Absorption of Carotenoids and Mechanisms Involved in Their Health-Related Properties
16.3 Bioaccessibility
16.3.1 Food Matrix
The effect of the food matrix includes the combined effects of all factors from a food that simultaneously promote or reduce the bioavailability/bioaccessibility of carotenoids (Ornelas-Paz et al.2008). The food matrix effect includes differences in the composition and storage sites of carotenoids as well as changes in the food by ripening and processing.
16.3.1.1 Chromoplast Morphology
The bioaccessibility of carotenoids from fruits is significantly higher than that of vegetables (de Pee et al.1998). This effect has been associated to the differential physical disposition of carotenoids within chromoplasts. Typically, carotenoids are stored as a lipid solution in globular and tubular chromoplasts of mature fruits; however, they can also be accumulated as crystalline structures. They may be complexed with proteins in chloroplasts of green vegetables (Schweiggert et al. 2012; Vásquez-Caicedo et al. 2006). During digestion, lipid bodies rich in carotenoids from fruits may easily interact with the lipidic phase of the gas- trointestinal content, making them more bioaccessible and bioavailable (West and Castenmiller 1998). In contrast, crystalline forms are not completely dissolved during their transit through the gastrointestinal tract (de Pee et al. 1998). The in vitroandin vivobioaccessibility of“-carotene from different sources followed the order of mango > papaya > tomato > carrot and this order was explained in terms of differences in the chromoplast morphology and accumulation forms of carotenoids in fruits and vegetables (Schweiggert et al.2012,2014). The difference in“-carotene bioaccessibility from mango and papaya could be consequence of differences in the presence of carotenoids in liquid-crystalline stores in the chromoplasts of these foods. The results for tomato could not be explained in these terms. Ornelas-Paz et al. (2010) also demonstrated in rats that “-carotene from mango was two times more bioavailable than from carrots. Carrillo-Lopez et al. (2010) reported that the levels of hepatic retinol in rats depended on the source of“-carotene, following the order of mango > carrot > spinach > parsley.
16.3.1.2 Ripening
Ripening modifies the amount and type of carotenoids in fruits and vegeta- bles. The chloroplasts of green vegetables and immature fruits mainly contain lutein,“-carotene, violaxanthin and neoxanthin. During ripening, the chloroplasts are transformed in chromoplasts with an increased biosynthesis of carotenoids (Rodriguez-Amaya and Kimura 2004; Yahia and Ornelas-Paz 2010). In some cases, the carotenoids of chloroplast serve as precursor of other carotenoids during ripening (Cervantes-Paz et al.2012,2014). The increase of total carotenoids during
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the ripening has been reported for different fruits and vegetables. The fully ripe mango, endive and lettuce have from 2.5 to 4 times more total carotenoids than the slightly ripe fruits or young leaves (Azevedo-Meleiro and Rodriguez-Amaya 2005b; Ornelas-Paz et al. 2008). The carotenoid content in red peppers (Jalapeño, Agridulce, Bola, Szentesi Kosszarvú Paprika) is 11 to 85 times higher than in green peppers (Cervantes-Paz et al.2012; Deli et al.1996; Mínguez-Mosquera and Hornero-Méndez1994b). Of course, this behavior is not observed in all vegetable foods, as occur in for young and mature leaves of kale or spinach (Azevedo-Meleiro and Rodriguez-Amaya2005a, b). These qualitative and quantitative changes may influence the carotenoid bioaccessibility. Thakkar et al. (2007) reported a positive correlation between the content of “-carotene in cassava and its efficiency of micellarization and uptake by Caco-2 cells.
