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Effect of high-fat diet on cerebral pathological changes of cerebral small vessel disease in SHR/SP rats

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Abstract

Cerebral small vessel diseases (CSVD) are neurological disorders associated with microvessels, manifested pathologically as white matter (WM) changes and cortical microbleeds, with hypertension as a risk factor. Additionally, a high-fat diet (HFD) can affect peripheral vessel health. Our study explored how HFD affects cerebral small vessels in normotensive WKY, hypertensive SHR, and SHR/SP rats. The MRI results revealed that HFD specifically increased WM hyperintensity in SHR/SP rats. Pathologically, it increased WM pallor and vacuolation in SHR and SHR/SP rats. Levels of blood–brain barrier (BBB) protein claudin 5 were decreased in SHR and SHR/SP compared to WKY, with HFD having minimal impact on these levels. Conversely, collagen IV levels remained consistent among the rat strains, which were increased by HFD. Consequently, HFD caused vessel leakage in all rat strains, particularly within the corpus callosum of SHR/SP rats. To understand the underlying mechanisms, we assessed the levels of hypoxia-inducible factor-1α (HIF-1α), Gp91-phox, and neuroinflammatory markers astrocytes, and microglia were increased in SHR and SHR/SP compared to WKY and were further elevated by HFD in all rat strains. Gp91-phox was also increased in SHR and SHR/SP compared to WKY, with HFD causing an increase in WKY but little effect in SHR and SHR/SP. In conclusion, our study demonstrates that HFD, in combined with hypertension, intensifies cerebral pathological alterations in CSVD rats. This exacerbation involves increased oxidative stress and HIF-1α in cerebral vessels, triggering neuroinflammation, vascular basement membrane remodeling, IgG leakage, and ultimately WM damage.

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Data Availability

The data that support the findings of this study are available upon request from the authors.

References

  1. Chojdak-Łukasiewicz J, Dziadkowiak E, Zimny A, Paradowski B. Cerebral small vessel disease: A review. Adv Clin Exp Med. 2021;30(3):349–56. https://doi.org/10.17219/acem/131216.

    Article  PubMed  Google Scholar 

  2. Cuadrado-Godia E, Dwivedi P, Sharma S, Ois Santiago A, Roquer Gonzalez J, Balcells M, Laird J, Turk M, Suri HS, Nicolaides A, Saba L, Khanna NN, Suri JS. Cerebral Small Vessel Disease: A Review Focusing on Pathophysiology, Biomarkers, and Machine Learning Strategies. J Stroke. 2018;20(3):302–20. https://doi.org/10.5853/jos.2017.02922.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Li Q, Yang Y, Reis C, Tao T, Li W, Li X, Zhang JH. Cerebral Small Vessel Disease. Cell Transplant. 2018;27(12):1711–22. https://doi.org/10.1177/0963689718795148.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Lee WJ, Chou KH, Lee PL, Peng LN, Wang PN, Lin CP, Chen LK, Chung CP. Cerebral small vessel disease phenotype and 5-year mortality in asymptomatic middle-to-old aged individuals. Sci Rep. 2021;11(1):23149. https://doi.org/10.1038/s41598-021-02656-7.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rensma SP, van Sloten TT, Launer LJ, Stehouwer CDA. Cerebral small vessel disease and risk of incident stroke, dementia and depression, and all-cause mortality: A systematic review and meta-analysis. Neurosci Biobehav Rev. 2018;90:164–73. https://doi.org/10.1016/j.neubiorev.2018.04.00.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ihara M, Yamamoto Y. Emerging Evidence for Pathogenesis of Sporadic Cerebral Small Vessel Disease. Stroke. 2016;47(2):554–60. https://doi.org/10.1161/STROKEAHA.115.009627.

    Article  PubMed  Google Scholar 

  7. Heye AK, Thrippleton MJ, Chappell FM, Hernández Mdel C, Armitage PA, Makin SD, Maniega SM, Sakka E, Flatman PW, Dennis MS, Wardlaw JM. Blood pressure and sodium: Association with MRI markers in cerebral small vessel disease. J Cereb Blood Flow Metab. 2016;36(1):264–74. https://doi.org/10.1038/jcbfm.2015.64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wang Z, Chen Q, Chen J, Yang N, Zheng K. Risk factors of cerebral small vessel disease: A systematic review and meta-analysis. Medicine (Baltimore). 2021;100(51): e28229. https://doi.org/10.1097/MD.0000000000028229.

