In Vitro Bioaccessibility of Carotenoids and Vitamin ... - ACS Publications

Article pubs.acs.org/JAFC

Cite This: J. Agric. Food Chem. 2018, 66, 3801−3809

In Vitro Bioaccessibility of Carotenoids and Vitamin E in Rosehip Products and Tomato Paste As Affected by Pectin Contents and Food Processing Ahlam Al-Yafeai‡,† and Volker Böhm*,‡ ‡

Institute of Nutrition, Friedrich Schiller University Jena, Dornburger Straße 25-29, 07743 Jena, Germany Department of Biology, Science Faculty, Ibb University, Ibb, Yemen

†

ABSTRACT: Limited bioavailability of antioxidants present in food from fruits and vegetables matrices is determined by their low bioaccessibility due to the physical and chemical interactions of the antioxidants with the indigestible polysaccharides of cell walls. Therefore, this in vitro investigation aimed to assess the bioaccessibility of carotenoids and vitamin E from rosehips as well as from tomato paste and to investigate several aspects of effects of pectin contents and food processing on bioaccessibility. Following the addition of the enzyme mixture Fructozym P6-XL, the bioaccessibility of carotenoids from rosehips as well as from tomato paste significantly increased. The average relative increase in bioaccessibility from rosehips was lower for (all-E)-βcarotene compared with (all-E)-lycopene and (all-E)-rubixanthin. In contrast, increases of bioaccessibility of α-tocopherol were comparable for rosehip samples and tomato paste. KEYWORDS: Fructozym P6-XL, in vitro digestion, Rosa rugosa, Rosa canina, jam, rosehip puree

■

INTRODUCTION Nowadays, consumers ask more and more for healthy, tasty, and natural functional food products, as there is an increasing focus on relations between food and health. For this reason, the food industry now focuses on developing new products with potential impact on public health and the nutritional status of the population. In recent decades, rosehips and tomatoes have been increasingly studied for their preventive properties. It has been reported that rosehips are composed of several biologically active compounds (e.g., flavonoids, tannins, carotenoids, fatty acids, vitamins; particularly vitamins C, E and provitamin A).1 Various rose hip products have been released to the market as nutritive aids, health supplements, and cosmetics. Most food products are based on the hips of R. canina, although they are small compared with the rugosa hips.2 Additionally, tomatoes and tomato products are considered as a main source of lycopene, delivering the red color. There is increasing interest in lycopene due to epidemiological evidence suggesting that it may provide protection against a number of degenerative diseases.3 Carotenoid pigments are mainly C40 lipophilic isoprenoids and synthesized in all photosynthetic organisms (bacteria, algae, and plants) as well as in some nonphotosynthetic bacteria and fungi. While carotenoids are necessary to maintain normal health and behavior of animals, in general, carotenoids are not synthesized by animals and so those found in animals are directly accumulated from food.4 In nature, carotenoids mostly occur as (all-E)-isomers in plants. However, contents of (Z-)isomers may increase due to the isomerization of the (all-E)-isomers of carotenoids during food processing.5 Equally important, vitamin E is a lipophilic antioxidant, the term vitamin E covers eight fat-soluble compounds (α-, β-, γ-, δ-tocopherol, and tocotrienol) synthesized in plant organisms. α-Tocopherol is the most common form of vitamin E in human tissues and has long been © 2018 American Chemical Society

considered as a protective factor, preventing inflammatory and degenerative processes in the liver during the exposure to a range of xenobiotics, environmental pollutants, and dietary factors.6 A high intake of fruits and vegetables was associated with a lowered risk to develop chronic diseases (e.g., cardiovascular diseases and cancers).7 As the potential health benefits of bioactive compounds such as carotenoids and vitamins become more and more clear, there has been a growing interest in determination of bioaccessibility and bioavailability of these compounds from plant foods. Bioaccessibility is defined as the fraction of a compound that releases from its matrix in the gastrointestinal tract and thus becomes available for intestinal absorption.8−10 However, human intervention studies to assess intestinal absorption are expensive, often invasive, and of long duration. Static in vitro models based on human physiology were developed as simple, inexpensive, and reproducible tools to predict the bioavailability of different food components. Although one of the most relevant factors limiting the bioaccessibility of carotenoids at the preabsorptive stages is the food matrix, Minekus et al. (2014)11 aimed to find a standardized processing for an in vitro digestion model. Pectin molecules are also important structural elements in plant-based emulsions. The backbone of pectin is composed of segments of homogalacturonan (HG) and rhamnogalacturonan type I (RGI) and II (RGII),12 which are esterified with a varying degree of methylation (DM).13 In addition, Fructozym P6-XL is a liquid, highly concentrated pectolytic enzyme preparation for quick and complete pectin hydrolysis in fruit mash and fruit juice. Therefore, one purpose Received: Revised: Accepted: Published: 3801

December 14, 2017 March 23, 2018 April 1, 2018 April 6, 2018 DOI: 10.1021/acs.jafc.7b05855 J. Agric. Food Chem. 2018, 66, 3801−3809

Article

Journal of Agricultural and Food Chemistry

Figure 1. Experimental design of in vitro digestion. Sulfuric acid 98% and galacturonic acid-monohydrate were from Fluka, and carbazole and sodium hydroxide were from Merck. Description of the Samples. One kilogram of Rosa rugosa Thunb. hips was harvested at full ripening stage in late summer and early autumn at Spiekeroog Island on the North Sea coast of Germany (53° 46′ 19′′ N, 7° 41′ 49′′ E). One kilogram of mature hips of Rosa canina, and 200 g of R. canina puree were supplied by Maintal Konfitüren GmbH, Haßfurt, Germany. In addition, 150 g of R. canina powder (Bio-Hagebutten-Pulver, RaabVitalfood GmbH, Rohrbach, Germany), 200 g of tomato paste (Bio Tomatenmark), and 100 g of 100% apple pectin (Bio-Apfelpektin, Natura-Werk Gebr. Hiller GmbH & Co. KG, Germany) were purchased from a local store, and 360 g of R. canina jam (Konfitüre extra Hagebutten) were supplied by Lorenz & Lihn GmbH & Co. KG (Zarrentin, Germany). For analysis, raw hips of R. rugosa Thunb. and R. canina were cleaned, and seeds, stem, and calyx were removed just before homogenization. The hips were first rinsed thoroughly for 1−2 min with tap water and then 1 min with demineralized water. Next they were ground for 20 s with a mill (Retsch Grindomix GM 200, Haan, Germany) and stored at −25 °C until analysis. Pectin Quantification. Pectin contents were determined in each raw hip, R. canina products, and tomato paste both before and after hydrolysis by using the enzyme mixture Fructozym P6-XL. Five hundred milligrams of ground rosehip samples as well as rosehip products or tomato paste were weighed in 50 mL glass tubes. Samples were dissolved in 10 mL HPLC grade water, and then 20 mL of 96% ethanol (previously heating to 75 °C) was added. The glass tubes were heated in a water bath for 10 min at 80 °C, while the mixture was mixed periodically by using a glass rod. Then the volume was

of this study was to determine how pectin affects the bioaccessibility of carotenoids and vitamin E in rosehips (R. rugosa and R. canina), R. canina products (powder, jam, and puree) as well as tomato paste. Moreover, this study offers some important insights about carotenoids and vitamin E concentrations as well as pectin contents before and after hydrolysis by enzymes. Our second aim was to look for the effects of food matrix, food processing, and carotenoid properties on bioaccessibility.

