Abstract
Purpose
Olive oil polyphenols have been associated with cardiovascular health benefits. This study examined the antioxidant and anti-inflammatory effect of extra-virgin high polyphenol olive oil (HPOO) vs. low polyphenol olive oil (LPOO) in healthy Australian adults.
Methods
In a double-blind cross-over trial, 50 participants (aged 38.5 ± 13.9 years, 66% females) were randomized to consume 60 mL/day of HPOO (320 mg/kg polyphenols) or LPOO (86 mg/kg polyphenols) for three weeks. Following a 2-week wash-out period, participants crossed-over to the alternate treatment. Plasma oxidized low-density lipoprotein (ox-LDL), total antioxidant capacity (TAC), high-sensitivity C-reactive protein (hs-CRP) and anthropometrics were measured at baseline and follow-up.
Results
Fourty-three participants completed the study. Although there were no significant differences between treatments in the total sample, plasma ox-LDL decreased by 6.5 mU/mL (95%CI − 12.4 to − 0.5) and TAC increased by 0.03 mM (95% CI 0.006–0.05) only in the HPOO arm. Stratified analyses were also performed by cardiovascular disease risk status defined by abdominal obesity (WC > 94 cm in males, > 80 cm in females) or inflammation (hs-CRP > 1 mg/L). In the subgroup with abdominal obesity, ox-LDL decreased by 13.5 mU/mL (95% CI − 23.5 to − 3.6) and TAC increased by 0.04 mM (95% CI 0.006–0.07) only after HPOO consumption. In the subgroup with inflammation, hs-CRP decreased by 1.9 mg/L (95% CI − 3.7 to −0.1) only in the HPOO arm.
Conclusions
Although there were no significant differences between treatments, the changes observed after HPOO consumption demonstrate the antioxidant and anti-inflammatory effect of this oil, which is more pronounced in adults with high cardiometabolic risk (Clinical Trial Registration: ACTRN12618000706279).
References
Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017 (2018). Lancet 392 (10159):1736–1788. https://doi.org/10.1016/s0140-6736(18)32203-7
Australian Bureau of Statistics National Health Survey: First Results, 2017–18 http://www.abs.gov.au/ausstats/abs@.nsf/Lookup/4835.0.55.001main+features32007-08. Accessed 16 Dec 2019
Steven S, Frenis K, Oelze M, Kalinovic S, Kuntic M, Bayo Jimenez MT, Vujacic-Mirski K, Helmstädter J, Kröller-Schön S, Münzel T, Daiber A (2019) Vascular inflammation and oxidative stress: major triggers for cardiovascular disease. Oxid Med Cell Longev 2019:7092151. https://doi.org/10.1155/2019/7092151
Siti HN, Kamisah Y, Kamsiah J (2015) The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul Pharmacol 71:40–56. https://doi.org/10.1016/j.vph.2015.03.005
Fitó M, Cladellas M, de la Torre R, Martí J, Alcántara M, Pujadas-Bastardes M, Marrugat J, Bruguera J, López-Sabater MC, Vila J, Covas MI (2005) Antioxidant effect of virgin olive oil in patients with stable coronary heart disease: a randomized, crossover, controlled, clinical trial. Atherosclerosis 181(1):149–158. https://doi.org/10.1016/j.atherosclerosis.2004.12.036
Gao S, Zhao D, Wang M, Zhao F, Han X, Qi Y, Liu J (2017) Association between circulating oxidized LDL and atherosclerotic cardiovascular disease: a meta-analysis of observational studies. Can J Cardiol 33(12):1624–1632. https://doi.org/10.1016/j.cjca.2017.07.015
Ishigaki Y, Oka Y, Katagiri H (2009) Circulating oxidized LDL: a biomarker and a pathogenic factor. Curr Opin Lipidol 20(5):363–369. https://doi.org/10.1097/MOL.0b013e32832fa58d
Sies H (2007) Total antioxidant capacity: appraisal of a concept. J Nutr 137(6):1493–1495. https://doi.org/10.1093/jn/137.6.1493
Wang Y, Chun OK, Song WO (2013) Plasma and dietary antioxidant status as cardiovascular disease risk factors: a review of human studies. Nutrients 5(8):2969–3004. https://doi.org/10.3390/nu5082969
Collins C BT, Rollo M (2017) Dietary Patterns and Cardiovascular Disease Outcomes: an Evidence Check rapid review brokered by the Sax Institute for the National Heart Foundation of Australia. http://www.saxinstitute.org.au. Accessed 2 June 2020
