Hindawi Publishing Corporation

Oxidative Medicine and Cellular Longevity

Volume 2017, Article ID 8361493, 13 pages

https://doi.org/10.1155/2017/8361493

 

Research Article

A Chilean Berry Concentrate Protects against Postprandial Oxidative Stress and Increases Plasma Antioxidant Activity in Healthy Humans 

Ines Urquiaga,1 Felipe Ávila,1,2 Guadalupe Echeverria,1 Druso Perez,1 Sebastian Trejo,1 and Federico Leighton1 

 

1Center for Molecular Nutrition and Chronic Diseases, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile

2Escuela de Nutrición y Dietética, Facultad de Ciencias de la Salud, Universidad de Talca, 3460000 Talca, Chile 

Correspondence should be addressed to Ines Urquiaga; iurquiaga@bio.puc.cl

Copyright © 2017 Ines Urquiaga et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

Abstract

This study formulated and characterized an antioxidant-rich concentrate of berries (BPC-350) produced in Chile, which was used to perform a crossover study aimed at determining the effect of the berries on the modulation of plasma postprandial oxidative stress and antioxidant status. Healthy male volunteers (𝑁 = 11) were randomly assigned to three experimental meals: (1) 250 g of ground turkey burger (GTB) + 500mL of water; (2) 250 g of GTB + 500mL of 5% BPC-350; (3) 250 g of GTB prepared with 6% BPC-350 + 500mL of 5% BPC-350. Venous blood samples were collected prior to meal intake and every hour for six hours after intake. Malondialdehyde (MDA), carbonyls in proteins, and DPPH (2,2-diphenyl-1-picrylhydrazyl) antioxidant capacity were quantified in plasma. Significant differences indicated that BPC-350 decreases MDA plasma concentration and protein carbonyls (𝑝 < 0.05). Additionally, a significant increase in the DPPH antioxidant capacity was observed in Meals 2 and 3 when compared to Meal 1 (𝑝 < 0.05). The results are discussed in terms of oxidative reactions that occur during digestion at the stomach level and the important effect of oxidative reactions that occur during the thermal processing of red meat.

PMID: 28243359

 

Supplement: 

Polyphenols widely present in foods such as fruits, vegetables, and red wine have been proposed as key molecules associated with the beneficial effects of a Mediterranean diet. Considerable evidence has demonstrated that foodstuffs or extracts with a high content of these biomolecules can induce protective effects against oxidative stress and inflammation in dietary intervention and postprandial studies in humans . Oxidative stress has been closely associated with the pathogenesis of numerous chronic diseases as well as metabolic syndrome. After a high fat meal increases plasma postprandial concentrations of oxidative stress markers, such as malondialdehyde (MDA), lipid peroxides, protein carbonylation, and hydrogen peroxide.

The postprandial oxidative response to eating depends on several factors including the chemical nature of the macronutrient intake, the unsaturation degree of dietary fatty acids, the lipid intake dose, phytonutrient quantity, gender, smoking habits, and race, among others. This information underscores the importance of developing functional foods aimed at effectively reducing levels to the postprandial state.

Polyphenols present in red wine and roasted ground coffee effectively protect against postprandial oxidative stress, decreasing plasma concentrations of MDA after red meat cutlet intake. This effect has been explained by the ability of polyphenols to prevent oxidative reactions occurring during digestion primarily at the stomach level, where an acidic environment can enhance lipid peroxidation reactions.

Native Chilean berries possess high antioxidant activity and, among 120 species and varieties studied, native berries such as maqui (Aristotelia chilensis), murta (Ugni molinae), and calafate (Berberis microphylla) displayed the highest Oxygen Radical Absorbance Capacity (ORAC) antioxidant activities. In human endothelial cell cultures, the addition of maqui, blackberry, or strawberry juice significantly protects cells from hydrogen peroxide-induced intracellular oxidative stress, with maqui and blackberry inhibiting more effectively than strawberry. In addition to the in vitro antioxidant capacities, intracellular antioxidant responses are activated by berry polyphenols, including Chilean wild raspberries (Rubus geoides Sm.), which induced an increase in the intracellular glutathione content.

In this sense, this work aimed to elaborate a non-alcoholic drink with a high antioxidant capacity that could be similar to the one found in red wine and to determine whether it could exert protective effects in the postprandial response in terms of oxidative stress and antioxidant capacity in healthy humans.

