P.
Lucci
*a,
M.
Borrero
b,
A.
Ruiz
c,
D.
Pacetti
d,
N. G.
Frega
d,
O.
Diez
e,
M.
Ojeda
b,
R.
Gagliardi
d,
L.
Parra
b and
M.
Angel
b
aDepartment of Food Science, University of Udine Via Sondrio 2/a, 33100 Udine, Italy. E-mail: paololucci2001@yahoo.it
bDepartment of Nutrition and Biochemistry, Faculty of Sciences, Pontificia Universidad Javeriana, KR 7 # 40-62, Bogota D.C., Colombia
cDepartment of Internal Medicine, School of Medicine, Pontificia Universidad Javeriana, KR 7 # 40-62, Bogota D.C., Colombia
dDepartment of Agricultural, Food, and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy
eDepartment of Microbiology, Faculty of Sciences, Pontificia Universidad Javeriana, KR 7 # 40-62, Bogota D.C., Colombia
First published on 8th October 2015
This study examines, for the first time, the effect of hybrid Elaeis oleifera × E. guineensis palm oil supplementation on human plasma lipids related to CVD risk factors. One hundred sixty eligible participants were randomized and assigned to one of the two treatments: 25 mL hybrid palm oil (HPO group) or 25 mL extra virgin olive oil (EVOO group) daily for 3 months. Fasting venous samples were obtained at baseline and after 1, 2 and 3 months for measurement of plasma lipids (TC, LDL-C, HDL-C and TAGs). Changes in body mass index and waist circumference were also assessed. Although there was an overall reduction in TC (7.4%, p < 0.001) and in LDL-C (15.6%, p < 0.001), no significant differences were found between the treatment groups in a repeated measures analysis of variance for TC (p = 0.0525), LDL-C (p = 0.2356), HDL-C (p = 0.8293) or TAGs (p = 0.3749). Furthermore, HPO consumption had similar effects on plasma lipids to EVOO, thus providing additional support for the concept that hybrid Elaeis oleifera × E. guineensis palm oil can be seen as a “tropical equivalent of olive oil”.
To date in Colombia more than 25000 hectares of oil palm interspecific hybrid Elaeis oleifera × E. guineensis has been planted. From an agronomic point of view, the good bud rot tolerance of the hybrids, compared to E. guineensis, justifies its use to replant severely decimated zones. However, the oil obtained from hybrid palm fruits may also have unexplored functional properties and health benefits, especially in reducing cardiovascular disease risk. In fact, in our recent study we fully characterized, for the first time, the composition and structure of triacylglycerols (TAGs) and partial glycerides of crude palm oil obtained from interspecific hybrid E. oleifera × E. guineensis grown in Colombia.11 The study revealed interesting nutritional properties of oils obtained from interspecific hybrid palm compared to the oils from African palm oil. Although only four fatty acid types (palmitic, C16:0; stearic C18:0; oleic C18:1; linolenic, C18:2) constituted more than 95% of the total fatty acids of both oils, the hybrid palm oil had a higher percentage of oleic acid (54.6 ± 1.0 vs. 41.4 ± 0.3) together with lower palmitic (28.3 ± 1.0 vs. 40.1 ± 0.1) and stearic (2.8 ± 0.3 vs. 5.0 ± 0.1) acids amounts. The percentage of the essential fatty acid, linoleic acid, does not differ significantly. Furthermore, the sn-2 position of TAGs in hybrid palm oil (HPO) was shown to be predominantly esterified with oleic acid with only 10–15% of the total palmitic acid and 6–20% of stearic acid acylated in the secondary position. These findings are very interesting, especially from a nutritional point of view since fatty acids in the sn-2 position of dietary triacylglycerols are preferentially absorbed through the intestinal wall. Therefore, our results demonstrate that a partial dietary replacement of saturated palmitic acid with monounsaturated oleic acid can be obtained by consuming crude HPO instead of African palm oil, without the need for any fractionation process to separate olein and stearin fractions because of HPO higher degrees of unsaturation. This also means that crude HPO could represent an extremely rich source of health-promoting minor components, since such bioactive compounds are not lost during the refining and fractionation processes required for African PO. Therefore, besides the interesting composition and structure of TAGs, HPO can also provide a substantial amount of antioxidants that might additionally contribute to lower the risk of developing CHD and certain cancers.12 In fact, our latest studies13,14 revealed that HPO unsaponifiable matter is characterized by a high content of tocotrienols (4.5 ± 1.4 mg of α-tocotrienol, 0.4 ± 0.1 β-tocotrienol, 14.8 ± 2.3 mg of γ-tocotrienol, 3.2 ± 0.4 mg of δ-tocotrienol per 100 g oil) with tocopherols, mainly entirely constituted of the α isomer, that accounted for 2.7 mg ± 0.7 per 100 g oil. These results highlight another interesting peculiarity of HPO, since tocotrienols are now well recognized for their superior antioxidant activity compared with tocopherols.