Farràs M, Canyelles M, Fitó M, Escolà-Gil JC (2020) Effects of virgin olive oil and phenol-enriched virgin olive oils on lipoprotein atherogenicity. Nutrients. https://doi.org/10.3390/nu12030601
Sofi F, Abbate R, Gensini GF, Casini A (2010) Accruing evidence on benefits of adherence to the Mediterranean diet on health: an updated systematic review and meta-analysis. Am J Clin Nutr 92(5):1189–1196. https://doi.org/10.3945/ajcn.2010.29673
Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvado J, Ruiz-Gutierrez V, Covas MI, Fiol M, Gomez-Gracia E, Lopez-Sabater MC, Vinyoles E, Aros F, Conde M, Lahoz C, Lapetra J, Saez G, Ros E (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145(1):1–11. https://doi.org/10.7326/0003-4819-145-1-200607040-00004
Donini LM, Serra-Majem L, Bulló M, Gil Á, Salas-Salvadó J (2015) The Mediterranean diet: culture, health and science. Br J Nutr 113(Suppl 2):S1-3. https://doi.org/10.1017/s0007114515001087
Ghanbari R, Anwar F, Alkharfy KM, Gilani AH, Saari N (2012) Valuable nutrients and functional bioactives in different parts of olive (Olea europaea L.)-a review. Int J Mol Sci 13(3):3291–3340. https://doi.org/10.3390/ijms13033291
Sarapis K, Thomas CJ, Hoskin J, George ES, Marx W, Mayr HL, Kennedy G, Pipingas A, Willcox JC, Prendergast LA, Itsiopoulos C, Moschonis G (2020) The effect of high polyphenol extra virgin olive oil on blood pressure and arterial stiffness in healthy Australian adults: a randomized, controlled, cross-over study. Nutrients. https://doi.org/10.3390/nu12082272
George ES, Marshall S, Mayr HL, Trakman GL, Tatucu-Babet OA, Lassemillante AM, Bramley A, Reddy AJ, Forsyth A, Tierney AC, Thomas CJ, Itsiopoulos C, Marx W (2019) The effect of high-polyphenol extra virgin olive oil on cardiovascular risk factors: a systematic review and meta-analysis. Crit Rev Food Sci Nutr 59(17):2772–2795. https://doi.org/10.1080/10408398.2018.1470491
Souza PAL, Marcadenti A, Portal VL (2017) Effects of olive oil phenolic compounds on inflammation in the prevention and treatment of coronary artery disease. Nutrients. https://doi.org/10.3390/nu9101087
Castaner O, Fito M, Lopez-Sabater MC, Poulsen HE, Nyyssonen K, Schroder H, Salonen JT, De la Torre-Carbot K, Zunft HF, De la Torre R, Baumler H, Gaddi AV, Saez GT, Tomas M, Covas MI (2011) The effect of olive oil polyphenols on antibodies against oxidized LDL. A randomized clinical trial. Clin Nutr 30(4):490–493. https://doi.org/10.1016/j.clnu.2011.01.013
Hohmann CD, Cramer H, Michalsen A, Kessler C, Steckhan N, Choi K, Dobos G (2015) Effects of high phenolic olive oil on cardiovascular risk factors: a systematic review and meta-analysis. Phytomedicine 22(6):631–640. https://doi.org/10.1016/j.phymed.2015.03.019
Schwingshackl L, Krause M, Schmucker C, Hoffmann G, Rucker G, Meerpohl JJ (2019) Impact of different types of olive oil on cardiovascular risk factors: a systematic review and network meta-analysis. Nutr Metab Cardiovasc Dis 29(10):1030–1039. https://doi.org/10.1016/j.numecd.2019.07.001
Marx W, George ES, Mayr HL, Thomas CJ, Sarapis K, Moschonis G, Kennedy G, Pipingas A, Willcox JC, Prendergast LA, Itsiopoulos C (2019) Effect of high polyphenol extra virgin olive oil on markers of cardiovascular disease risk in healthy Australian adults (OLIVAUS): a protocol for a double-blind randomised, controlled, cross-over study. Nutr Diet. https://doi.org/10.1111/1747-0080.12531
Sarapis K, Thomas CJ, Shivantha S, George ES, Marx W, Mayr HL, Kennedy G, Pipingas A, Willcox JC, Prendergast LA, Drummond GR, Itsiopoulos C, Moschonis G The Effect of High Polyphenol Extra Virgin Olive Oil on Markers of Cardiovascular Disease Risk in Healthy Australian Adults (OLIVAUS): results from a double blind, randomised, controlled cross-over feasibility pilot study. In: Dietitians Association of Australia 36th National Conference, Gold Coast, QLD, Australia, 12–14 August 2019 2019.