We develop and characterize a Chilean berry concentrate that consists of four berries produced in Chile, two of which are native species, with a high antioxidant capacity. In a randomized, crossover study, the effects of ingesting a dilute beverage prepared from the berry concentrate with a turkey meat burger prepared with or without 6% of the same concentrate were assessed on postprandial response, in terms of oxidative stress markers and antioxidant capacity.

The analysis of BPC-350 antioxidant capacity was evaluated using two different antioxidant assays: ORAC and FRAP (Table 1). These results indicate a high antioxidant capacity in comparison to other berries. Anthocyanins are the main phenolic compounds reported in native Chilean berries such as maqui (Aristotelia chilensis) or calafate (Berberis microphylla). The analysis of BPC-350 phenolic content by HPLC indicated that anthocyanins are the primary polyphenols present in BPC-350 (88.5%), and flavonoids and phenolic acids account for 4.5% and 7%, respectively. This formulation was created to obtain a high quality polyphenols beverage with good taste.

When volunteers ate the turkey burger with water, plasma MDA/TG levels rose, but when volunteers drank 5% w/v BPC-350 beverage instead of water they exhibited a 35% reduction in the area under the curve of plasma MDA/TG concentration during the 6 hour post-meal period (figure 1). This beverage diminished MDA accumulation in plasma. Interestingly, intake of the turkey burger with water did not change carbonyls in plasma proteins. However, the 5% w/v BPC-350 beverage produced a significant decrease in plasma protein carbonyl concentration. These results indicate that the 5% w/v BPC-350 beverage, under the scheme of this study, prevented lipid peroxidation and the consequent formation of MDA and MDA-protein adduct that occurs during digestion at the stomach level.

When MDA plasma concentrations were analyzed post-intake of Meal 3, no significant differences were observed when comparing MDA basal levels (time 0) with those produced 6 hours post-intake, indicating the inhibitory effect of plasma MDA produced by this meal. The mean values of the area under the curve indicate a complete reduction of MDA absorption compared with the response post-intake of Meals 1 and 2. In agreement with this information, we determined that the MDA quantity of Meal 3 (turkey burger prepared with BPC-350 concentrate and cooked) was 22.5 times less than the MDA quantity of Meal 1 and 2 (turkey burger prepared without BPC-350 and cooked, figure 2).

These data suggest that the strong effect observed for Meal 3 was due to the inhibition capacity of lipid peroxidation reactions by BPC-350 concentrate when the turkey burger was thermally processed. There was a dual protective effect produced by the inhibition of lipid peroxidation reactions, occurring at the stomach level and during thermal food processing.

The antioxidant capacity determined by DPPH post-intake of Meals 2 and 3 increased probably due to low molecular weight molecules, including; polyphenols, vitamin C, and urate (figure 3). Therefore, considering that BPC-350 do not contain vitamin C, the increase in the antioxidant activity induced by BPC-350 intake (especially in Meal 3) could be attributed to other compounds present in this concentrate or synthesized in the organism post-consumption.

The intake of Meal 1 diminished the antioxidant capacity of plasma measured as DPPH, according to the increase in MDA plasma concentrations. This could be explained by the utilization of endogenous antioxidants (able to react with DPPH radical) such as urate and glutathione, due to hydroperoxide absorption, which promotes lipid oxidation. The postprandial state induces immediate oxidative stress that triggers atherogenic changes including inflammation, endothelial dysfunction, hypercoagulability, and sympathetic hyperactivity.

The consumption of high-fat and high-iron potentially pro-oxidant foods such as red meat produced postprandial oxidative stress, as detected by the increment in plasma MDA and the reduction in plasma antioxidant capacity. The intake of food- or beverage-derived polyphenols with the meal prevented plasma oxidative stress, as evidenced by this work and those of other researchers.

The results obtained in this study indicate the usefulness of a berry-based drink to decrease postprandial oxidative stress. Our results emphasize the effectiveness of a berry concentrate for inhibiting lipoperoxidation reactions occurring at the stomach level but primarily during thermal treating of foods. The way in which food is prepared is critical to our health.

 

 

Figure 1. BPC-350 modulates postprandial levels of plasmatic malondialdehyde and protein carbonyls in human healthy subjects after the intake of three different meals: ■ meal 1 (ground turkey cutlets + water); ● meal 2 (ground turkey cutlets + BPC 350); ▲ meal 3 (ground turkey cutlets cooked in BPC-350 + BPC-350). ). Panels A and B show the time profile of malondialdehyde and protein carbonyls levels after the intake of three different meals, respectively. Panel C and D show the area under the curve of the different time profiles corresponding to three different meals for malondialdehyde and protein carbonyls levels, respectively. Data were expressed as the mean, * p < 0.05 compared to meal 1.

