://doi.org/10.1016/j.biopsych.2008.03.024 Kling, J. M., Miller, V. M., Tosakulwong, N., Lesnick, T., & Kantarci, K. (2020). Associations of pituitary-ovarian hormones and white matter hyperintensities in recently menopausal women using hormone therapy. Menopause (New York, N.Y.), 27(8). https://journals.lww.com/menopausejournal/Fulltext/2020/08000/Associations_of_pituitary_ovarian_hormones_and.7.aspx Lampe, L., Zhang, R., Beyer, F., Huhn, S., Kharabian Masouleh, S., Preusser, S., & Witte, A. V. (2019). Visceral obesity relates to deep white matter hyperintensities via inflammation. Annals of Neurology, 85(2), 194–203. https://doi.org/10.1002/ana.25396 Liu, Y. Y., Hu, L., Ji, C., Chen, D. W., Shen, X., Yang, N., & Zuo, P. P. (2009). Effects of hormone replacement therapy on magnetic resonance imaging of brain parenchyma hyperintensities in postmenopausal women. Acta Pharmacologica Sinica, 30(7), 1065–1070. https://doi.org/10.1038/aps.2009.81 Low, L. F., Anstey, K. J., Maller, J., Kumar, R., Wen, W., Lux, O., & Sachdev, P. (2006). Hormone replacement therapy, brain volumes and white matter in postmenopausal women aged 60–64 years. NeuroReport, 17(1), 101–104. https://doi.org/10.1097/01.wnr.0000194385.10622.8e Maas, A. H. E. M. (2021). Hormone therapy and cardiovascular disease: benefits and harms. Best Practice & Research Clinical Endocrinology & Metabolism, 35(6), 101576. https://doi.org/10.1016/j.beem.2021.101576 Madika, A. L., MacDonald, C. J., Fournier, A., Mounier-Vehier, C., Béraud, G., & Boutron-Ruault, M. C. (2021). Menopausal hormone therapy and risk of incident hypertension: role of the route of estrogen administration and progestogens in the E3N cohort. Menopause (New York, N.Y.), 28(11). https://journals.lww.com/menopausejournal/Fulltext/2021/11000/Menopausal_hormone_therapy_and_risk_of_incident.3.aspx Miller, K. L., Alfaro-Almagro, F., Bangerter, N. K., Thomas, D. L., Yacoub, E., Xu, J., & Smith, S. M. (2016). Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nature Neuroscience, 19(11), 1523–1536. https://doi.org/10.1038/nn.4393 Miller, V. M., Garovic, V. D., Kantarci, K., Barnes, J. N., Jayachandran, M., Mielke, M. M., & Rocca, W. A. (2013). Sex-specific risk of cardiovascular disease and cognitive decline: pregnancy and menopause. Biology of Sex Differences, 4(1), 6–6. https://doi.org/10.1186/2042-6410-4-6 Miller, V. M., Jayachandran, M., Barnes, J. N., Mielke, M. M., Kantarci, K., & Rocca, W. A. (2020). Risk factors of neurovascular ageing in women. Journal of Neuroendocrinology, 32(1), e12777. https://doi.org/10.1111/jne.12777 Moscufo, N., Wolfson, L., Meier, D., Liguori, M., Hildenbrand, P. G., Wakefield, D., & Guttmann, C. R. G. (2012). Mobility decline in the elderly relates to lesion accrual in the splenium of the corpus callosum. Age, 34(2), 405–414. https://doi.org/10.1007/s11357-011-9242-4 Mounier-Vehier, C., Angoulvant, T., Boivin, J. M., & Plu-Bureau, G. (2019). [Hypertension and menopausal hormone therapy]. Presse Medicale (Paris, France: 1983), 48(11 Pt 1), 1295–1300. https://doi.org/10.1016/j.lpm.2019.09.027 Nyquist, P. A., Bilgel, M., Gottesman, R., Yanek, L. R., Moy, T. F., Becker, L. C., & Vaidya, D. (2015). Age differences in periventricular and deep white matter lesions. Neurobiology of Aging, 36(4), 1653–1658. https://doi.org/10.1016/j.neurobiolaging.2015.01.005 Persyn, E., Hanscombe, K. B., Howson, J. M. M., Lewis, C. M., Traylor, M., & Markus, H. S. (2020). Genome-wide association study of MRI markers of cerebral small vessel disease in 42,310 participants. Nature Communications, 11(1), 2175. https://doi.org/10.1038/s41467-020-15932-3 