The aim of the present paper was to investigate, for the first time, the health benefits of hybrid palm oil consumption and its potential as a functional food oil for the prevention of CVD. In a randomized trial we compared the effects of supplementation with crude hybrid palm oil (E. oleifera × E. guineensis) and extra-virgin olive oil, which is universally recognized as putative anti-atherogenic and cardioprotective oil, on human plasma lipids related to cardiovascular disease risk.
The oil unsaponifiable matter was analysed according to the procedure described by Lucci et al.14
The extraction of the phenolic fraction from the oils was performed as reported by Montedoro et al.17 whereas the total phenolic content of the oils was determined according to the procedure reported by Loizzo et al.18 The results were expressed as gallic acid equivalents (mg per kg oil) based on the calibration curve (R2 = 0.996). The estimation of the total phenolic content was carried out in triplicate and the results were averaged.
The total fatty acid profile, the unsaponifiable matter composition and the total phenolic content of the oils are shown in Table 1. It is noteworthy that the amount of antioxidant compounds provided by HPO supplementation was similar to that provided by EVOO supplementation. In fact, the dose of EVOO (25 ml per day) corresponded to a daily intake of tocols and phenols of 4.5 and 38.5 mg per day, respectively. Similarly, the dose of HPO (25 ml per day) corresponded to a daily intake of tocols and phenols of 6.5 and 47.5 mg per day, respectively. Once again, it is important to mention that in HPO tocotrienols constitute ∼90% of the total tocols.
EVOO | HPO | |
---|---|---|
SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids; legend for fatty acids – m:n Δx, m = number of carbon atoms, n = number of double bonds, x = position of double bonds.a Tocols = sum of α-tocopherol, α-tocotrienol, β-tocotrienol, γ-tocotrienol and δ-tocotrienol contents. | ||
Fatty acids (%) | ||
C16:0 | 12.5 ± 0.8 | 27.9 ± 1.2 |
C16:1 | 0.9 ± 0.1 | 0.5 ± 0.1 |
