Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial
Mild cognitive impairment (MCI) and early Alzheimer’s disease (AD) are characterized by blood–brain barrier (BBB) breakdown leading to abnormal BBB permeability ahead of brain atrophy or dementia. Previous findings in AD mouse models have reported the beneficial effect of extra-virgin olive oil (EVO...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-12-01
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| Series: | Nutrients |
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| Online Access: | https://www.mdpi.com/2072-6643/14/23/5102 |
| _version_ | 1797462453811937280 |
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| author | Amal Kaddoumi Thomas S. Denney Gopikrishna Deshpande Jennifer L. Robinson Ronald J. Beyers David T. Redden Domenico Praticò Tassos C. Kyriakides Bonian Lu Anna N. Kirby Darren T. Beck Nancy D. Merner |
| author_facet | Amal Kaddoumi Thomas S. Denney Gopikrishna Deshpande Jennifer L. Robinson Ronald J. Beyers David T. Redden Domenico Praticò Tassos C. Kyriakides Bonian Lu Anna N. Kirby Darren T. Beck Nancy D. Merner |
| author_sort | Amal Kaddoumi |
| collection | DOAJ |
| description | Mild cognitive impairment (MCI) and early Alzheimer’s disease (AD) are characterized by blood–brain barrier (BBB) breakdown leading to abnormal BBB permeability ahead of brain atrophy or dementia. Previous findings in AD mouse models have reported the beneficial effect of extra-virgin olive oil (EVOO) against AD, which improved BBB and memory functions and reduced brain amyloid-β (Aβ) and related pathology. This work aimed to translate these preclinical findings to humans in individuals with MCI. We examined the effect of daily consumption of refined olive oil (ROO) and EVOO for 6 months in MCI subjects on BBB permeability (assessed by contrast-enhanced MRI), and brain function (assessed using functional-MRI) as the primary outcomes. Cognitive function and AD blood biomarkers were also assessed as the secondary outcomes. Twenty-six participants with MCI were randomized with 25 participants completed the study. EVOO significantly improved clinical dementia rating (CDR) and behavioral scores. EVOO also reduced BBB permeability and enhanced functional connectivity. While ROO consumption did not alter BBB permeability or brain connectivity, it improved CDR scores and increased functional brain activation to a memory task in cortical regions involved in perception and cognition. Moreover, EVOO and ROO significantly reduced blood Aβ<sub>42</sub>/Aβ<sub>40</sub> and p-tau/t-tau ratios, suggesting that both altered the processing and clearance of Aβ. In conclusion, EVOO and ROO improved CDR and behavioral scores; only EVOO enhanced brain connectivity and reduced BBB permeability, suggesting EVOO biophenols contributed to such an effect. This proof-of-concept study justifies further clinical trials to assess olive oil’s protective effects against AD and its potential role in preventing MCI conversion to AD and related dementias. |
| first_indexed | 2024-03-09T17:36:50Z |
| format | Article |
| id | doaj.art-6577c2e7e3b34fbdb513df2fafe488d9 |
| institution | Directory Open Access Journal |
| issn | 2072-6643 |
| language | English |
| last_indexed | 2024-03-09T17:36:50Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Nutrients |
| spelling | doaj.art-6577c2e7e3b34fbdb513df2fafe488d92023-11-24T11:52:15ZengMDPI AGNutrients2072-66432022-12-011423510210.3390/nu14235102Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled TrialAmal Kaddoumi0Thomas S. Denney1Gopikrishna Deshpande2Jennifer L. Robinson3Ronald J. Beyers4David T. Redden5Domenico Praticò6Tassos C. Kyriakides7Bonian Lu8Anna N. Kirby9Darren T. Beck10Nancy D. Merner11Department of Drug Discovery and Development, Harrison College of Pharmacy, Auburn University, Auburn, AL 36849, USACenter for Neuroscience, Auburn University, Auburn, AL 36849, USACenter for Neuroscience, Auburn University, Auburn, AL 36849, USACenter for Neuroscience, Auburn University, Auburn, AL 36849, USAAuburn University MRI Research