Raffield, L. M., Cox, A. J., Freedman, B. I., Hugenschmidt, C. E., Hsu, F. C., Wagner, B. C., & Bowden, D. W. (2016). Analysis of the relationships between type 2 diabetes status, glycemic control, and neuroimaging measures in the diabetes heart study mind. Acta Diabetologica, 53(3), 439–447. https://doi.org/10.1007/s00592-015-0815-z Rossi, R., Grimaldi, T., Origliani, G., Fantini, G., Coppi, F., & Modena, M. G. (2002). Menopause and cardiovascular risk. Pathophysiology of Haemostasis and Thrombosis, 32(5–6), 325–328. https://doi.org/10.1159/000073591 Sachdev, P., Parslow, R., Salonikas, C., Lux, O., Wen, W., Kumar, R., & Jorm, A. (2004). Homocysteine and the brain in midadult life: evidence for an increased risk of leukoaraiosis in men. JAMA Neurology, 61(9), 1369–1376. https://doi.org/10.1001/archneur.61.9.1369 Sachdev, P. S., Parslow, R., Wen, W., Anstey, K. J., & Easteal, S. (2009). Sex differences in the causes and consequences of white matter hyperintensities. Neurobiology of Aging, 30(6), 946–956. https://doi.org/10.1016/j.neurobiolaging.2007.08.023 Schmidt, R., Fazekas, F., Reinhart, B., Kapeller, P., Fazekas, G., Offenbacher, H., & Freidl, W. (1996). Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. Journal of the American Geriatrics Society, 44(11), 1307–1313. https://doi.org/10.1111/j.1532-5415.1996.tb01400.x Schmidt, R., Schmidt, H., Haybaeck, J., Loitfelder, M., Weis, S., Cavalieri, M., & Jellinger, K. (2011). Heterogeneity in age-related white matter changes. Acta Neuropathologica, 122(2), 171–185. https://doi.org/10.1007/s00401-011-0851-x Srinath, R., Gottesman, R. F., Golden, H., Carson, S., & Dobs, A. (2016). Association between endogenous testosterone and cerebrovascular disease in the ARIC study (atherosclerosis risk in communities). Stroke, 47(11), 2682–2688. https://doi.org/10.1161/strokeaha.116.014088 Thurston, R. C., Aizenstein, H. J., Derby, C. A., Sejdić, E., & Maki, P. M. (2016). Menopausal hot flashes and white matter hyperintensities. Menopause (New York, N.Y.), 23(1), 27–32. https://doi.org/10.1097/GME.0000000000000481 van den Heuvel, D. M., Admiraal-Behloul, F., ten Dam, V. H., Olofsen, H., Bollen, E. L., Murray, H. M., & van Buchem, M. A. (2004). Different progression rates for deep white matter hyperintensities in elderly men and women. Neurology, 63(9), 1699–1701. https://doi.org/10.1212/01.wnl.0000143058.40388.44 Veldsman, M., Kindalova, P., Husain, M., Kosmidis, I., & Nichols, T. E. (2020). Spatial distribution and cognitive impact of cerebrovascular risk-related white matter hyperintensities. NeuroImage: Clinical, 28, 102405. https://doi.org/10.1016/j.nicl.2020.102405 Wardlaw, J. M., Hernandez, V., & Munoz-Maniega, S. (2015). What are white matter hyperintensities made of? Relevance to vascular cognitive impairment. Journal of the American Heart Association, 4(6), 001140. https://doi.org/10.1161/jaha.114.001140 Wharton, S. B., Simpson, J. E., Brayne, C., & Ince, P. G. (2015). Age-associated white matter lesions: the MRC cognitive function and ageing study. Brain Pathology, 25(1), 35–43. https://doi.org/10.1111/bpa.12219 Yin, Z. G., Li, L., Cui, M., Zhou, S. M., Yu, M. M., & Zhou, H. D. (2014). Inverse relationship between apolipoprotein A-I and cerebral white matter lesions: a cross-sectional study in middle-aged and elderly subjects. PLoS One, 9(5), e97113–e97113. https://doi.org/10.1371/journal.pone.0097113 Yin, Z. G., Wang, Q. S., Yu, K., Wang, W. W., Lin, H., & Yang, Z. H. (2018). Sex differences in associations between blood lipids and cerebral small vessel disease. Nutrition, Metabolism, and Cardiovascular Diseases: NMCD, 28(1), 28–34. https://doi.org/10.1016/j.numecd.2017.10.001