■

MATERIALS AND METHODS

Chemicals. All chemicals and buffer salts were of analytical grade. Solvents for chromatography were of HPLC quality. HPLC grade water was prepared using a MicroPure instrument (Thermo Electron LED GmbH, Niederelbert, Germany). Specific chemicals were of the highest quality available (95−99%) and used without purification. Carotenoid standards (97−99%) were from CaroteNature (Münsingen, Switzerland). Pure tocopherols (>95%) and tocotrienols (>97%) were from Calbiochem (Darmstadt, Germany) and Davos Life Sciences (Singapore, Singapore), respectively. DL-α-Tocopheryl acetate (>96%) was from Sigma-Aldrich (Taufkirchen, Germany). αAmylase from Aspergillus oryzae (208 U/mg protein), pepsin (8002500 U/mg protein), pancreatin from porcine pancreas 8 × USP (U.S. Pharmacopeia), and porcine bile extract were also from Sigma-Aldrich. The enzyme mixture Fructozym P6-XL contains endopolygalacturonase (40−50 U/mL), pectinlyase (10000−12000 U/mL), pectinesterase (600−800 U/mL), and endoarabanase (40−50 U/mL) and was kindly supplied by Erbslöh Geisenheim AG (Geisenheim, Germany). 3802

DOI: 10.1021/acs.jafc.7b05855 J. Agric. Food Chem. 2018, 66, 3801−3809

Article


process was finalized by incubations of samples in a shaker at 250 rpm at 37 °C for 3 h. Isolation of Micellar Fraction. The fraction of carotenoids released from food matrix was isolated by centrifugation. At intervals of 20 min, the digest was centrifuged with 5000g at 4 °C. Then, 1.5 mL Eppendorf tubes with 1 mL aliquots were again centrifuged for 5 min with 20 000g at ambient temperature. The aqueous supernatant was filtered through a 0.45 μm polypropylene filter; afterward, filtrates and digestion residues were stored at −25 °C until analysis within 2 days. Extraction of Carotenoids and Vitamin E. The extraction of carotenoids and vitamin E is in line with the procedure used by Werner and Böhm (2011)16 with minor modifications. In centrifuge tubes, 5 ± 0.05 g of filtered supernatants and 0.5 ± 0.02 g of digestion residues were weighed. Glass beads and 1 mL of water were added to the residues, followed by vortexing for 30 s. Following this, 2 mL of ethanol and internal standards including 50 μL of echinenone solution and 20 μL of α-tocopheryl acetate solution were added to all samples.16 The extraction with 1 mL of MtBE and 1 mL of petroleum ether was replicated by vortexing for 30 s. After the completion of these steps, samples were centrifuged at room temperature for 3 min with 3000g, the upper phase was collected, and the extraction was repeated four times. As soon as these steps have been carried out, the volume of combined extracts can be reduced by using a rotaryevaporator at 30 °C. The dried residues were dissolved in 5 mL of MeOH/THF (1/1, v/v, + 0.1% BHT) using an ultrasonic bath. Additional centrifugation was performed for 5 min and 20 000g, and carotenoids were analyzed by using HPLC-DAD.16 Finally, an independent 250 μL aliquot of this solution was dried under a stream of nitrogen and dissolved again in 250 μL of n-hexane/MTBE (98:2, v/m), followed by centrifugation (20 000g, 5 min) prior to HPLC analysis of vitamin E.16 Saponification. This processing is necessary for the determination of xanthophyll contents in rosehips to remove chlorophylls (and degradation products) and to hydrolyze xanthophyll esters. Saponification was conducted by using 10% methanolic KOH for 60 min at room temperature. Carotenoids Analysis. Carotenoids contents in the samples were analyzed according to the method described by Al-Yafeai et al.18 Individual carotenoids were identified by comparing their retention times with those of external standards,16 and all lycopene isomers were quantified by a 3-point calibration curve of external standard (all-E)lycopene. Vitamin E Analysis. Contents of tocopherols and tocotrienols in the samples were analyzed according to the method described by AlYafeai et al.18 Individual tocochromanols were identified by comparing their retention times with those of external standards16 and quantified by 5-point calibration curve of external standards. Total vitamin E contents were calculated as sum of all individual tocopherols and tocotrienols determined by HPLC analysis. Calculations. Bioaccessibility refers to the fraction of the total amount of carotenoids and vitamin E that is potentially available for absorption. For the calculations, the following equation was used:

completed to 50 mL with 96% ethanol; the mixture was centrifuged for 15 min with 5000g, and supernatants were removed and discarded. Previous steps were repeated once again by using 40 mL of 63% ethanol (previously heated to 75 °C), and supernatants were removed and discarded. The precipitates were removed to 100 mL glass flask by using a rubber policeman with HPLC grade water. The rubber policeman was cleaned also by using HPLC-grade water to avoid losing any amount of pectin. Following this, 5 mL of NaOH was added to the flask, and the volume was increased to 100 mL by using HPLCgrade water and then was left for 15 min with shaking periodically. Finally, the mixture was filtrated by using filter paper. The quantification was done by using a colorimetric reaction with carbazole at 525 nm14 Enzymatic Hydrolysis of Pectin. The enzymatic hydrolysis of pectin was optimized according to the procedure described by Erbslöh Geisenheim.15 A 600 mg sample was subjected to treatment with 200 μL Fructozym P6-XL enzyme in a 50 mL glass tube. Then, 10 mL of demineralized water were added, and the pH was adjusted to 4. Finally, the mixture was incubated for 90 min at 45 °C. Then pectin quantification was carried out by using the method that has been described above. Pectin content is calculated by using the following equation:14