C18:0 | 2.5 ± 0.4 | 2.9 ± 0.3 |
C18:1Δ9c | 76.0 ± 1.2 | 55.2 ± 1.3 |
C18:2Δ9c,12c | 5.5 ± 0.8 | 10.8 ± 0.5 |
C18:3Δ9c,12c,15c | 0.6 ± 0.1 | 0.4 ± 0.0 |
C20:0 | 0.4 ± 0.2 | 0.3 ± 0.1 |
C20:1Δ11 | 0.3 ± 0.1 | 0.4 ± 0.2 |
∑SFA | 15.4 ± 0.8 | 30.8 ± 1.6 |
∑MUFA | 77.2 ± 1.2 | 56.1 ± 1.0 |
∑PUFA | 6.1 ± 0.4 | 11.1 ± 0.7 |
Unsaponifiable components (mg per 100 g oil) | ||
Squalene | 321± 8.6 | 24.7 ± 0.3 |
Campesterol | 1.1 ± 0.4 | 9.8 ± 0.3 |
Stigmasterol | 2.9 ± 0.1 | 8.2 ± 1.0 |
β-Sitosterol | 127 ± 11.4 | 39.1 ± 3.3 |
Δ5-Avenasterol | 21.3 ± 2.8 | 1.7 ± 0.2 |
n-Alkanols | 13.2 ± 1.4 | 6.2 ± 1.7 |
4-Methylsterols | 20.7 ± 2.1 | 1.3 ± 0.2 |
4,4-Dimethylsterols | 135.6 ± 9.5 | 7.4 ± 1.2 |
Tocolsa | 18.1 ± 1.5 | 25.9 ± 4.8 |
Total phenolic content (ppm) | ||
154 ± 4.6 | 190 ± 2.5 |
Variable | Baseline population | EVOO (n = 82) | HPO (n = 78) | EVOO vs. HPO (p value) |
---|---|---|---|---|
Sample sizes in parenthesis, S.D. = standard deviation. EVOO = extra-virgin olive oil; HPO = hybrid palm oil; Significance (P < 0.05). | ||||
Age in years – mean (S.D.) | 63.5 (7.2) | 62.8 (6.1) | 64.3 (8.5) | 0.3591 |
Gender (% male) | 13 (8.1%) | 6 (7.4%) | 7 (8.9%) | 0.0710 |
Body mass index – mean (S.D.) | 28.3 (3.8) | 28.1 (3.7) | 28.5 (3.8) | 0.4148 |
Waist perimeter – mean (S.D.) | 87.9 (9.1) | 87.2 (8.8) | 88.6 (9.4) | 0.3405 |
Hypercholesterolemia (%) | 56 (35.2%) | 26 (32.1%) | 30 (38.4%) | 0.3738 |
Hypertriglyceridemia (%) | 70 (43.8%) | 43 (53.0%) | 27 (34.6%) | 0.5802 |
Cholesterol Total – mean (S.D.) | 205.1 (37.9) | 203.8 (36.9) | 206.5 (39.1) | 0.6429 |
Cholesterol, HDL – mean (S.D.) | 44.9 (12.4) | 43.5 (10.4) | 46.3 (14.2) | 0.1689 |
Cholesterol, LDL – mean (S.D.) | 120.4 (38.2) | 116.9 (38.1) | 124.0 (38.1) | 0.2464 |
Triglycerides – mean (S.D.) | 218.4 (128) | 242.0 (155.6) | 194.9 (85.7) | 0.0698 |
As we can see from Table 3, there were final differences for all fractions, although significant only in the univariate analysis (considering only the treatment effect and not the interactions) for TC and for LDL-C levels (baseline vs. Visit 3).