    Article  CAS  PubMed  Google Scholar 

  9. Inoue Y, Shue F, Bu G, Kanekiyo T. Pathophysiology and probable etiology of cerebral small vessel disease in vascular dementia and Alzheimer’s disease. Mol Neurodegener. 2023;18(1):46. https://doi.org/10.1186/s13024-023-00640-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Marini S, Anderson CD, Rosand J. Genetics of Cerebral Small Vessel Disease. Stroke. 2020;51(1):12–20. https://doi.org/10.1161/STROKEAHA.119.024151.

    Article  PubMed  Google Scholar 

  11. Bai T, Yu S, Feng J. Advances in the Role of Endothelial Cells in Cerebral Small Vessel Disease. Front Neurol. 2022;13: 861714. https://doi.org/10.3389/fneur.2022.861714.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rajeev V, Fann DY, Dinh QN, Kim HA, De Silva TM, Lai MKP, Chen CL, Drummond GR, Sobey CG, Arumugam TV. Pathophysiology of blood brain barrier dysfunction during chronic cerebral hypoperfusion in vascular cognitive impairment. Theranostics. 2022;12(4):1639–58. https://doi.org/10.7150/thno.68304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ohtsuki S, Yamaguchi H, Katsukura Y, Asashima T, Terasaki T. mRNA expression levels of tight junction protein genes in mouse brain capillary endothelial cells highly purified by magnetic cell sorting. J Neurochem. 2008;104(1):147–54. https://doi.org/10.1111/j.1471-4159.2007.05008.x.

    Article  CAS  PubMed  Google Scholar 

  14. Dearborn JL, Schneider AL, Sharrett AR, Mosley TH, Bezerra DC, Knopman DS, Selvin E, Jack CR, Coker LH, Alonso A, Wagenknecht LE, Windham BG, Gottesman RF. Obesity, Insulin Resistance, and Incident Small Vessel Disease on Magnetic Resonance Imaging: Atherosclerosis Risk in Communities Study. Stroke. 2015;46(11):3131–6. https://doi.org/10.1161/STROKEAHA.115.010060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tb M, G, T., A, G., D, A. Erratum to “Suffering from Cerebral Small Vessel Disease with and without Metabolic Syndrome.” Open Med (Wars). 2020;16(1):23. https://doi.org/10.1515/med-2021-0006.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Nassir CMNCM, Ghazali MM, Hashim S, Idris NS, Yuen LS, Hui WJ, Norman HH, Gau CH, Jayabalan N, Na Y, Feng L, Ong LK, Abdul Hamid H, Ahamed HN, Mustapha M. Diets and Cellular-Derived Microparticles: Weighing a Plausible Link With Cerebral Small Vessel Disease. Front Cardiovasc Med. 2021;8:632131. https://doi.org/10.3389/fcvm.2021.632131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chen YC, Lu BZ, Shu YC, Sun YT. Spatiotemporal Dynamics of Cerebral Vascular Permeability in Type 2 Diabetes-Related Cerebral Microangiopathy. Front Endocrinol (Lausanne). 2022;12: 805637. https://doi.org/10.3389/fendo.2021.805637.

    Article  PubMed  Google Scholar 

  18. Attuquayefio T, Stevenson RJ, Oaten MJ, Francis HM. A four-day Western-style dietary intervention causes reductions in hippocampal-dependent learning and memory and interoceptive sensitivity. PLoS ONE. 2017;12(2): e0172645. https://doi.org/10.1371/journal.pone.0172645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Clemente-Suárez VJ, Beltrán-Velasco AI, Redondo-Flórez L, Martín-Rodríguez A, Tornero-Aguilera JF. Global Impacts of Western Diet and Its Effects on Metabolism and Health: A Narrative Review. Nutrients. 2023;15(12):2749. https://doi.org/10.3390/nu15122749.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mustapha M, Nassir CMNCM, Aminuddin N, Safri AA, Ghazali MM. Cerebral Small Vessel Disease (CSVD) - Lessons From the Animal Models. Front Physiol. 2019;10:1317. https://doi.org/10.3389/fphys.2019.01317.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Olivera, S., Graham, D. Sex differences in preclinical models of hypertension. J Hum Hypertens, 2022. 1–7. https://doi.org/10.1038/s41371-022-00770-1

  22. Yamori Y, Horie R, Sato M, Ohta K. Proceedings: Prophylactic trials for stroke in stroke-prone SHR: effect of sex hormones. Jpn Heart J. 1976;17(3):404–6. https://doi.org/10.1536/ihj.17.404.