Miró-Casas E, Farré Albaladejo M, Covas MI, Rodriguez JO, Menoyo Colomer E, Lamuela Raventós RM, de la Torre R (2001) Capillary gas chromatography-mass spectrometry quantitative determination of hydroxytyrosol and tyrosol in human urine after olive oil intake. Anal Biochem 294(1):63–72. https://doi.org/10.1006/abio.2001.5160
WHO (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO expert consultation. Geneva, World Health Organization
WHO Waist Circumference and Waist-Hip Ratio: Report of a WHO expert consultation Geneva, World Health Organization
Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC Jr, Taubert K, Tracy RP, Vinicor F (2003) Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 107(3):499–511. https://doi.org/10.1161/01.cir.0000052939.59093.45
Hernaez A, Fernandez-Castillejo S, Farras M, Catalan U, Subirana I, Montes R, Sola R, Munoz-Aguayo D, Gelabert-Gorgues A, Diaz-Gil O, Nyyssonen K, Zunft HJ, de la Torre R, Martin-Pelaez S, Pedret A, Remaley AT, Covas MI, Fito M (2014) Olive oil polyphenols enhance high-density lipoprotein function in humans: a randomized controlled trial. Arterioscler Thromb Vasc Biol 34(9):2115–2119. https://doi.org/10.1161/atvbaha.114.303374
Neveu V, Perez-Jiménez J, Vos F, Crespy V, du Chaffaut L, Mennen L, Knox C, Eisner R, Cruz J, Wishart D, Scalbert A (2010) Phenol-explorer: an online comprehensive database on polyphenol contents in foods. Database. https://doi.org/10.1093/database/bap024
Marrugat J, Covas MI, Fitó M, Schröder H, Miró-Casas E, Gimeno E, López-Sabater MC, de la Torre R, Farré M (2004) Effects of differing phenolic content in dietary olive oils on lipids and LDL oxidation–a randomized controlled trial. Eur J Nutr 43(3):140–147. https://doi.org/10.1007/s00394-004-0452-8
Hernáez Á, Remaley AT, Farràs M, Fernández-Castillejo S, Subirana I, Schröder H, Fernández-Mampel M, Muñoz-Aguayo D, Sampson M, Solà R, Farré M, de la Torre R, López-Sabater MC, Nyyssönen K, Zunft HJ, Covas MI, Fitó M (2015) Olive oil polyphenols decrease LDL concentrations and LDL atherogenicity in men in a randomized controlled trial. J Nutr 145(8):1692–1697. https://doi.org/10.3945/jn.115.211557
Moreno-Luna R, Munoz-Hernandez R, Miranda ML, Costa AF, Jimenez-Jimenez L, Vallejo-Vaz AJ, Muriana FJ, Villar J, Stiefel P (2012) Olive oil polyphenols decrease blood pressure and improve endothelial function in young women with mild hypertension. Am J Hypertens 25(12):1299–1304. https://doi.org/10.1038/ajh.2012.128
Tsartsou E, Proutsos N, Castanas E, Kampa M (2019) Network meta-analysis of metabolic effects of olive-oil in humans shows the importance of olive oil consumption with moderate polyphenol levels as part of the mediterranean diet. Front Nutr 6:6. https://doi.org/10.3389/fnut.2019.00006
Fitó M, Covas MI, Lamuela-Raventós RM, Vila J, Torrents L, de la Torre C, Marrugat J (2000) Protective effect of olive oil and its phenolic compounds against low density lipoprotein oxidation. Lipids 35(6):633–638. https://doi.org/10.1007/s11745-000-0567-1
Visioli F, Bellomo G, Montedoro G, Galli C (1995) Low density lipoprotein oxidation is inhibited in vitro by olive oil constituents. Atherosclerosis 117(1):25–32. https://doi.org/10.1016/0021-9150(95)05546-9
Covas MI, Fitó M, Lamuela-Raventós RM, Sebastiá N, de la Torre-Boronat C, Marrugat J (2000) Virgin olive oil phenolic compounds: binding to human low density lipoprotein (LDL) and effect on LDL oxidation. Int J Clin Pharmacol Res 20(3–4):49–54
Nojiri S, Daida H, Mokuno H, Iwama Y, Mae K, Ushio F, Ueki T (2001) Association of serum antioxidant capacity with coronary artery disease in middle-aged men. Jpn Heart J 42(6):677–690. https://doi.org/10.1536/jhj.42.677
Wang Y, Yang M, Lee SG, Davis CG, Kenny A, Koo SI, Chun OK (2012) Plasma total antioxidant capacity is associated with dietary intake and plasma level of antioxidants in postmenopausal women. J Nutr Biochem 23(12):1725–1731. https://doi.org/10.1016/j.jnutbio.2011.12.004
Oliveras-López M-J, Berná G, Jurado-Ruiz E, López-García de la Serrana H, Martín F (2014) Consumption of extra-virgin olive oil rich in phenolic compounds has beneficial antioxidant effects in healthy human adults. J Funct Foods 10:475–484. https://doi.org/10.1016/j.jff.2014.07.013
Visioli F, Caruso D, Grande S, Bosisio R, Villa M, Galli G, Sirtori C, Galli C (2005) Virgin Olive Oil Study (VOLOS): vasoprotective potential of extra virgin olive oil in mildly dyslipidemic patients. Eur J Nutr 44(2):121–127. https://doi.org/10.1007/s00394-004-0504-0
