The impact of red cabbage fermentation on bioavailability of anthocyanins and antioxidant capacity of human plasma

Highlights

• Anthocyanin bioavailability after fresh and fermented red cabbage intake was compared.

• Ten new red cabbage anthocyanin metabolites in plasma and urine were identified.

• Among cyanidin metabolites identified, methylated forms were predominant.

• Fermentation process affects bioavailability of red cabbage anthocyanins.

• Plasma antioxidant capacity are higher after fresh red cabbage intake than fermented red cabbage.

Abstract

The effect of red cabbage fermentation on anthocyanin bioavailability and plasma antioxidant capacity in humans was studied. In a randomized crossover study, 13 volunteers consumed fresh and fermented red cabbage. Blood and urine samples were collected before and after consumption. Analyses of anthocyanins by HPLC–MS/MS and plasma antioxidant capacity by photochemiluminescence assay were conducted. Red cabbage products contained 20 different nonacylated and acylated anthocyanins with the main structure of cyanidin triglucosides. The anthocyanins ingested were present in physiological fluids in form of 18 native anthocyanins and 12 metabolites (methylated, glucuronided, sulfated). Among cyanidin metabolites identified, methylated forms were predominant. Bioavailability of anthocyanin from fresh red cabbage was over 10% higher than from fermented red cabbage. Upon fresh cabbage consumption, volunteers plasma showed higher antioxidant capacity than after fermented cabbage intake. The study has shown that fermentation process affects red cabbage anthocyanins bioavailability and human plasma antioxidant capacity.

Introduction

Previous studies have shown that vegetables are rich in a number of chemical substances known as phytochemicals, among others anthocyanins, which may have beneficial effects on the human body. Anthocyanins are red, orange, blue or purple water soluble pigments characterized by complex patterns of hydroxylation, methoxylation, glycosylation and acylation (Wu & Prior, 2005). They are considered to have cardio-protective, anti-carcinogenic, anti-neurodegenerative, vision-improving and diabetes-preventing properties (De Pascual-Teresa and Sanchez-Ballesta, 2008, Norberto et al., 2013). In addition, it has been found that when consumed, anthocyanins do not show any negative effects in experiments with animals, even at high doses (Clifford, 2000). As demonstrated in previous studies, anthocyanins are the main compounds among phytochemicals found in red cabbage (Manchali et al., 2012, Podsedek, 2007). The content of anthocyanins in red cabbage is high in comparison to other food sources (Wu et al., 2006), differs significantly across the varieties, and is influenced by vegetation period (Wiczkowski, Topolska, & Honke, 2014). Furthermore, it has been identified that technological processes, such as fermentation, affects the concentration and profile of red cabbage anthocyanins (Wiczkowski, Szawara-Nowak, & Topolska, 2015).

Since the positive effect of vegetables (e.g. red cabbage) on the body is attributed to the phytochemicals present in these plants, it is necessary to fully understand their function and, therefore, conduct a detailed and accurate assessment of dietary intake of phytochemicals (among others anthocyanins), their absorption, metabolism and accumulation in humans and animals upon intake of various foods. Up to now, it has been shown that flavonoids bioavailability such as quercetin and isoflavones is dependent on the solubility of compounds in the digestive tract, nutritional status of a subject, the chemical form of compounds (glycosides, aglycone), and the dietary matrix (Piskula, 2000). Moreover, there are only a few studies on bioavailability of phytochemicals from foodstuffs, which at the same time show the actual concentrations of phytochemicals in physiological fluids, compare differently processed foods, and take under consideration the high interindividual variability (Cermak et al., 2009). Also, there is no information regarding the comparison of bioavailability of anthocyanins from fresh and fermented red cabbage. Previous reports only prove that red cabbage anthocyanins are absorbed from gastrointestinal tract and are metabolized through the detoxification processes. Moreover, native derivatives of anthocyanins were also found in biological fluids after anthocyanins intake (Charron, Clevidence, Britz, & Novotny, 2007).

One of the theories referring to the formation of disorders in animal and human organisms holds that they are induced by the uncontrolled oxidation processes (Castro and Freeman, 2001, Magalhaes et al., 2008). Thus, it is considered that processes and factors which inhibit uncontrolled oxidation may reveal prophylactic activity. It is well established that blood plasma components, which form its antioxidant capacity, are albumins, uric and ascorbic acids, α-tocopherol, glutathione, a group of antioxidative enzymes, and other compounds, including anthocyanins, derived from food consumed. This suggests that a diet rich in anthocyanins may increase blood plasma antioxidative capacity, and may therefore be favorable for human health. The antioxidant properties of anthocyanins depend on the number and position of hydroxyl groups in their molecule. The structural conditions responsible for strong antioxidative activity are present in a cyanidin molecule, which in the in vitro systems scavenge radicals efficiently (Galvano et al., 2004, Kahkonen and Heinonen, 2003).

In previous studies, from nine to thirty-six different anthocyanins with a high concentration were found in various red cabbages (Charron et al., 2007, Pliszka et al., 2009), where occurred in nonacylated, monoacylated, and diacylated forms of only one anthocyanin aglycone such as cyanidin (Wiczkowski, Topolska, et al., 2014). In addition, it has been found that the kind of acylation affects antioxidant activity of acylated anthocyanins (Wiczkowski, Szawara-Nowak, & Topolska, 2013). Former reports also indicated that red cabbage is considered a vegetable of a considerably high antioxidant activity (Hassimotto et al., 2005, Wu et al., 2004), resulting from a high content of anthocyanins. To sum up, red cabbage rich in acylated anthocyanins with a high degree of glycosylation (marking higher stability) may be a better source of bioactivity than other foodstuffs containing only glycosylated form of anthocyanins. Red cabbage is also often exposed to various types of processing, including fermentation, in order to obtain more suitable and attractive food products with longer and more stable storage possibilities (Wiczkowski et al., 2015). Red cabbage is an attractive for consumers not only because of its intense purple/red color, but also its crucial dietetic and taste values. Therefore, red cabbage is gaining popularity all over the world and is eaten raw and after both home and technological treatment. Taking the above qualities into consideration, red cabbage proves to be a unique food matrix for investigating the relationship between the content and profile of anthocyanins in combination with the type of food processing applied against bioavailability of anthocyanins. Consequently, our study introduces new information about the bioavailability of anthocyanins from both fresh and fermented red cabbage, with the diet-relevant doses of these natural colorants. Since cyanidin aglycone and its derivatives are marked by strong biological activities (Galvano et al., 2004), to measure the potential beneficial effect of these compounds on the consumer’s body after absorption, the research in focus has been directed only at the compounds with flavylium cation structure as the main core.

Taking the above into account, in this study, the comparison of anthocyanins bioavailability from fresh and fermented red cabbage, with determination of anthocyanins derivatives profile appearing in physiological fluids after consumption of these red cabbage products have been explored for the first time. In addition, the effects of consumption of red cabbage anthocyanins on the antioxidant capacity of human blood plasma have been investigated.