P[mgGA/100g] = (G × 100)⋰(W × 10) G = μg galacturonic acid−monohydrate/mL filtrate (taken from calibration), W = weight of sample in g. Experimental Design. The static in vitro digestion model was optimized according to procedures previously described.9,10,16 Several modifications have been adopted according to the standardized protocol.11 To study the effect of pectin on bioaccessibility, the experiment was conducted in three groups (Figure 1) depending on the pectin contents: (i) control sample, (ii) sample treated with Fructozym P6-XL, (iii) sample with added pectin. Rosehip raw materials and products were investigated with and without Fructozym P6-XL. In contrast, in addition to these two variants, 800 mg of pectin was added to tomato paste before the initial phase to make pectin contents comparable to rosehips. All procedures were performed in subdued light to minimize the oxidation of the carotenoids. Sample Preparations. Samples were prepared in triplicates, approximately 5 ± 0.05 g of materials were weighed into 50 mL centrifuge tubes (which were covered with aluminum foil). For the same processing, 5 mL of NaCl 0.9% were added to all samples. As presented in Figure 1, group (ii) was treated with 0.5 mL enzyme mixture Fructozym P6-XL. Then, the mixture was mixed for 2 min and incubated in a shaking water bath at 40 °C for 2 h. In group (iii), 800 mg of apple pectin was added to the samples and then mixed for 2 min. Initial Phase. Olive oil (0.25 ± 0.02 g) was added, and the mixture was incubated at 37 °C for 1 h at 250 rpm in a shaker. The addition of dietary oils with high contents of unsaturated fatty acids has been shown to promote carotenoid bioaccessibility by enhancing their micellarization during digestion.17 Eight milliliters of a pyrogallol solution (12.6 mg/mL NaCl 0.9%) was added, and the mixture was incubated in a shaking water bath for 10 min at 37 °C.10 In Vitro Bioaccessibility Assay. To mimic the oral phase, pH was adjusted to 6.5 by adding 2 M NaOH. Two milliliters of α-amylase solution (20 mg/mL NaCl 0.9%) was added, and the mixture was overlaid with nitrogen and incubated at 37 °C for 30 min at 250 rpm in a shaker. To simulate gastric conditions, the pH was adjusted to 2.0 with 1 M HCl, and 2 mL of porcine pepsin (40 mg/mL in 0.1 M HCl buffer solution) was added. The mixture was overlaid with nitrogen and incubated in a shaker at 37 °C for 1 h at 250 rpm. To mimic the intestinal phase, the pH of the previously simulated stomach condition was increased to 6.5 by adding 2 M NaOH. After that, a mixture of porcine bile extract and pancreatin (9 mL containing 12 mg/mL bile extract and 2 mg/mL pancreatin in 0.1 M NaHCO3) and 4 mL of porcine bile extract (0.1 g/mL 0.1 M NaHCO3) were added. The additional amount of bile extract was used because previous experiments resulted in an increase in the bioaccessibility of lycopene and more polar compounds such as rubixanthin.9,16 The digestion

efficiency of micellarization [%] content in supernatant ·100 = (content in residue + content in supernatant) The stability of carotenoids and vitamin E during simulated digestion was determined by comparing results with the raw samples.16 The calculation was expressed by the contents in the digesta (solid residue + supernatant) in relation to contents in the raw samples.16 The raw samples were extracted in the same way as supernatants and residues.

recovery [%] =

(solid residue + supernatant) ·100 content in raw sample

loss [%] = 100 − recovery 3803


Article


Table 1. Carotenoids Concentrations in Saponified Extracts of R. Rugosa and R. Canina Products as well as in Tomato Paste [mg/100 g] (mean ± SD) (n = 3)a carotenoids/sample

R. rugosa

(all-E)-rubixanthin (all-E)-β-carotene (all-E)-lycopene (Z)-lycopene

5.5 3.2 7.9 8.3

± ± ± ±

0.7d 0.2b 1.5b 0.5

R.C.R

R.C.Pr

R.C.Pu

tomato paste

± ± ± ±

4.4 ± 0.1c 5.1 ± 0.5d 4.7 ± 0.5a -

0.9 ± 0.1a 1.9 ± 0.2a 4.8 ± 0.2a -

1.3 ± 0.01 28 ± 3 10 ± 12

2.1 4.2 7.4 8.3

0.2b 0.2c 1.2b 0.1

a

Different letters in the same line indicate significant differences in carotenoids contents between rosehip samples (P < 0.05; ANOVA, followed by S−N−K).

α- and γ-tocopherol as well as vitamin E contents in raw hips and R. canina products as well as in tomato paste. The high concentration of each tocopherol and tocotrienol in rosehips is related to the presence of oil (different fatty acids).20 On the other hand, vitamin E analysis in tomato paste revealed α- and γ-tocopherol but no tocotrienols (Table 2). Pectin Contents. Pectin is a mixture of compounds with pectinic acid as the major component. In the current analysis, raw hips as well as products already had high contents of pectin. In this context, R. canina raw hips contained 2.0 ± 0.01 g GA/ 100 g compared with R. rugosa raw hips 1.7 ± 0.01 g GA/100 g (Table 3). The difference in pectin contents depends on the ecotype as well as on ripening time. On the other hand, a high content of pectin in R. canina products is comparable to a previous investigation.21 Pectin contents in samples were reduced significantly (P < 0.05) after being treated with the enzyme mixture Fructozym P6-XL. As mentioned above, Fructozym P6-XL is a liquid, highly concentrated pectolytic enzyme mixture containing pectinmethylesterase (PME), pectinlyase (PL), and endopolygalacturonase (PG), and it is used to complete pectin degradation in juice for a good clarification and filterability. PME catalyzes de-esterification of methoxyl group of pectin forming pectic acid. The enzyme acts preferentially on a methyl ester group of a galacturonate unit next to a nonesterified galacturonate unit. In contrast, PG is a pectin-depolymerizing enzyme, cleaving α-(1−4)-glycosidic linkages in polygalacturonic acid by trans-elimination.22 Moreover, the results also showed incomplete degradation of pectin in samples after treatment with Fructozym P6-XL, perhaps because fruit cell walls are often pectin-enriched. Grassin and Fauquembergue23 reported that residual pectins and hemicelluloses in the strawberries and raspberries bind to phenolic substances and proteins during processing and storage, resulting in irreversible complexes that enzymes cannot break down. Table 3 also presents different relative degradation rates in the treated samples because the type of carbon source and structure of pectin substrates influences the enzyme activity

Statistical Analysis. Significance of the results and statistical differences were analyzed by using Prism program for windows, version 7.0 (GraphPad Software, Inc., San Diego CA, U.S.A.). All analyses were performed at least three times, and the results are expressed as mean ± standard deviation (SD). A difference was considered statistically significant at p < 0.05. One-way ANOVA with Student−Newman−Keuls posthoc test, multiple t test, and unpaired t test were used to compare data obtained from samples.