Variable | Baselinea | Visit 1 | Visit 2 | Visit 3 | Baseline vs. Visit 3 (p valuec) | p valued | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
EVOO (n = 82) | HPO (n = 78) | EVOO (n = 81) | HPO (n = 73) | EVOO (n = 76) | HPO (n = 73) | EVOO (n = 77) | HPO (n = 68) | EVOO | HPO | ||
Sample sizes in parenthesis; data are expressed as mean (standard deviation). EVOO = extra-virgin olive oil; HPO = hybrid palm oil; NA = not assessed.a Number of participants who were receiving stable doses of statin across the study: EVOO (n = 37), HPO (n = 39).b Number of participants for whom LDL-C levels were measured by enzymatic colorimetric methods because of TAG levels higher than 400 mg/dL: baseline [EVOO (n = 14), HPO (n = 7)]; Visit 1 [EVOO (n = 15), HPO (n = 7)]; Visit 2 [EVOO (n = 14), HPO (n = 6)]; Visit 3 [EVOO (n = 13), HPO (n = 7)].c p value for univariate analysis [considering only the treatment effect and not interactions; significance (p < 0.05) = ○; significance (p < 0.01) = ●].d p value for multivariate analysis [considering interactions among visits and treatment; significance (p < 0.05)]. | |||||||||||
Body mass index | 28.1 (3.7) | 28.5 (3.8) | NA | NA | NA | NA | 27.7 (4.1) | 28.3 (3.3) | — | — | 0.2185 |
Cholesterol Total | 203.8 (36.9) | 206.5 (39.1) | 217.2 (35.4) | 213.2 (33.1) | 201.9 (35.3) | 212.5 (34.2) | 185.8 (28.4) | 193.9 (31.5) | ● | ○ | 0.0525 |
Cholesterol, HDL | 43.5 (10.4) | 46.3 (14.2) | 50.11 (14.1) | 50.3 (16.6) | 44.3 (17.5) | 45.1 (14.4) | 43.2 (16.6) | 44.3 (17.9) | — | — | 0.8293 |
Cholesterol, LDLb | 116.9 (38.1) | 124.0 (38.1) | 161.1 (38.2) | 161.2 (34.7) | 119.4 (36.6) | 132.3 (36.1) | 95.7 (33.8) | 107.2 (36.4) | ● | ○ | 0.2356 |
Triglycerides | 242.0 (155.6) | 194.9 (85.7) | 222.1 (111.4) | 185.5 (83.3) | 224.4 (110.5) | 200.6 (87.8) | 245.4 (122.9) | 210.8 (136.5) | — | — | 0.3749 |
Total:HDL cholesterol | 4.97 (1.89) | 4.71 (1.20) | 4.61 (1.31) | 4.61 (1.56) | 5.09 (1.75) | 5.22 (1.99) | 5.34 (2.98) | 5.36 (2.48) | — | — | 0.4031 |
LDL:HDL cholesterol | 2.91 (1.63) | 2.84 (1.06) | 3.48 (1.37) | 3.58 (1.59) | 3.58 (1.59) | 3.11 (1.53) | 2.93 (2.22) | 3.18 (2.87) | — | — | 0.5344 |
In general, there was an initial rise, for both treatments, in TC, LDL-C and HDL-C levels, followed by reduction for both groups (Fig. 2). These results are confirmed by the changes observed throughout the experiment in the overall population (Table 4). A possible explanation for this finding is that in the case of insulin and leptin resistance, monounsaturated oil supplementation increases the liver fat content, which may cause an increased release of lipids from the liver to prevent fatty liver development.19 As a result, a temporary increase in serum lipids could be observed.
Fig. 2 Changes in plasma lipid levels in both groups throughout the experiment. (A) TC levels; (B) LDL-C levels; (C) HDL-C levels; (D) TAG levels. |
TC | LDL-C | HDL-C | TAGs | |||||
---|---|---|---|---|---|---|---|---|
Change (mg dL−1) | 95% Conf. Int. | Change (mg dL−1) | 95% Conf. Int. | Change (mg dL−1) | 95% Conf. Int. | Change (mg dL−1) | 95% Conf. Int. | |
Visit 1 | 9.99 | 3.96 to 16.01 | 40.67 | 33.94 to 47.39 | 5.24 | 2.21 to 8.28 | −14.31 | −29.18 to 0.55 |
Visit 2 | 1.94 | −4.14 to 8.03 | 5.55 | −1.23 to 12.35 | −0.11 | −3.17 to 2.95 | −7.87 | −22.91 to 7.17 |
