Cardio-metabolic and Immunological Impacts of Extra Virgin Olive Oil Consumption in Overweight and Obese Older Adults

A Randomized Controlled Trial

Mitra Rozati; Junaidah Barnett; Dayong Wu; Garry Handelman; Edward Saltzman; Thomas Wilson; Lijun Li; Junpeng Wang; Ascensión Marcos; José M. Ordovás; Yu-Chi Lee; Mohsen Meydani; Simin Nikbin Meydani

Disclosures

Nutr Metab. 2015;12(28) 

In This Article

Discussion

To our knowledge, our study is the first comprehensive one to determine the impact of substituting extra virgin olive oil for the cooking oils used in a typical American diet on cardio-metabolic and immunological outcomes in overweight and obese older adults, a population at higher risk for infectious and non-infectious chronic diseases. We showed that consumption of extra virgin olive oil for 3 months reduced blood pressure, tended to increase plasma HDL-C levels, and improved T cell proliferation. Further, participants in both groups with the highest change in plasma oleic acid showed higher increase in IL-2 production. There was no effect on other blood lipids, glucose, and inflammatory mediators.

In agreement with the previous studies,[35,56–59] we observed a blood pressure-lowering effect of EVOO consumption. However, our observation is particularly important because the participants, obese and older adults, are at higher risk compared to lean younger adults for developing cardiovascular disease. Furthermore, since lower blood pressure is a predictor of survival and freedom from physical and cognitive impairment,[60] both of which increase with age, our results support the notion that consumption of EVOO may have the potential to extend health span and curb development of age-related diseases.

We observed a trend toward increased blood concentrations of HDL-C after olive oil consumption, which supports the earlier reports of a beneficial effect of olive oil on blood lipid profiles by Marrugat et al.[61] The less pronounced effect observed in our study compared to theirs might be related to the difference in administering olive oil between the two studies. Throughout their study, subjects were provided with a daily dose of 25 mL of raw virgin olive oil and were directed to replace all other cooking fats with refined olive oil. In our study, EVOO was provided to the subjects to use as they wished (reflecting their actual lifestyle); therefore, they might have consumed less uncooked olive oil. Given that heating EVOO might destroy some of its active phenolic compounds,[62,63] it is possible that subjects in Marrugat's study consumed more uncooked virgin olive oil, and thus, higher levels of phenolic compounds, which might have resulted in a more profound effect on their plasma HDL-C levels.

Limited information is available about the impact of olive oil on immune and inflammatory responses, and no studies have used outcome variables as specific and comprehensive as those in our current study or in any study of overweight and obese older adults. For example, a study by Yaqoob et al. showed no effect on T cell proliferation in healthy middle-aged men (45–64 y, BMI 21.9–30.7) after they consumed only refined olive oil for 8 weeks.[37] This is in contrast to our observation that extra virgin olive oil consumption resulted in a modest improvement in T cell proliferation as well as an association between an increased production of T cell cytokine IL-2 and the magnitude of increase in plasma oleic acid. The difference between our findings and those of Yaqoob et al.[37] might be related to the fact that the participants in our study were 65 y or older, while the age range in their study was 45–64 y. It is reasonable to assume that T cell function in the participants of our study might have been less vigorous due to our subjects' more advanced ages compared to those in the study by Yaqoob et al.,[37] possibly explaining the discrepancy between the results of the two studies. This speculation is also supported by the observation that a study conducted in patients with rheumatoid arthritis, who are known to have reduced T cell-mediated function,[64,65] showed that olive oil increased T-lymphocyte proliferation in peripheral blood mononuclear cells (PBMC).[38] Additionally, in our study, we used EVOO, which has a higher content of phenolic compounds and might have caused a different effect compared to the refined olive oil used in the study by Yaqoob et al.[37] Furthermore, the duration of the two studies differed--our study was 12-weeks, their study was 8-weeks. This variation may have also contributed to the difference in findings between the two studies.

To determine the mechanism of olive oil-induced enhancement in anti-CD3/anti-CD28-induced T cell proliferation, we evaluated the production of IL-2, the key cytokine involved in the activation of T cells. When assessing the entire group, we found no difference in IL-2 production between the two study groups; however, since the range of change in plasma oleic acid in the subjects who consumed olive oil (−3.84 % to 7.32 %) and control oil (−5.14 % to 3.15 %) was large, we explored the relationship between quintiles of change in IL-2 production and those in plasma oleic acid in all subjects. Participants with the largest change in plasma oleic acid levels, i.e., those in quintile 5, showed a highly significant increase in IL-2 production compared to those with the lowest change in plasma oleic acid levels, i.e., those in quintile 1. These data suggest that the increase in T cell proliferation might be partly due to an oleic acid-induced increase in IL-2 production. However, further investigation is needed to confirm this finding. Furthermore, our data indicate that the olive oil-induced enhancement in T cell proliferation is not due to changes in blood composition of lymphocytes or T cell profiles as we did not find any difference in the percent of lymphocytes or T cell phenotype profiles between the two groups after 3 months.

It is noteworthy that the effect of olive oil on T cell proliferation in our study may be stimulation-specific because enhanced T cell proliferation was found when anti-CD3/anti-CD28 Abs (TCR activation together with co-stimulation), but not when T cell mitogen Con A, was used to activate T cells. Although mechanisms of signaling pathways were not the subject of our current study, this finding implies that specific signaling pathways or lipid/protein microenvironment involved in T cell receptor activation and co-stimulation-induced T cell activation might be influenced by olive oil.

In contrast to a moderate effect on T cell proliferation, olive oil consumption showed no effect on DTH skin test, an in vivo marker for recall antigen-specific cell-mediated immunity. Given that both groups showed an increase in total diameter of induration, it is possible that the boosting effect of repeated administration of the skin test might have masked any additional effect of olive oil.

There are some limitations to this study. First, since participants were given oil/spread for ad libitum use in their cooking at home, which allowed them to share with their families, it was difficult to determine the exact amount they themselves actually consumed even though their average use was measured using a 3DDR. Second, for those who used the oil for frying, only some of the oil absorbed by the food was expected to be ingested. The plasma fatty acid analysis reflected this situation since it showed a moderate 2 % increase with a wide range (−3.84 % to 7.32 %) in plasma oleic acid levels after 3 months in the olive oil group compared to the control group.

Nevertheless, based on significant changes in plasma oleic acid as well as the information recorded by 3DDR, both groups (OO and CON) were compliant to the treatments. We are aware that measuring blood levels of phenolic compounds present in olive oil could have enhanced compliance validation and data interpretation. However, in the current study, the participants used the oils at home at different times, thus a pre-determined time between olive oil consumption and blood collection could not be tightly controlled. Given that these phenolic compounds are metabolized over time after absorption, it would be unreliable to use random blood sample to assess phenolic compounds following olive oil consumption.[66]

In conclusion, our findings suggest that substituting EVOO for oils used in a typical American diet may have both cardio-metabolic and immunologic health benefits as indicated by reduced systolic blood pressure, a strong trend toward increased plasma HDL-C, and a moderate enhancing effect on T cell-mediated function. However, our results do not support an anti-inflammatory effect of EVOO in obese older adults. Given the increased risk of high blood pressure and a decline in T cell-mediated function in older adults, particularly those who are overweight and obese, our results suggest that overweight and obese older adults might benefit from substituting the oils used in their typical American diet with extra virgin olive oil.

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