The esterification of xanthophylls during ripening has been reported in peppers, sea buckthorn berries, bananas, kiwis, among others (Andersson et al. 2009;
Cervantes-Paz et al.2012, 2014; Mínguez-Mosquera and Hornero-Méndez,1994a;
Montefiori et al. 2009). The esterification of carotenoids reduces their polarity and bioaccessibility. After in vitro digestions of citrus juices, the micellarization of free “-cryptoxanthin was three times higher than that of the monoesterified forms (Dhuique-Mayer et al.2007). Thein vitromicellarization of free zeaxanthin was about two and seven times higher than that of mono and diesterified forms in wolfberry, orange pepper, red pepper and squash (Chitchumroonchokchai and Failla 2006). These tendencies were also seen for the uptake by Caco-2 cells in both studies. Victoria-Campos et al. (2013a, b) reported that the micellarization of free and esterified forms of capsanthin, antheraxanthin, mutatoxanthin, and zeaxanthin also followed the order of free > monoesterified > diesterified forms after in vitro digestions of raw or heat-processed red peppers. The study of the in vitro bioaccessibility of different monoesterified forms of capsanthin and“-cryptoxanthin suggests that their micellarization is influenced by the polarity provided by the fatty acid bounded to the carotenoid backbone, following an order of micellarization efficiency of laurate > myristate > palmitate (Dhuique-Mayer et al.2007; Victoria- Campos et al.2013a, b). However, Breithaupt et al. (2003) demonstrated that free and esterified forms of “-cryptoxanthin showed similar in vivo bioaccessibility.
The absence of esterified carotenoids in human plasma after the consumption of fruits rich in carotenoid esters suggests that only free forms are absorbed or that some esterases cleavage carotenoid esters (Granado et al. 1998; Wingerath et al.
1995). Further studies about the digestion, absorption and metabolism of esterified carotenoids are needed.
Ripening also cause fruit softening, which involve the solubilization, depoly- merization and demethylation of pectins from cell walls (de Roeck et al. 2008;
Gross and Sams 1984; Redgwell et al. 1997). Pectins and other fibers could alter the emulsification of lipids in the gastrointestinal medium and their further hydrolysis (Pasquier et al. 1996). These fibers are also able to interact with bile salts, disturbing the micellarization processes (Dongowski et al. 1996; Pasquier et al. 1996). Ornelas-Paz et al. (2008) demonstrated that the bioaccessibility of
“-carotene was significantly enhanced by the ripening of mango. This effect was
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associated with the quantitative and qualitative ripening-related changes of mango pectin. Victoria-Campos et al. (2013a, b) reported that ripening of peppers did not affect the micellarization of free carotenoids; however, the ripening stage of fruits determined the number and micellarization efficiency of esterified xanthophylls.
The information about the effect of ripening on the bioaccessibility of carotenoids is scarce; however, some studies suggest that qualitative and quantitative changes of the intrinsic pectin substances during fruit ripening play an important role. Cell wall composition and metabolism vary widely between plant foods.
16.3.1.3 Heat Processing
Heat processing reduces the negative effects of food matrix on carotenoid bioac- cessibility and bioavailability (Ornelas-Paz et al. 2008; Yahia & Ornelas-Paz 2010). The heat processing causes the disruption of food matrix, loss of cellular integrity and breaking of protein-carotenoid complexes. These effects may increase the carotenoid extractability during digestion and their further bioaccessibility and bioavailability (Yahia and Ornelas-Paz 2010). The softening of fruits by the heat processing has been associated with the solubilization, depolymerization and demethylation of pectins (de Roeck et al 2008; Ramos-Aguilar et al. 2015; Sila et al. 2006). These heat processing mediated effects in the food matrix may vary as a function of time, intensity and type of processing. The bioaccessibility of lycopene from tomato pulp increased as the heat processing temperature rose from 60 to 140 ıC, with the bioaccessibility of cis- and trans-lycopene being almost 2 times higher in puree treated at 140ıC, as compared with raw samples (Colle et al.2010). The bioaccessibility of carotenes from carrots was 80 and 57 % greater after cooking (100 ıC, 10 min) and blanching (80 ıC, 10 min), respectively, as compared with raw samples (Netzel et al. 2011). Lemmens et al. (2009) reported that the bioaccessibility of “-carotene from carrots increased as the duration and temperature of heat processing increased from 0 to 50 min and from 90 to 110ıC, respectively. The heat-processing style also alters the carotenoid bioaccessibility.