■

RESULTS AND DISCUSSION Carotenoids Contents. Damage and loss of free carotenoids during the saponification procedure is possible. However, the saponified extracts were used for identification and quantification of carotenoids in rosehips, especially rubixanthin, according to our previous work18 (Table 1), with results being almost comparable to Andersson et al.19 Vitamin E Contents. As previously reported, α- and γtocopherol were the main tocopherol isomers in R. canina rosehip raw materials and products, whereas in R. rugosa, only α-tocopherol was determined.18 Table 2 illustrates contents of Table 2. Tocopherol and Tocotrienol Contents (mean ± SD) in Rosehips of R. rugosa and R. canina [μmol/100 g] (n = 3)a α-tocopherol

γ-tocopherol

sample

∑ tocotrienol

vitamin E

C [μmol/100 g]

R. rugosa R.C.R R.C.Pr R.C.Pu R.C.Ja Tomato paste

14 11 20 7 3 8

± ± ± ± ± ±

0.1c 1c 2d 1b 0.1a 1

4.4 12 2.3 0.9 0.6

n.d. ± 1b ± 2c ± 0.2a ± 0.2a ± 0.01

n.d. n.d. n.d. n.d. n.d n.d.

14 16 32 9 4 9

± ± ± ± ± ±

0.1c 2c 3d 1b 0.1a 1

a

Different letters in the same column indicate significantly different results (P < 0.001; ANOVA, followed by S−N−K), n.d. = not detected.

Table 3. Pectin Contents (mean ± SD) in Rosehip Raw Materials and Products as well as in Tomato Paste [mg GA/100 g] (n = 3)a sample R. rugosa R.C.R R.C.Pr R.C.Pu R.C.Ja tomato paste

untreated samples

samples+ Fructozym P-6L

P [mg GA/100 g]

P [mg GA/100 g]

1.7 2.0 1.8 1.6 1.6 0.4

± ± ± ± ± ±

0.01 0.01 0.00 0.00 0.01 0.0

0.6 0.8 0.5 0.5 0.4

± ± ± ± ±

0.01* 0.01* 0.00* 0.00* 0.00*

% of degradation 65 60 72 70 75

-

a

Unpaired t test (Graphpad Software, USA). Asterisk within the same line indicates significant difference (p < 0.05) of result in comparison to the untreated sample. 3804


Article


(i) effects of pectin, (ii) effects of food matrix and processing, and (iii) effects of carotenoid properties (Figure 2).

profile. PL prefers to hydrolyze high-esterified pectin while exoPG and endo-PG more often cleave low-esterified pectin. In Vitro Model. Although rosehips have more recently attracted attention because of their potential health benefits, no study has investigated the bioaccessibility of carotenoids and vitamin E from rosehip raw materials as well as its products. The in vitro model has been adapted to investigate several influential factors on the bioaccessibility of carotenoids and vitamin E. In this context, different in vitro methods have been previously described9,10,16 and were used in the assessment of carotenoid accessibility in each rosehip raw material. Several modifications of static in vitro digestion have been conducted and adopted according to the standardized protocol of Minekus et al.11 Interestingly, the bioaccessibility of rubixanthin, βcarotene and lycopene in rose hips was improved (+ 300− 400%).24 Mild heating in the initial phase, in addition to extending digestion times during the stomach phase and intestinal phase, as recommended by Minekus et al.,11 were the main reasons for this improvement. Initial Phase. Carotenoids are lipophilic micronutrients, located inside the chromoplast organelles in a specific substructure of crystalline, membranous, or globular nature embedded in a cellular structure.25 Several factors involve components of the food matrix, which are cellular and subcellular species-specific characteristics of the food that act as barriers to nutrient release.26 Crushing the raw materials helps to release carotenoids by reducing particle size and thus promotes bioaccessibility. Furthermore, amount and type of lipids seem to affect carotenoid bioavailability. In this study, 0.25 ± 0.05 mL of olive oil (main fatty acid: oleic acid (C18:1)) was added, followed by incubation for 1 h at 40 °C with shaking at 250 rpm (Figure 1). There are similarities between the attitudes expressed by Huo et al.27 and Salvia-Trujillo et al.28 who showed an increase in the bioaccessibility of each lycopene and β-carotene with increasing fatty acyl chain length (C18:1 > C8:0 > C4:0) upon addition of oil to a salad meal. This was attributed to the greater solubilization capacity of mixed micelles containing long-chain fatty acids.28 Additionally, thermal processing with 40 °C facilitated the transfer of carotenoids from the cells to the olive oil droplets through weakened plant wall structure. Hedrén et al. (2002)9 reported that thermal treatments promoted the disruption of the food matrix, leading to an increase in β-carotene bioaccessibility in carrot pieces. In Vitro Bioaccessibility of Lipophilic Micronutrients. Knowledge of lipid digestion is important for understanding of absorption of lipophilic food ingredients. Dietary lipids enhanced secretion of bile salts and led to a stimulation of the activity of pancreatic lipase, which in turn increase micellarization capacity.29 Pancreatic lipase facilitated the transfer of carotenoids from emulsified lipid droplets toward mixed micelles.30 Therefore, lipid digestion can be divided into two steps: (i) the hydrolysis and (ii) the micellarization. Hydrolysis of dietary triacylglycerols (TAGs) into diacylglycerols (DAGs), monoacylglycerols (MAGs), and free fatty acids (FFAs) is essential for their absorption by enterocytes and their incorporation into micelles.31 The micellarization is a process to form molecular aggregates of 3−10 nm (micelles) through the action of bile salts on lipid particles.32 The micelles are composed of MAGs and FFAs, bile salts, phospholipids, and lipid-soluble compounds.33 Regarding the carotenoids bioaccessibility, results will be discussed by handling three aspects:

Figure 2. Structures of the investigated carotenoids.