    Article  CAS  PubMed  Google Scholar 

  23. Tochinai R, Sekizawa S, Kobayashi I, Kuwahara HM. Autonomic nervous activity in rats can be evaluated by blood photoplethysmography-derived pulse rate variability analysis. Transl Regul Sci. 2021;3(1):17–21. https://doi.org/10.33611/trs.2021-001.

    Article  Google Scholar 

  24. Kuwahara M, Sugano S, Yayou K, Tsubone H, Kobayashi H. Evaluation of a new tail-cuff method for blood pressure measurements in rats with special reference to the effects of ambient temperature. Jikken Dobutsu. 1991;40(3):331–6. https://doi.org/10.1538/expanim1978.40.3_331.

    Article  CAS  PubMed  Google Scholar 

  25. Sasaki K, Yoshizaki F. Investigation into hippocampal nerve cell damage through the mineralocorticoid receptor in mice. Mol Med Rep. 2015;12(5):7211–20. https://doi.org/10.3892/mmr.2015.4406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Herisson F, Zhou I, Mawet J, Du E, Barfejani AH, Qin T, Cipolla MJ, Sun PZ, Rost NS, Ayata C. Posterior reversible encephalopathy syndrome in stroke-prone spontaneously hypertensive rats on high-salt diet. J Cereb Blood Flow Metab. 2019;39(7):1232–46. https://doi.org/10.1177/0271678X17752795.

    Article  CAS  PubMed  Google Scholar 

  27. Azad AK, Sheikh AM, Haque MA, Osago H, Sakai H, Shibly AZ, Yano S, Michikawa M, Hossain S, Tabassum S, Zhou AG, Zhang X, Nagai YA. Time-Dependent Analysis of Plasmalogens in the Hippocampus of an Alzheimer’s Disease Mouse Model: A Role of Ethanolamine Plasmalogen. Brain Sci. 2021;11(12):1603. https://doi.org/10.3390/brainsci11121603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Shibly AZ, Sheikh AM, Michikawa M, Tabassum S, Azad AK, Zhou X, Zhang Y, Yano S, Nagai A. Analysis of Cerebral Small Vessel Changes in AD Model Mice. Biomedicines. 2022;11(1):50. https://doi.org/10.3390/biomedicines11010050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Weiss HR, Buchweitz E, Murtha TJ, Auletta M. Quantitative regional determination of morphometric indices of the total and perfused capillary network in the rat brain. Circ Res. 1982;51(4):494–503. https://doi.org/10.1161/01.RES.51.4.494.

    Article  CAS  PubMed  Google Scholar 

  30. Saubaméa B, Cochois-Guégan V, Cisternino S, Scherrmann JM. Heterogeneity in the rat brain vasculature revealed by quantitative confocal analysis of endothelial barrier antigen and P-glycoprotein expression. J Cereb Blood Flow Metab. 2012;32(1):81–92. https://doi.org/10.1038/jcbfm.2011.109.

    Article  CAS  PubMed  Google Scholar 

  31. Lee SP, Duong TQ, Yang G, Iadecola C, Kim SG. Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: implications for BOLD fMRI. Magn Reson Med. 2001;45(5):791–800. https://doi.org/10.1002/mrm.1107.

    Article  CAS  PubMed  Google Scholar 

  32. Elabi OF, Cunha JPMCM, Gaceb A, Fex M, Paul G. High-fat diet-induced diabetes leads to vascular alterations, pericyte reduction, and perivascular depletion of microglia in a 6-OHDA toxin model of Parkinson disease. J Neuroinflammation. 2021;18(1):175. https://doi.org/10.1186/s12974-021-02218-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Tabitha Green. (2019). Shape-shifting Brain Cells. ASU - Ask A Biologist. Retrieved January 8, 2024 from https://askabiologist.asu.edu/plosable/shape-shifting-brain-cells.

  34. Arba F, Leigh R, Inzitari D, Warach SJ, Luby M, Lees KR. Blood–brain barrier leakage increases with small vessel disease in acute ischemic stroke. Neurol. 2017;89(21):2143–50. https://doi.org/10.1212/WNL.0000000000004677.

    Article  Google Scholar 

  35. Lai Y, Jiang C, Du X, Sang C, Guo X, Bai R, Tang R, Dong J, Ma C. Effect of intensive blood pressure control on the prevention of white matter hyperintensity: systematic review and meta-analysis of randomized trials. J Clin Hypertens (Greenwich). 2020;22(11):1968–73. https://doi.org/10.1111/jch.14030.