Bengtsston et al. (2009) reported that the bioaccessibility of“-carotene from carrots was almost 50 % lower after microwave heating in comparison with boiling and steaming. Ryan et al. (2008) demonstrated that the bioaccessibility of “-carotene from boiled courgette, red pepper and tomato was higher than that of the raw, grilled, microwaved and steamed foods. Similar tendencies were observed for lutein. The bioaccessibility of lycopene from courgette was increased by grilling and microwaving. Contrarily, these treatments hindered the bioaccessibility of “- cryptoxanthin from all evaluated fruits (Ryan et al.2008). Victoria-Campos et al.
(2013b) reported that heat processing decreased the bioaccessibility of many free and esterified carotenoids from red peppers. These studies suggest that the effect of heat processing on carotenoid bioaccessibility depends on carotenoid type and plant food.
The heat processing also alters the qualitative and quantitative profile of carotenoids. These pigments are highly thermolabile. Heat processing may
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induce the trans to cis isomerization, epoxidation and degradation of carotenoids (Cervantes-Paz et al. 2012, 2014; Rodriguez-Amaya 1999). The micellarization of 13-cis and 9-cisisomers of “-carotene is higher than that of the form all-trans (Bengtsson et al.2009; Bechoff et al.2009; Ekesa et al.2012; Tyssandier et al.2003;
Victoria-Campos et al. 2013b). The micellarization and uptake of cis-lycopene by Caco-2 cells was also higher than that of all-trans-lycopene (Failla et al.2008).
Accordingly, the greater bioaccessibility of cis-lycopene in comparison with the all-trans isomer has also been reportedin vivo (Boileau et al. 1999; Cooperstone et al. 2015; Stahl and Sies 1992). This phenomenon might be explained in terms of the higher solubility of thecisisomers of carotenoids due to the bent backbone.
This might favor their transference to the micelles (Yahia and Ornelas-Paz2010).
There is scarce information about the bioaccessibility of carotenoid epoxides. It has been suggested that they are not absorbed in humans (Stinco et al.2012). Recently, Victoria-Campos et al. (2013a,b) reported the formation of capsanthin 5,6-epoxide in Jalapeño peppers as a consequence of heat processing and demonstrated that this compound was efficiently micellarized. However, Asai et al. (2008) reported that although some epoxyxanthophylls (neoxanthin and fucoxanthin) are efficiently micellarizaced, their concentration in plasma (about 1 nmol/L) does not increase after the consumption of foods containing these carotenoids.
16.3.1.4 Mechanical Processing
The release of carotenoids from the food matrix is directly enhanced by the rupture of cells and cellular compartments before the consumption of a plant food. van het Hof et al. (2000) reported that the concentration of lycopene in the triglyceride- rich lipoprotein fraction of plasma increased 32 and 62 % after the ingestion of mildly and severely homogenized tomato products, respectively, as compared with the consumption of non-homogenized tomatoes. The concentration of “- carotene in this plasma fraction increased 5.6 and 8.2 times as a consequence of these homogenization levels. Livny et al. (2003) also demonstrated the“-carotene bioaccessibility from carrots puree is 50 % greater than that of chopped carrots.
Castenmiller et al. (1999) reported that the estimated relative bioavailability of “- carotene increased 86 % after the consumption of liquefied spinach in comparison to whole leaf in healthy subjects. Recently, Aschoff et al. (2015) found that thein vitro micellarization of lutein, “-cryptoxanthin, ’-carotene, and “-carotene increased from 1.3 to 3.5 times when the orange segments were replaced by orange juice in the digestive reactions. These studies collectively indicate that homogenization style alters the bioaccessibility of carotenoids. The new homogenization technologies such as high-pressure homogenization did not represent an advantage on the bioaccessibility of lycopene from tomato pulp (Colle et al.2010). Apparently, this technology induces a fiber network that entraps lycopene.
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