Visit 3 | −15.08 | −21.94 to −8.94 | −18.68 | −25.53 to −11.83 | −1.07 | −4.16 to 2.01 | 9.19 | −5.98 to 24.37 |
In the HPO group, the initial level of TAGs (194.9 ± 85.7 mg dL−1) remained relatively unchanged with a final 3-month concentration of 210.8 ± 136.4 mg dL−1. The same trend has been observed in the EVOO group with TAG values of 242.0 ± 155.6 mg dL−1 and 245.4 ± 122.9 mg dL−1 at baseline and month 3, respectively. In subjects who received HPO, the HDL-C concentration increased by 6.1% at month 1, followed by a decrease gradually leading to the final value (3-month) of 44.3 ± 17.9 mg dL−1 (Table 3; Fig. 2C). A similar pattern was observed in the EVOO group with plasma HDL-C levels of 43.5 ± 10.4 mg dL−1 and 43.2 ± 16.6 mg dL−1, respectively, at the beginning and the end of the study. After 1 month of HPO supplementation, plasma LDL-C concentration was higher than at baseline (124.0 ± 38.1 mg dL−1 compared with 161.2 ± 34.7 mg dL−1). At month 2, however, LDL-C decreased to 132.3 ± 36.1 mg dL−1, and this trend continued over the next month reaching a final 3-month value of 107.2 ± 36.4 mg dL−1 (Fig. 2B). Therefore, during the study period, LDL-C concentration in patients receiving HPO decreased 13.3%. Furthermore, it should be stressed that reduction in LDL-C of HPO subjects was similar to that observed in the patients who received EVOO. In fact, the EVOO group showed a decrease in LDL-C from 116.9 ± 38.1 mg dL−1 at baseline to 95.7 ± 33.8 mg dL−1 at the end of the study. In HPO patients, plasma TC concentrations decreased from baseline (206.5 ± 39.1 mg dL−1) to month 3 (193.9 ± 31.5 mg dL−1), a reduction of 6.3%. Again, as with LDL-C, a small increase of the TC level was observed at both month 1 and month 2: the TC level was 206.5 ± 39.1 mg dL−1 at baseline, increased to 213.2 ± 33.1 mg dL−1 at month 1 and to 212.5 ± 34.2 mg dL−1 at month 2, then decreased to 193.9 ± 31.5 mg dL−1 by month 3 (Fig. 2A). The plasma levels of TC in the EVOO group also showed a reduction over the study period. However, in contrast to the LDL-C results, the reduction in TC was more pronounced in subjects who received EVOO. In fact, plasma levels of TC increased at month 1 (217.2 ± 35.4 mg dL−1) followed by a decline at the second and third assessment times (201.9 ± 35.3 and 185.8 ± 28.4), an overall reduction of approximately 9%. With regard to the TC/HDL-C and LDL-C/HDL-C ratios, used as predictors of ischemic heart disease risk,20 only a small but not significant change has been observed. The TC/HDL-C ratio increased from 4.71 to 5.36 over the study period (from 4.97 to 5.34 in the EVOO group) and a small effect has also been detected for the LDL-C/HDL-C ratio (2.84 baseline vs. 3.18 month 3) (Table 3). In the same way, the triglycerides to HDL-cholesterol ratio (TG/HDL-c), which has been proven to be strongly correlated with the plasma level of small, dense LDL atherogenic particles (phenotype B), showed little increase from 4.20 to 4.75 and from 5.56 to 5.68 for the HPO and EVOO groups, respectively.
No significant differences were observed for BMI between baseline and month 3 in both groups (Table 3). There were significant changes in all fractions when time was considered (across visits) for TC (p < 0.001), LDL-C (p < 0.001), HDL-C (p < 0.0005) and TAGs (p = 0.0191), independent of the treatment received (Table 5).