Wongwarawipat T, Papageorgiou N, Bertsias D, Siasos G, Tousoulis D (2018) Olive oil-related anti-inflammatory effects on atherosclerosis: potential clinical implications. Endocr Metab Immune Disord Drug Targets 18(1):51–62. https://doi.org/10.2174/1871530317666171116103618
Rosillo MA, Sánchez-Hidalgo M, Sánchez-Fidalgo S, Aparicio-Soto M, Villegas I, Alarcón-de-la-Lastra C (2016) Dietary extra-virgin olive oil prevents inflammatory response and cartilage matrix degradation in murine collagen-induced arthritis. Eur J Nutr 55(1):315–325. https://doi.org/10.1007/s00394-015-0850-0
Fitó M, Cladellas M, de la Torre R, Martí J, Muñoz D, Schröder H, Alcántara M, Pujadas-Bastardes M, Marrugat J, López-Sabater MC, Bruguera J, Covas MI, the members of the SI (2008) Anti-inflammatory effect of virgin olive oil in stable coronary disease patients: a randomized, crossover, controlled trial. Eur J Clin Nutr 62(4):570–574. https://doi.org/10.1038/sj.ejcn.1602724
Santangelo C, Filesi C, Varì R, Scazzocchio B, Filardi T, Fogliano V, D’Archivio M, Giovannini C, Lenzi A, Morano S, Masella R (2016) Consumption of extra-virgin olive oil rich in phenolic compounds improves metabolic control in patients with type 2 diabetes mellitus: a possible involvement of reduced levels of circulating visfatin. J Endocrinol Invest 39(11):1295–1301. https://doi.org/10.1007/s40618-016-0506-9
Acknowledgements
The quantitative immunoturbidimetric determination of hs-CRP in human serum was performed at PathWest laboratory (Fiona hospital, WA) under the coordination of Mr Ramon Lambert (Scientist in Charge). Laboratory analysis for TAC assay was conducted by AL, KP, OF and for ox-LDL assay by MG. The authors would like to acknowledge Professor Luke Prendergast who contributed in the original sample size calculation. The authors would also like to thank Professor Andrew Pipingas and Dr Gregory Kennedy who contributed in parts of the protocol related to blood pressure and measures of arterial stiffness. We would also like to acknowledge the work of Ms Johanna Hoskin (Honours student) who was involved in the data collection phase of the main study. Finally, we thank our participants for their cooperation.
Funding
This trial is supported by a seeding grant from the La Trobe University Understanding Disease Research Focus Area. Cobram Estate Pty. Ltd. has provided partial financial support and intervention EVOO for this trial. K.S., who conducted her PhD on this trial, has been supported by an Australian Government Research Training Program Scholarship.
Author information
Authors and Affiliations
Contributions
Conceptualization/study design, CI, ESG, and WM; investigation, KS; data curation, KS and GM; statistical analysis, KS, and GM; writing—original draft preparation, KS; review and editing, all authors; supervision, GM, CJT and CI; project administration, KS, ESG, JCW and WM; funding acquisition, CI, ESG, WM, HLM, and CJT All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. W.M. is currently funded by an Alfred Deakin Postdoctoral Research Fellowship and a Multiple Sclerosis Research Australia early-career fellowship. W.M. has previously received funding from the Cancer Council Queensland and university grants/fellowships from La Trobe University, Deakin University, University of Queensland, and Bond University, received industry funding and has attended events funded by Cobram Estate Pty. Ltd., received travel funding from Nutrition Society of Australia, received consultancy funding from Nutrition Research Australia, and has received speakers honoraria from the Cancer Council Queensland and the Princess Alexandra Research Foundation.
Ethics approval and consent to participate
This study was conducted according to the Guidelines for Good Clinical Practice (GCP), the guidelines laid down in the Declaration of Helsinki and the CONSORT reporting guidelines. All procedures involving human subjects were approved by the Human Research Ethics Committee of La Trobe University (HEC17-067) and written informed consent was obtained from all volunteers.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sarapis, K., George, E.S., Marx, W. et al. Extra virgin olive oil high in polyphenols improves antioxidant status in adults: a double-blind, randomized, controlled, cross-over study (OLIVAUS). Eur J Nutr 61, 1073–1086 (2022). https://doi.org/10.1007/s00394-021-02712-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-021-02712-y