Pectin and Bioaccessibility. Although soluble fiber consumption has widely recognized health benefits, the impact of pectin and other dietary fibers on the bioavailability and metabolism of other nutrients, including lipids, is still under investigation. Some in vitro studies showed for pectin a potential to impact lipid digestion processes,34 which can affect the carotenoid’s bioaccessibility. The relations between pectin contents and carotenoids bioaccessibility in rosehips as well as in tomato paste are shown in Tables 4 and 5. Following the addition of the enzyme mixture Fructozym P6-XL, the bioaccessibility of carotenoids from rosehips significantly increased. The average relative increase was lower for ((allE))-β-carotene (+21%) compared with ((all-E))-lycopene (+50%) and (all-E)-rubixanthin (+48%). In contrast, in tomato paste, a strong evidence of bioaccessibility of individual carotenoids was found after treatment with Fructozym P6-XL (P < 0.001). Likewise, as shown in Table 5, adding pectin to tomato paste caused significantly reduced bioaccessibility of each (all-E)-lycopene to 13 ± 1%, (Z)-lycopene to 25 ± 2% and (all-E)-β-carotene to 44 ± 3% compared with untreated samples. These results match those observed in earlier studies.35 Xu et al.36 have speculated that pectin can effect bioaccessibility through two mechanisms. The passive absorption in the small intestine may block as a result of pectin action on the lipids and bile salt molecules, thereby avoiding micelle formation with carotenoids. Furthermore, pectin increases the viscosity of the intestinal content. Thus, absorption of antioxidants was reduced perhaps due to lower activity of enzymes and increased difficulty in contacting intestinal enterocyte. The effects of pectin on bioaccessibility and bioavailability depend on different factors; such as pectin degree of methylation (DM), distribution of nonmethylesterified galacturonic acid residues, molar mass, linear charge density and hydrophobicity. Kyomugasho et al.37 showed that in regions containing pectin with a higher DM, cell adhesion is probably weaker, and thus, tissues are more easily disintegrated into smaller particles.37 On the other hand, pectin with a lower DM is more strongly bound in cell walls, and thus, regions rich in low DM pectin are not easily disrupted resulting in larger particles.37 In general, high-DM pectin increases the lipolysis, bile salt binding, and micellarization of polar carotenoids.35 However, low-DM pectin can reduce the levels of calcium 3805


Article

Journal of Agricultural and Food Chemistry Table 4. Bioaccessibility of Carotenoids in Rosehip Raw Materials and Hip Products (n = 3)a (all-E)-lycopene bioaccessibility % sample R. rugosa R.C.R R.C.Pr R.C.Ja R.C.Pu

WE 32 16 23 20 15

± ± ± ± ±

5* 1* 5 3* 1*

(Z)-lycopene bioaccessibility %

Un. 18 8 19 14 10

± ± ± ± ±

WE 4 1 3 1 3

51 52 64 47 50

± ± ± ± ±

total lycopene bioaccessibility %

Un.

4* 0.1* 4 10 0.0*

44 37 61 41 33

± ± ± ± ±

WE 3 5 3 4 5

40 27 45 32 27

± ± ± ± ±

(all-E)-β-carotene bioaccessibility %

Un.

4* 2* 1 6* 1*

31 17 40 25 21

± ± ± ± ±

WE 1 1 1 1 5

67 61 74 73 73

± ± ± ± ±

6* 1* 2* 1* 4*

(all-E)-rubixanthin bioaccessibility %

Un. 58 53 60 53 67

± ± ± ± ±

WE 5 2 6 3 6

63 67 74 76 76

± ± ± ± ±

2* 4* 1* 0* 1*

Un. 49 44 54 49 43

± ± ± ± ±

3 6 5 1 5

a

Unpaired t test (Graphpad Software, U.S.A.). Asterisks in the same line indicate significant differences (p < 0.05) between treated and untreated sample. WE: with enzyme (Fructozym P6-XL), Un: untreated samples

comparison of the two results in Tables 4 and 5 reveals that the bioaccessibilities of individual carotenoids in tomato paste were higher than in rosehips. The present findings seem to be consistent with results of an in vivo study (Unpublished data).42 Schweiggert and Carle43 showed for hips of R. rugosa tubular or globular-tubular chromoplasts, containing partly lipid-dissolved but mostly liquid-crystalline carotenoids.43 Consequently, the globular-tubular deposition form might be more favorable than the protein-complexed and solid-crystalline forms, respectively.43 In contrast, crystalloid chromoplasts were previously described in red tomato.44 Zhou et al.45 have previously reported that the crystalline state of carotenoids was associated with their poor bioavailability. The low bioavailability was affected by the deposition of carotenoids in proteinpigment complexes and crystalline aggregates, respectively.46 These two reasons as well as high pectin contents in rosehips may explain the relatively low bioavailability in rosehips compared to tomato paste. Noncrystalline deposition of lycopene is rarely found in natural plant foods since (all-E)lycopene easily crystallizes. Therefore, most common lycopene containing fruits (red tomatoes, watermelon, and red-fleshed papaya) have crystalline lycopene aggregates.44 According to Cooperstone et al.,47 lycopene was markedly more bioavailable from tangerine than from red tomato juice, consistent with a predominance of (Z)-lycopene isomers and presence in chromoplasts in a lipid dissolved globular state. These reasons in addition to the profile structure of cis-isomers could be a possible explanation for the more efficient micellarization of cisisomers compared to trans-isomers. Effect of Carotenoid Properties. As shown in Tables 4 and 5, regardless of the sample type or the treatment, the carotenoids showed different bioaccessibility. Overall, the bioaccessibility decreased in the following order: (all-E)rubixanthin ≥ (all-E)-β-carotene > (Z)-lycopene > (all-E)lycopene. Carotenoid hydrophobicity and transfer efficiency were inversely related. Xanthophylls are more efficiently transferred into micelles and thus show a higher bioaccessibility than the hydrocarbons β-carotene or lycopene.25 In agreement with this hypothesis, the micellarization of rubixanthin increased after treatment with Fructozym P6-XL in all rosehip samples (Table 4). However, an unexpected result was observed in the present study, the bioaccessibility of (all-E)β-carotene was greater than that of (all-E)-rubixanthin in all untreated rosehip samples. A possible explanation for these results: the hydrophobicity is not the only factor affecting the carotenoids bioaccessibility. In the same vein, Sólyom et al.48 showed the following order of bioaccessibilities: β-carotene > γcarotene > lycopene ≈ β-cryptoxanthin > rubixanthin after delivery of carotenoids to an in vitro digestion model. Furthermore, (all-E)-lycopene had a significantly lower

Table 5. Bioaccessibility of Carotenoids in Tomato Paste (n = 3)a bioaccessibility % tomato paste (all-E)-lycopene (Z)-lycopene total lycopene (all-E)-β-carotene

Un. 41 64 46 86

± ± ± ±

WE 2b 6b 3b 2b

61 72 60 84

± ± ± ±

WP 5c 2b 6c 3b

13 25 16 44

± ± ± ±

1a 2a 1a 3a

a Different letters in the same line indicate significant differences in different treatments (P < 0.001; ANOVA, followed by S−N−K). WE: with enzyme (Fructozym P 6-XL), Un: untreated samples, and WP: with pectin.