    Article  PubMed  Google Scholar 

  36. Giezendanner S, Fisler MS, Soravia LM, Andreotti J, Walther S, Wiest R, Dierks T, Federspiel A. Microstructure and cerebral blood flow within white matter of the human brain: a TBSS analysis. PLoS ONE. 2016;11(3): e0150657. https://doi.org/10.1371/journal.pone.0150657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ritz MF, Grond-Ginsbach C, Kloss M, Tolnay M, Fluri F, Bonati H, Traenka L, Zeis C, Schaeren-Wiemers T, Peters N, Engelter N, Engelter ST, Alexandre Lyrer P. Identification of inflammatory, metabolic, and cell survival pathways contributing to cerebral small vessel disease by postmortem gene expression microarray. Curr Neurovasc Res. 2016;13(1):58–67. https://doi.org/10.2174/1567202612666151027151025.

    Article  CAS  PubMed  Google Scholar 

  38. Murray ME, Vemuri P, Preboske GM, Murphy MC, Schweitzer KJ, Parisi JE, Jack CR Jr, Dickson DW. A quantitative postmortem MRI design sensitive to white matter hyperintensity differences and their relationship with underlying pathology. Neuropathol Exp Neurol. 2012;71(12):1113–22. https://doi.org/10.1097/NEN.0b013e318277387e.

    Article  Google Scholar 

  39. Ritz MF, Fluri F, Engelter ST, Schaeren-Wiemers N, Lyrer PA. Cortical and putamen age-related changes in the microvessel density and astrocyte deficiency in spontaneously hypertensive and stroke-prone spontaneously hypertensive rats. Curr Neurovasc Res. 2009;6(4):279–87. https://doi.org/10.2174/156720209789630311.

    Article  CAS  PubMed  Google Scholar 

  40. Li W, Prakash R, Kelly-Cobbs AI, Ogbi S, Kozak A, El-Remessy AB, Schreihofer DA, Fagan SC, Ergul A. Adaptive cerebral neovascularization in a model of type 2 diabetes: relevance to focal cerebral ischemia. Diabetes. 2010;59(1):228–35. https://doi.org/10.2337/db09-0902.

    Article  PubMed  Google Scholar 

  41. Prakash R, Johnson M, Fagan SC, Ergul A. Cerebral neovascularization and remodeling patterns in two different models of type 2 diabetes. PLoS ONE. 2013;8(2): e56264. https://doi.org/10.1371/journal.pone.0056264.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang, H., Xu, R., Wang, Z., Contribution of oxidative stress to HIF-1-mediated profibrotic changes during the kidney damage. Oxid Med Cell Longev. 2021, 6114132. https://doi.org/10.1155/2021/6114132

  43. Cao Y, Li Z, Li H, Ni C, Li L, Yang N, Shi C, Zhong Y, Cui D, Guo X. Hypoxia-inducible factor-1α is involved in isoflurane-induced blood-brain barrier disruption in aged rats model of POCD. Behav Brain Res. 2018;339:39–46. https://doi.org/10.1016/j.bbr.2017.09.004.

    Article  CAS  PubMed  Google Scholar 

  44. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci U S A. 2009;106(6):1977–82. https://doi.org/10.1073/pnas.080869810.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  45. Terashima J, Sampei S, Iidzuka M, Ohsakama A, Tachikawa C, Satoh J, Kudo K, Habano W, Ozawa S. VEGF expression is regulated by HIF-1α and ARNT in 3D KYSE-70, esophageal cancer cell spheroids. Cell Biol Int. 2016;40(11):1187–94. https://doi.org/10.1002/cbin.10656.

    Article  CAS  PubMed  Google Scholar 

  46. Barallobre-Barreiro J, Loeys B, Mayr M, Rienks M, Verstraeten A, Kovacic JC. Extracellular matrix in vascular disease, part 2/4: JACC Focus Seminar. J Am Coll Cardiol. 2020;75(17):2189–203. https://doi.org/10.1016/j.jacc.2020.03.018.