 

 

Figure 2. Malondialdehyde content in experimental foods used to perform the cross-over study. Malondialdehyde concentrations were quantified in uncooked and cooked turkey burgers prepared with or without BPC-350 at 6% (N=3). Data were expressed as the mean ± SD. * indicates significant differences when compared to uncooked turkey burger, uncooked turkey burger + BPC-350 and cooked turkey burger + BPC-350 (p < 0.05).

 

 

Figure 3. Antioxidant activity of human plasma determined by means of DPPH method before and after the intake of three different meals. ■ meal 1 (red meat + water); ● meal 2 (red meat + BPC 350); ▲ meal 3 (red meat cooked in BPC-350 + BPC-350). Panel A shows the time profile of normalized values of DPPH antioxidant. Panel B shows the area under the curve of the different time profiles, corresponding to the three different meals.

 

Table 1: Concentration of total polyphenols, total anthocyanins and antioxidant capacity of BPC-350 and 5% BPC-350 beverage.

GAE, gallic acid equivalents; CE, cyanidine 3-glucoside equivalents

 

References

[1] F. Leighton, G. Polic, P. Strobel, D. Perez, C. Martinez, L. Vasquez, O. Castillo, L. Villarroel, G. Echeverria, I. Urquiaga, D. Mezzano, J. Rozowski, Health impact of Mediterranean diets in food at work, Public Health Nutr 12(9a) (2009) 1635-43.
[2] G. Annuzzi, L. Bozzetto, G. Costabile, R. Giacco, A. Mangione, G. Anniballi, M. Vitale, C. Vetrani, P. Cipriano, G. Della Corte, F. Pasanisi, G. Riccardi, A.A. Rivellese, Diets naturally rich in polyphenols improve fasting and postprandial dyslipidemia and reduce oxidative stress: a randomized controlled trial, Am J Clin Nutr 99(3) (2014) 463-71.
[3] S. Devaraj, J. Wang-Polagruto, J. Polagruto, C.L. Keen, I. Jialal, High-fat, energy-dense, fast-food-style breakfast results in an increase in oxidative stress in metabolic syndrome, Metabolism 57(6) (2008) 867-70.
[4] F. Cardona, I. Tunez, I. Tasset, L. Garrido-Sanchez, E. Collantes, F.J. Tinahones, Circulating antioxidant defences are decreased in healthy people after a high-fat meal, Br J Nutr 100(2) (2008) 312-6.
[5] J. Kanner, S. Gorelik, S. Roman, R. Kohen, Protection by polyphenols of postprandial human plasma and low-density lipoprotein modification: the stomach as a bioreactor, J Agric Food Chem 60(36) (2012) 8790-6.
[6] S. Miranda-Rottmann, A.A. Aspillaga, D.D. Pérez, L. Vasquez, A.L.F. Martinez, F. Leighton, Juice and Phenolic Fractions of the Berry Aristotelia chilensis Inhibit LDL Oxidation in Vitro and Protect Human Endothelial Cells against Oxidative Stress, Journal of Agricultural and Food Chemistry 50(26) (2002) 7542-7547.
[7] A. Ruiz, I. Hermosín-Gutiérrez, C. Mardones, C. Vergara, E. Herlitz, M. Vega, C. Dorau, P. Winterhalter, D. von Baer, Polyphenols and Antioxidant Activity of Calafate (Berberis microphylla) Fruits and Other Native Berries from Southern Chile, Journal of Agricultural and Food Chemistry 58(10) (2010) 6081-6089.
[8] J.H. O’Keefe, N.M. Gheewala, J.O. O’Keefe, Dietary Strategies for Improving Post-Prandial Glucose, Lipids, Inflammation, and Cardiovascular Health, Journal of the American College of Cardiology 51(3) (2008) 249-255.
[9] F. Natella, A. Macone, A. Ramberti, M. Forte, F. Mattivi, R.M. Matarese, C. Scaccini, Red wine prevents the postprandial increase in plasma cholesterol oxidation products: a pilot study, Br J Nutr 105(12) (2011) 1718-23.
[10] R.B. Pereira, C. Sousa, A. Costa, P.B. Andrade, P. Valentao, Glutathione and the antioxidant potential of binary mixtures with flavonoids: synergisms and antagonisms, Molecules 18(8) (2013) 8858-72.