involved in the lipolysis and generation of lipid digestion products for micelle formation.37 Effects of Food Processing on Bioaccessibility of Carotenoids. To our knowledge, no previous study has investigated the effect of food matrix and food processing on the bioaccessibility of carotenoids in rose hips. As shown in Table 4, there were differences in the efficiency of carotenoids micellarization in each two rosehip species. The bioaccessibility of total lycopene in hips of R. rugosa was higher than that in hips of R. canina. These findings are supported by Stinco et al.38 These authors suggested that the food matrix structure is one of the most important factors that affect the bioaccessibility of carotenoids. In addition, as mentioned above, pectin foodmatrix-related factors may hinder carotenoids bioaccessibility. As presented in Table 3, raw R. canina hips had higher pectin contents compared with raw R. rugosa hips, this could be a reason for the relatively low carotenoids bioaccessibilities of the R. canina hips. In addition, samples (Table 3) also include three different products of R. canina (powder, jam, and puree). (allE)- and (Z)-Lycopene were highly variable in different products, whereas the accessibilities of (all-E)-β-carotene and (all-E)-rubixanthin were almost comparable. The order of lycopene bioaccessibilities was determined to be R.C.Pr > R.C.Ja ≥ R.C.Pu. A possible explanation for this might be related to food processing. Food processing with breaking of the natural matrix may lead to higher bioavailability.39 Consequently, the effect of particle size reduction is expected to arise from disintegration of the food matrix and reduction in the potential plant cell wall barrier toward digestion.40 Accordingly, the solubility is enhanced by increasing the surface area for dissolution, thus enhancing the enzymes and permeation of bile salts. The positive effect of food processing on carotenoid bioaccessibility is in accordance with in vivo studies on carotenoid bioavailability41 and confirms that eating processed vegetables improves carotenoid bioavailability. Interestingly, a 3806


Article


bioaccessibility, significantly increasing the bioaccessibilities of carotenoids and vitamin E after pectin hydrolysis by using Fructozym P6-XL.

bioaccessibility compared to (all-E)-β-carotene in all samples with different treatments. These findings seem to be consistent with other research.45 Lycopene is more lipophilic than βcarotene because of its acyclic structure without a β-ionone ring. On the other hand, the interactions between carotenoids have been demonstrated. During micellar formation, the competition between lycopene and β-carotene has been recorded.49 The favored β-carotene transfer into the micelles could also hinder lycopene incorporation. Further analysis showed that the efficiency of micellarization of (Z)-lycopene was significantly greater than that of (E)-lycopene (Tables 4 and 5). These results match those observed in earlier studies by Ferruzzi et al.50 who found that the profile structures of cis− isomers were micellarized more efficiently than trans-isomers. The (Z)-lycopene isomers are less likely to crystallize, more oil/hydrocarbon soluble, compared to (E)-lycopene. During a simulated in vitro digestion model, the recovery rates of carotenoids were determined, the rates of stabilities were >70% with average 80%. Oil droplets were removed from the aqueous fraction by filtration, resulting thus in a loss in carotenoids in supernatant and residue. Vitamin E Bioaccessibility. The results obtained from the preliminary analysis of vitamin E bioaccessibility are presented in Figure 3A,B. Vitamin E bioaccessibility significantly increased

■

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel.: +49 3641 949633. Fax: +49 3641 949702. ORCID

Volker Böhm: 0000-0002-9474-4718 Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS We appreciate the help of Mohamed Yahya (Institute of Pharmacy, Ernst-Moritz-Arndt-University, Greifswald, Germany) and Chelsee Holloway (Department of Animal Science, Rutgers the State University of New Jersey, USA) who have helped in this paper and in that line improved the manuscript significantly.

■

ABBREVIATIONS USED HG, homogalacturonan; RGI, rhamnogalacturonan type I; RGII, rhamnogalacturonan type II; R.C.R, Rosa canina raw; R.C.Pr, Rosa canina powder; R.C.Pu, Rosa canina puree; R.C.Ja, Rosa canina jam; WE, with enzyme (Fructozym P6-XL); Un, untreated samples; WP, with pectin; DM, degree of methylation; TAGs, triacylglycerols; MAGs, monoacylglycerols; DAGs, diacylglycerols; FFAs, free fatty acids; PME, pectinmethylesterase; PL, pectinlyase and; PG, endopolygalacturonase

■

REFERENCES

(1) Demir, F.; Ö zcan, M. Chemical and technological properties of rose (Rosa canina L.) fruits grown wild in Turkey. J. Food Eng. 2001, 47, 333−336. (2) Barros, L.; Carvalho, A. M.; Ferreira, I. C. F. R. Exotic fruits as a source of important phytochemicals: improving the traditional use of Rosa canina fruits in Portugal. Food Res. Int. 2011, 44, 2233−2236. (3) Khachik, F.; Carvalho, L.; Bernstein, P. S.; Muir, G. J.; Zhao, D. Y.; Katz, N. B. Chemistry, distribution, and metabolism of tomato carotenoids and their impact on human health. Exp. Biol. Med. 2002, 227, 845−851. (4) Agarwal, M.; Parameswari, R. P.; Vasanthi, H. R.; Das, D. K. Dynamic action of carotenoids in cardioprotection and maintenance of cardic health. Molecules 2012, 17, 4755−4769. (5) Schieber, A.; Carle, R. Occurrence of carotenoid cis-isomers in food: Technological, analytical, and nutritional implications. Trends Food Sci. Technol. 2005, 16, 416−422. (6) Aboul-Soud, M. A.; Al-Othman, A. M.; El-Desoky, G. E.; AlOthman, Z. A.; Yusuf, K.; Ahmad, J.; Al Khedhairy, A. A. Hepatoprotective effects of vitamin E/selenium against malathioninduced injuries on the antioxidant status and apoptosis related gene expression in rats. J. Toxicol. Sci. 2011, 36, 285−296. (7) Singh, P.; Goyal, G. K. ″Dietary lycopene: Its properties and anticarcinogenic effects. Compr. Rev. Food Sci. Food Saf. 2008, 7 (3), 255−270. (8) Benito, P.; Miller, D. Iron absorption and bioavailability: an updated review. Nutr. Res. (N. Y., NY, U. S.) 1998, 18, 581−603. (9) Hedrén, E.; Diaz, V.; Svanberg, U. ″Estimation of carotenoid accessibility from carrots determined by an in vitro digestion method.″. Eur. J. Clin. Nutr. 2002, 56 (5), 425−430. (10) Reboul, E.; Richelle, M.; Perrot, E.; Desmoulins-Malezet, C.; Pirisi, V.; Borel, P. Bioaccessibility of carotenoids and vitamin E from their main dietary sources. J. Agric. Food Chem. 2006, 54, 8749−8755.