TC | LDL-C | HDL-C | TAGs | |
---|---|---|---|---|
ANOVA analysis of repeated measures: significance (p < 0.05). | ||||
Treatment | 0.2898 | 0.0993 | 0.5466 | 0.043 |
Visit | <0.001 | <0.0001 | <0.0005 | 0.0191 |
Interaction (between treatment and visit) | 0.0525 | 0.2356 | 0.8293 | 0.3749 |
On the other hand, no statistically significant differences were found between the two groups for TAGs (p = 0.043), TC (p = 0.2898), LDL-C (p = 0.0993) or HDL-C (p = 0.5466). Finally, the repeated measures ANOVA shows that no differences were detected between the two treatment groups for TC (p = 0.0525), LDL-C (p = 0.2356), HDL-C (p = 0.8293) or TAGs (p = 0.3749), once the interaction between treatment and time (visits) was taken into account (Tables 3 and 5).
But the observed “positive” effects of HPO consumption may also be associated with the intake of antioxidants contained in crude HPO. As stated before, consistent evidence now suggests that vitamin E, carotenoids and other antioxidant nutrients such as phenolic compounds also offer protection against CVD by decreasing oxidative damage. Thus, nutritional properties of edible oil depend not only on its glyceridic oil composition and structure but also on its potential as a source of health-promoting minor components. In fact, oxidation of LDL-C leads to a change in the lipoprotein conformation by which LDL cholesterol can better enter into the monocyte–macrophage system of the arterial wall and promote the atherosclerotic process. As mentioned previously, no previous studies have been undertaken to determine the health effects of HPO consumption. Studies reported in the literature are almost exclusively focused on refined palm oil fractions and based on the use of animal models. To our knowledge, our study constitutes the first human intervention trial with crude hybrid palm oil. It is certainly true that the effects of refined African palm olein on human plasma lipids and lipoproteins have been relatively well investigated in the past.30–34 However, palm olein, which is the liquid fraction obtained by fractionation of palm oil after crystallization at controlled temperatures, completely loses nutritionally important components such as carotenes, tocopherols and polyphenols. For instance, tocotrienol-enriched fraction from palm oil has been shown to decrease TC and LDL-C plasma levels.35 The favorable effect of crude HPO consumption on plasma lipids can therefore also be attributed to its high content of polyphenols (190 ppm) and tocols (>25 mg per 100 g) (Table 1), as well as by its high carotenoid concentration (>1038 mg per 100 g)13 which may play a crucial role by improving plasma antioxidant defenses and lipid profiles. In fact, because of the greater degree of unsaturation of HPO compared to African palm oil, HPO can be directly consumed without the need for any fractionation or refining process to separate olein and stearin fractions.
Our positive findings of crude HPO on plasma lipids are also consistent with previous animal model studies focused on a different kind of mildly refined palm oil called “red palm olein” (RPO) which suggested favorable cardiovascular effects of the oil. Contrary to palm olein, more than 80% of the vitamin E and 75% of carotenoids present in crude palm oil is retained in red palm olein. For instance, Boon et al.36 recently reported changes in serum lipid profiles of red palm olein treated hypertensive rats, with a significant reduction in LDL-cholesterol level and TC/HDL ratio (atherogenic index) compared to the untreated ones. Szucs et al.37 recently investigated the effects of dietary RPO supplementation in a cholesterol-enriched diet-induced hyperlipidemic rat model showing attenuation of the increased susceptibility of the hearts in cholesterol fed rats to ischaemia/reperfusion injury. RPO-supplementation also altered the pre-ischaemic levels of matrix metalloproteinase-2 (MMP2), thus indicating that myocardial MMP2 may be implicated as a possible role player in RPO mediated protection against ischaemia/reperfusion injury in the hearts of cholesterol supplemented rats. Previously, Esterhuyse et al.38 also suggested that dietary RPO-supplementation can improve reperfusion aortic output through mechanisms that may include activation of the NO-cGMP and inhibition of the cAMP pathway.
Finally, the results obtained in this study provide additional support for the concept that hybrid Elaeis oleifera × E. guineensis palm oil can be seen as the “tropical equivalent of olive oil”.
Footnote |
† Electronic supplementary information (ESI) available. See DOI: 10.1039/c5fo01083g |
This journal is © The Royal Society of Chemistry 2016 |