    Article  CAS  PubMed  Google Scholar 

  47. Martinez-Quinones P, McCarthy CG, Watts SW, Klee NS, Komic A, Calmasini FB, Priviero F, Warner A, Chenghao Y, Wenceslau CF. Hypertension induced morphological and physiological changes in cells of the arterial wall. Am J Hypertens. 2018;31(10):1067–78. https://doi.org/10.1093/ajh/hpy083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gilkes DM, Bajpai S, Chaturvedi P, Wirtz D, Semenza GL. Hypoxia-inducible factor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibroblasts. J Biol Chem. 2013;288(15):10819–29. https://doi.org/10.1074/jbc.M112.442939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Iglesias-de la Cruz MC, Ziyadeh FN, Isono M, Kouahou M, Han DC, Kalluri R, Mundel P, Chen S. Effects of high glucose and TGF-beta1 on the expression of collagen IV and vascular endothelial growth factor in mouse podocytes. Kidney Int. 2002;62(3):901–13. https://doi.org/10.1046/j.1523-1755.2002.00528.x.

    Article  CAS  PubMed  Google Scholar 

  50. Barrows IR, Ramezani A, Raj DS. Inflammation, immunity, and oxidative stress in hypertension-partners in crime? Adv Chronic Kidney Dis. 2019;26(2):122–30. https://doi.org/10.1053/j.ackd.2019.03.001.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Bruce-Keller AJ, White CL, Gupta S, Knight AG, Pistell PJ, Ingram DK, Morrison CD, Keller JN. NOX activity in brain aging: exacerbation by high fat diet. Free Radic Biol Med. 2010;49(1):22–30. https://doi.org/10.1016/j.freeradbiomed.2010.03.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2017;114(12):1752–61. https://doi.org/10.1172/JCI21625.

    Article  Google Scholar 

  53. Pepping JK, Vandanmagsar B, Fernandez-Kim SO, Zhang J, Mynatt RL, Bruce-Keller AJ. Myeloid-specific deletion of NOX2 prevents the metabolic and neurologic consequences of high fat diet. PLoS ONE. 2017;12(8): e0181500. https://doi.org/10.1371/journal.pone.0181500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to acknowledge the technical expertise of the Interdisciplinary Center for Science Research, Organization for Research and Academic Information, and Department of Experimental Animals, Interdisciplinary Center for Science Research, Shimane University. We would also like to thank Yasuko Wada, Abul Kalam Azad, Yuxin Liu, Xinlang Liu, and Pang Bo for their technical support during the experiments.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Neurology, Faculty of Medicine, Shimane University, 89-1 Enya-Cho, Izumo, 693-8501, Japan

    Yuchi Zhang, Kenichi Iwasa, Abu Zaffar Shibly, Xiaojing Zhou, Ruochen Wang, Jubo Bhuiya, Fatema Binte Abdullah, Yoshihito Aoki & Atsushi Nagai

  2. Department of Pharmacology, School of Basic Medical Sciences, Heilongjiang University of Chinese Medicine, Harbin, 150040, China

    Yuchi Zhang

  3. Department of Laboratory Medicine, Faculty of Medicine, Shimane University, Izumo, 693-8501, Japan

    Abdullah Md. Sheikh, Shatera Tabassum & Shozo Yano

  4. Department of Biotechnology and Genetic Engineering, Mawlana Bhashani Science and Technology University, Santosh, Tangail, 1902, Bangladesh

    Abu Zaffar Shibly

  5. Department of Neurology, Zhoushan Hospital, Zhoushan, 316004, China

    Xiaojing Zhou

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  1. Yuchi Zhang
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Contributions

Yuchi Zhang: Conceptualization, Data curation, Methodology, Writing – original draft. Abdullah Md. Sheikh: Conceptualization, Methodology, Writing – review & editing. Shatera Tabassum: Methodology, Supervision, Validation. Kenichi Iwasa: Supervision, Validation. Abu Zaffar Shibly: Methodology, Supervision. Xiaojing Zhou: Validation. Ruochen Wang: Validation. Jubo Bhuiya: Methodology, Validation. Abdullah Fatema Binte: Validation. Shozo Yano: Validation. Yoshihito Aoki: Validation. Atsushi Nagai: Conceptualization, Project administration, Supervision, Writing – review & editing. All authors provided critical feedback and contributed to the final manuscript.

Corresponding author

Correspondence to Atsushi Nagai.

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All animals were used according to the ARRIVE reporting guidelines (Animal Research: Reporting of In Vivo Experiments), and guidelines of the Institute of Experimental Animals of Shimane University. The experimental protocols and procedures were approved by the Ethical Committee of Shimane University (approval code: IZ2-96).

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Zhang, Y., Sheikh, A.M., Tabassum, S. et al. Effect of high-fat diet on cerebral pathological changes of cerebral small vessel disease in SHR/SP rats. GeroScience (2024). https://doi.org/10.1007/s11357-024-01074-7

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