Figure 3. (A) Bioaccessibility of vitamin E in rosehip raw materials and hip products (n = 3). Asterisks indicate significant differences of results in comparison to the untreated samples (* p ≤ 0.05, ** p ≤ 0.001. Multiple t test (GraphPad Software, USA). Un: untreated samples, WE: with enzymes (B) Bioaccessibility of vitamin E in tomato paste (n = 3), different letters a/b/c indicate significant differences (P < 0.001) in differently treated samples. One-way ANOVA Tukey’s multiple comparisons test (GraphPad Software, U.S.A.). Un: untreated samples, WE: with enzymes, WP: with pectin

after treatment with Fructozym. On the other hand, these results also accord with our earlier observations in carotenoids. The stability of vitamin E during simulated digestion was >78% and averaged 82%. In agreement with Reboul et al.,10 the bioaccessibility of tocopherols from different foodstuffs was highly variable. As mentioned above, the bioaccessibility of nutrients depend on the physical properties of the food matrix. Dietary tocopherols are mostly present in the free forms (except in fortified food). Dietary carotenoids may be present as protein-bound, ester, and free forms. This may explain the higher bioaccessibility of vitamin E compared with lycopene. These results match those observed in earlier studies.10 Although the study has successfully gone some way toward enhancing our understanding of correlations between the pectin contents, food processing, and bioaccessibility, it has raised some new questions in need of further investigation. Our results confirm that pectin has a major effect on the 3807


Article

Journal of Agricultural and Food Chemistry (11) Minekus, M.; Alminger, M.; Alvito, P.; Ballance, S.; Bohn, T.; Bourlieu, C.; Carrière, F.; Boutrou, R.; Corredig, M.; Dupont, D.; Dufour, C.; Egger, L.; Golding, M.; Karakaya, S.; Kirkhus, B.; Le Feunteun, S.; Lesmes, U.; Macierzanka, A.; Mackie, A.; Marze, S.; McClements, D. J.; Menard, O.; Recio, I.; Santos, C. N.; Singh, R. P.; Vegarud, G. E.; Wickham, M. S. J.; Weitschies, W.; Brodkorb, A. A standardised static in vitro digestion method suitable for food − an international consensus. Food Funct. 2014, 5, 1113−1124. (12) Sila, D. N.; Van Buggenhout, S.; Duvetter, T.; Fraeye, I.; De Roeck, A.; Van Loey, A.; Hendrickx, M. Pectins in processed fruits and vegetables: Part II Structure function relationships. Compr. Rev. Food Sci. Food Saf. 2009, 8, 86−104. (13) Wicker, L.; Kim, Y.; Kim, M. J.; Thirkield, B.; Lin, Z.; Jung, J. Pectin as a bioactive polysaccharide - Extracting tailored function from less. Food Hydrocolloids 2014, 42, 251−259. (14) Matissek, R.; Steiner, G. Lebensmittelanalytik; 3. Auflage; Springer-Verlag: Berlin Heidelberg, 2006. (15) Product Datasheet for FructozymP. http://www.erbsloeh.com/ product_datasheets/en/PMB_FructozymP_GB_001.pdf. (16) Werner, S.; Böhm, V. Bioaccessibility of carotenoids and vitamin E from pasta: evaluation of an in vitro digestion model. J. Agric. Food Chem. 2011, 59, 1163−1170. (17) Failla, M. L.; Chitchumronchokchai, C.; Ferruzzi, M. G.; Goltz, S. R.; Campbell, W. W. Unsaturated fatty acids promote bioaccessibility and basolateral secretion of carotenoids and αtocopherol by Caco-2 cells. Food Funct. 2014, 5, 1101−1112. (18) Al-Yafeai, A.; Malarski, A.; Böhm, V. Characterization of carotenoids and vitamin E in R. rugosa and R. canina: Comparative analysis. Food Chem. 2018, 242, 435−442. (19) Andersson, S. C.; Rumpunen, K.; Johansson, E.; Olsson, M. E. Carotenoids content and compostion in rosehips (Rosa spp) during ripening, determination of suitable maturity marker and implications for health promoting food products. Food Chem. 2011, 128, 689−696. (20) Asplund, K. Antioxidant vitamins in the prevention of cardiovascular disease: Asystematic review. J. Intern. Med. 2002, 251, 372−392. (21) Yildiz, O.; Alpaslan, M. Properties of rose hip marmalades. Food Technol. Biotech 2012, 50, 98−106. (22) Verlent, I.; Hendrickx, M.; Verbeyst, L.; Van Loey, A. Effect of temperature and pressure on the combined action of purified tomato pectin methylesterase and polygalacturonase in presence of pectin. Enzyme Microb. Enzyme Microb. Technol. 2007, 40 (5), 1141−1146. (23) Grassin, C.; Fauquembergue, P. Fruit juices. In Industrial Enzymology, 2nd ed.; Godfrey, T., Reichelt, J., West, S., Eds.; Nature Publishing Group: London, 1996; pp 225−264. (24) Al-Yafeai, A.; Böhm, V. Factors affecting bioaccessibility of rosehip carotenoids - in vitro results. Lebensmittelchemie 2015, 69, 105. (25) Schweiggert, R. M.; Mezger, D.; Schimpf, F.; Steingass, C. B.; Carle, R. Influence of chromoplast morphology on carotenoid bioaccessibility of carrot, mango, papaya, and tomato. Food Chem. 2012, 135, 2736−2742. (26) Palmero, P.; Lemmens, L.; Ribas-Agustí, A.; Sosa, C.; Met, K.; de Dieu Umutoni, J.; Hendrickx, M.; Van Loey, A. Novel targeted approach to better understand how natural structural barriers govern carotenoid in vitro bioaccessibility in vegetable based systems. Food Chem. 2013, 141, 2036−2043. (27) Huo, T.; Ferruzzi, M. G.; Schwartz, S. J.; Failla, M. L. Impact of fatty acyl composition and quantity of triglycerides on bioaccessibility of dietary carotenoids. J. Agric. Food Chem. 2007, 55 (22), 8950−8957. (28) Salvia-Trujillo, L.; Qian, C.; Martin-Belloso, O.; McClements, D. J. Modulating β-carotene bioaccessibility by controlling oil composition and concentration in edible nanoemulsions. Food Chem. 2013, 139, 878−884. (29) Furr, H. C.; Clark, R. M. Intestinal absorption and tissue distribution of carotenoids. J. Nutr. Biochem. 1997, 8, 364−377. (30) Borel, P.; Tyssandier, V.; Mekki, N.; Grolier, P.; Rochette, Y.; Alexandre-Gouabau, M. C.; Lairon, D.; Azaïs-Braesco, V. Chylomicron beta-carotene and retinyl palmitate responses are dramatically