Center, Department of Electrical & Computer Engineering, Auburn University, Auburn, AL 36849, USABiomedical Affairs and Research, Edward Via College of Osteopathic Medicine, Auburn University, Auburn, AL 36849, USAAlzheimer’s Center at Temple, Lewis Katz School of Medicine Temple University, Philadelphia, PA 19140, USAYale School of Public Health, New Haven, CT 06510, USAAuburn University MRI Research Center, Department of Electrical & Computer Engineering, Auburn University, Auburn, AL 36849, USADepartment of Cell Biology and Physiology and Preventive Medicine and Public Health, Edward Via College of Osteopathic Medicine, Auburn University, Auburn, AL 36849, USADepartment of Cell Biology and Physiology, Via College of Osteopathic Medicine, Auburn University, Auburn, AL 36849, USADepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USAMild cognitive impairment (MCI) and early Alzheimer’s disease (AD) are characterized by blood–brain barrier (BBB) breakdown leading to abnormal BBB permeability ahead of brain atrophy or dementia. Previous findings in AD mouse models have reported the beneficial effect of extra-virgin olive oil (EVOO) against AD, which improved BBB and memory functions and reduced brain amyloid-β (Aβ) and related pathology. This work aimed to translate these preclinical findings to humans in individuals with MCI. We examined the effect of daily consumption of refined olive oil (ROO) and EVOO for 6 months in MCI subjects on BBB permeability (assessed by contrast-enhanced MRI), and brain function (assessed using functional-MRI) as the primary outcomes. Cognitive function and AD blood biomarkers were also assessed as the secondary outcomes. Twenty-six participants with MCI were randomized with 25 participants completed the study. EVOO significantly improved clinical dementia rating (CDR) and behavioral scores. EVOO also reduced BBB permeability and enhanced functional connectivity. While ROO consumption did not alter BBB permeability or brain connectivity, it improved CDR scores and increased functional brain activation to a memory task in cortical regions involved in perception and cognition. Moreover, EVOO and ROO significantly reduced blood Aβ<sub>42</sub>/Aβ<sub>40</sub> and p-tau/t-tau ratios, suggesting that both altered the processing and clearance of Aβ. In conclusion, EVOO and ROO improved CDR and behavioral scores; only EVOO enhanced brain connectivity and reduced BBB permeability, suggesting EVOO biophenols contributed to such an effect. This proof-of-concept study justifies further clinical trials to assess olive oil’s protective effects against AD and its potential role in preventing MCI conversion to AD and related dementias.https://www.mdpi.com/2072-6643/14/23/5102Alzheimer’s diseasemild cognitive impairmentblood–brain barriercontrast-enhanced MRIfunctional MRIextra-virgin olive oil |
| spellingShingle | Amal Kaddoumi Thomas S. Denney Gopikrishna Deshpande Jennifer L. Robinson Ronald J. Beyers David T. Redden Domenico Praticò Tassos C. Kyriakides Bonian Lu Anna N. Kirby Darren T. Beck Nancy D. Merner Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial Nutrients Alzheimer’s disease mild cognitive impairment blood–brain barrier contrast-enhanced MRI functional MRI extra-virgin olive oil |
| title | Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial |
| title_full | Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial |
| title_fullStr | Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial |
| title_full_unstemmed | Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial |
| title_short | Extra-Virgin Olive Oil Enhances the Blood–Brain Barrier Function in Mild Cognitive Impairment: A Randomized Controlled Trial |
| title_sort | extra virgin olive oil enhances the blood brain barrier function in mild cognitive impairment a randomized controlled trial |
| topic | Alzheimer’s disease mild cognitive impairment blood–brain barrier contrast-enhanced MRI functional MRI extra-virgin olive oil |
| url | https://www.mdpi.com/2072-6643/14/23/5102 |
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