diminished when men ingest beta-carotene with medium-chain rather than long-chain triglycerides. J. Nutr. 1998, 128, 1361−1367. (31) McClements, D. J.; Decker, E. A. Controlling lipid bioavailability using emulsion based delivery systems. In McClements, D. J., Decker, E. A., Eds.; Designing functional foods; CRC Press: New York, 2009; pp 502−546. (32) Johnson, L. R.; Gerwin, T. A. Gastrointestinal Physiology; Mosby: St. Louis, MO. 2001. (33) Yonekura, L.; Nagao, A. Intestinal absorption of dietary carotenoids. Mol. Nutr. Food Res. 2007, 51, 107−115. (34) Zhang, R.; Zhang, Z.; Zhang, H.; Decker, E. A.; McClements, D. J. Influence of emulsifier type on gastrointestinal fate of oil-in-water emulsions containing anionic dietary fiber (pectin). Food Hydrocolloids 2015, 45, 175−185. (35) Cervantes-Paz, B.; Ornelas-Paz, J.; Pérez-Martínez, J. D.; ReyesHernández, J.; Zamudio-Flores, P. B.; Rios-Velasco, V.; IbarraJunquera, S.; Ruiz-Cruz, S. Ruiz-Cruz. Effect of pectin concentration and properties on digestive events involved on micellarization of free and esterified carotenoids. Food Hydrocolloids 2016, 60, 580−588. (36) Xu, H.; Jiao, Q.; Yuan, F.; Gao, Y. In vitro binding capacities and physicochemical properties of soluble fiber prepared by micro fluidization pre-treatment and cellulose hydrolysis of peach pomace. LWT - Food Sci. Technol. 2015, 63, 677−684. (37) Kyomugasho, C.; Willemsen, L. D. D.; Christiaens, S.; Van Loey, A. M.; Hendrickx, M. E. Pectin-interactions and in vitro bioaccessibility of calcium and iron in particulated tomato-based suspensions. Food Hydrocolloids 2015, 49, 164−175. (38) Stinco, C. M.; Fernández-Vázquez, R.; Escudero-Gilete, M. L.; Heredia, F. J.; Meléndez-Martínez, A. J.; Vicario, M. Effect of orange juice’s processing on the color, particle size, and bioaccessibility of carotenoids. J. Agric. Food Chem. 2012, 60, 1447−1455. (39) Parada, J.; Aguilera, J. M. Food microstructure affects the bioavailability of several nutrients. J. Food Sci. 2007, 72 (2), R21−32. (40) Bohn, T.; McDougall, G. J.; Alegría, A.; Alminger, M.; Arrigoni, E.; Aura, A. M.; Brito, C.; Cilla, A.; El, S. N.; Karakaya, S.; MartínezCuesta, M. C.; Santos, C. N. Mind the gap - deficits in our knowledge of aspects impacting the bioavailability of phytochemicals and their metabolitesa position paper focusing on carotenoids and polyphenols. Mol. Nutr. Food Res. 2015, 59 (7), 1307−1323. (41) van het Hof, K. H.; de Boer, B. C.; Tijburg, L. B.; Lucius, B. R.; Zijp, I.; West, C. E.; Hautvast, J. G.; Weststrate, J. A. Carotenoid bioavailability in humans from tomatoes processed in different ways determined from the carotenoid response in the triglyceride-rich lipoprotein fraction of plasma after a single consumption and in plasma after four days of consumption. J. Nutr. 2000, 130 (5), 1189−1196. (42) Brose, A. Humaninterventionsstudien zur Untersuchung der intestinalen Absorption von Lycopin und Rubixanthin aus Hagebuttenmark. Diploma Thesis, Friedrich Schiller University Jena, Jena, Germany, 2010. (43) Schweiggert, R. M.; Carle, R. Carotenoid deposition in plant and animal foods and its impact on bioavailability. Crit. Rev. Food Sci. Nutr. 2017, 57, 1807−1830. (44) Schweiggert, R. M.; Steingass, C. B.; Heller, A.; Esquivel, P.; Carle, R. Characterization of chromoplasts and carotenoids of red- and yellow-fleshed papaya (Carica papaya L.). Planta 2011, 234, 1031− 1044. (45) Zhou, J. R.; Gugger, E. T.; Erdman, J. W., Jr. The crystalline form of carotenes and the food matrix in carrot root decrease the relative bioavailability of β- and α-carotene in the ferret model. J. Am. Coll. Nutr. 1996, 15, 84−91. (46) Schweiggert, R. M.; Kopec, R. E.; Villalobos-Gutierrez, M. G.; Högel, J.; Quesada, S.; Esquivel, P.; Schwartz, S. J.; Carle, R. Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: a randomised cross-over study. Br. J. Nutr. 2014, 111, 490−498. (47) Cooperstone, J. L.; Ralston, R. A.; Riedl, K. M.; Haufe, T. C.; Schweiggert, R. M.; King, S. A.; Timmers, C. D.; Francis, D. M.; Lesinski, G. B.; Clinton, S. K.; Schwartz, S. J. Enhanced bioavailability of lycopene when consumed as cis-isomers from tangerine compared 3808


Article

Journal of Agricultural and Food Chemistry to red tomato juice, a randomized, cross-over clinical trial. Mol. Nutr. Food Res. 2015, 59, 658−669. (48) Sólyom, K.; Maier, C.; Weiss, J.; Cocero, M. J.; Mato, R. B.; Carle, R.; Schweiggert, R. Structure−response relationship of carotenoid bioaccessibility and antioxidant activity as affected by the hydroxylation and cyclization of their terminal end groups. Food Res. Int. 2014, 66, 107−114. (49) Fernández-García, E.; Mínguez-Mosquera, M. I.; Pérez-Gálvez, A. Changes in composition of the lipid matrix produce a differential incorporation of carotenoids in micelles. Interaction effect of cholesterol and oil. Innovative Food Sci. Emerging Technol. 2007, 8 (3), 379−384. (50) Ferruzzi, M. G.; Lumpkin, J. L.; Schwartz, S. J.; Failla, M. Digestive Stability, Micellarization, and Uptake of α-Carotene isomers by Caco-2 human intestinal cells. J. Agric. Food Chem. 2006, 54, 2780− 2785.

3809


In Vitro Bioaccessibility of Carotenoids and Vitamin ... - ACS Publications

Recommend Documents