Original Research ArticleEffects of pectins and sugars on β-carotene bioaccessibility in an in vitro simulated digestion model
Introduction
The consumption of fruit- and vegetable-based products has been associated with various health benefits, including reduced risk of certain cancers, cardiovascular disease, and eye disease (Stinco et al., 2019; Zhao et al., 2017). Nowadays, consumer demand for fruit and vegetable juice, such as those higher in nutritional values, minimal processing, and high quality, have been growing quickly (Suárez-Jacobo et al., 2010). Since only a fraction of these nutrients absorbed by the human body can effectively contribute any health benefits, nutrient bioaccessibility can provide more relative information than total nutrient concentration when evaluating the nutritional quality of fruits and vegetables (Knockaert et al., 2012). Carotenoid bioaccessibility is defined as the amount of carotenoid that is released from the food matrix into the gastrointestinal tract, becoming available for intestinal absorption (Hedrén et al., 2002b; Kopec and Failla, 2018). Carotenoids possess various biological functions for humans, predominantly provitamin A activity, antioxidant properties, and immune system enhancement (Granado-Lorencio et al., 2017; Xavier and Mercadante, 2019). On account of their lipophilic nature and specific localization in plant-based tissues, carotenoid bioaccessibility is generally quite low in raw fruits and vegetables (Lemmens et al., 2014). Since carotenoids need to be released from plant cell, solubilized into the lipid phase, and incorporated into mixed micelles with certain hydrolysates of lipids before absorption (Mutsokoti et al., 2017; Palmero et al., 2016); thermal or mechanical processing prior to consumption is essential to open the structural organization in which the carotenoids are embedded and promote their liberation from food matrices (Lemmens et al., 2014). In addition to applying food processing as a first step to promote the release of carotenoids from fruits and vegetables, improving carotenoid biacccessibility during digestion and absorption from a molecular interaction perspective is also required. During this process, pectin plays an important role since it is mostly located in plant cell walls, and thus is released in fruits and vegetables along with carotenoids after food processing.
Pectins are a family of heterogeneous polysaccharides with galacturonic acid (GalA) as the main monosaccharide moiety. In its primary structure, pectin is mainly composed of the following four domains: homogalacturonan (HG), rhamnogalacturonan-I (RG-I), rhamnogalacturonan-II (RG-II), and xylogalacturonan (XGA) (Mohnen, 2008). The functional properties of pectin in fruit- and vegetable-based products are strongly dependent on the characteristics of the HG region. The proportion and distribution of esterified GalA residues in HG strongly impact many of the functional properties of pectin, including its solubility, thickening, gelling, and hydration properties, which might influence its interactions with other compounds present in the sample or digestive fluids (e.g. ions, lipids, lipase, bile acids, or micelles) (Cervantes-Paz et al., 2017; Ngouémazong et al., 2011; Verrijssen et al., 2015). During the gastrointestinal stage, pectin may inhibit lipid digestion by binding with calcium, interacting with bile salts, altering digestive medium viscosity, changing the interface between oil and water phases, and inhibiting lipase activity (Cervantes-Paz et al., 2017). Consequently, pectin has the potential to influence the digestion of carotenoids via changing the digestive environment, since carotenoids are digested and absorbed along with lipids. The assumption that pectin can influence carotenoid bioaccessibility is based on experimental observations. For example, the relative bioaccessibility of β-carotene and lutein from uncooked leaves of eight vegetables was inversely correlated with pectin and cell wall contents (Sriwichai et al., 2016). Similar to this, Aschoff et al. (2015) reported a negative correlation between pectin content and the β-cryptoxanthin bioaccessibility of orange juice. The network formation of de-esterified pectin molecules held together by hydrogen bonding and hydrophobic interactions induced by ultrasound treatment resulted in gel-like properties within the tomato pulp that inhibited lycopene digestion (Barba et al., 2017). Besides macromolecular polysaccharides (e.g. pectin), the effects of micromolecular sugars (e.g. fructose, glucose, and sucrose) on digestive fluids, especially in fruits and vegetables rich in sugars, including apple, pear, and sugar beet, are also deserved to study.
To estimate the bioaccessibility of carotenoids from different food matrices, in vitro digestion models are proposed and considered to be appropriate analytical methods (Bengtsson et al., 2009). The in vitro bioaccessibility of carotenoid is usually calculated as the fraction of carotenoids from intestinal digesta to micellar fraction (O’Connell et al., 2007; Li et al., 2017; Zhang et al., 2015). The in vitro digestion models vary depending on the specific food component being analysed, the nature of the food matrices, and the sophistication of the in vitro digestion model applied (Hur et al., 2011). Generally, in vitro digestion models related to the carotenoid bioaccessibility of fruit and vegetable-based juice systems or emulsion systems include the stomach and small intestine phase (Corte-Real et al., 2018; Rodrigo et al., 2015; Salvia-Trujillo et al., 2019), and there are also models that contain the mouth, stomach, and small intestine phase (Cano et al., 2019; Liu et al., 2019a, b; Yuan et al., 2018). In recent years, most of the studies on the correlations between pectin and carotenoid bioaccessibility have been conducted on real juice or emulsion systems (Cervantes-Paz et al., 2016; Gence et al., 2018; Verrijssen et al., 2014). A simple juice model system might provide direct insight into the interactions between two nutrients during digestion. Consequently, the present study aims to understand how pectin and sugars affect the characteristics of digestive fluids and the bioaccessibility of β-carotene in simple juice model systems using in vitro digestion. Specifically, this study aims to understand the characteristics of digestive fluids, including the investigation of color parameters and rheological properties, to gain insight into the digestive process.
Section snippets
Materials
Pectin esterified from citrus fruit (≥ 85% esterified), pectin-esterified potassium salt from citrus fruit (55–70% esterified), and pectin from citrus peel (≥ 6.7% esterified), β-carotene (≥ 93%), β-carotene (HPLC grade), D-(-)-Fructose (≥ 99%), D-(+)-Glucose (≥ 99%), sucrose (99%), uric acid sodium salt, and sodium DL-lactate; along with mucin from porcine stomach, pepsin from porcine gastric mucosa (≥ 250 units/mg), lipase from porcine pancreas (type II), and butylated hydroxytoluene (BHT)
FT-IR analysis of initial pectin
The infrared spectra of the initial pectin were similar in wavenumbers of absorption peaks (Fig. 1). The major characteristics of the absorption peaks were as follows: (i) The peak at 3438.96 cm−1 was attributed to an OH stretch, (ii) the peaks at 2935.56 cm−1, 1753.23 cm−1, and 1620.15 cm−1 were attributed to the C–H stretching of CH2 groups, CO stretching vibration of methyl esters of carboxyl groups, and asymmetric CO stretching vibration of the carboxylate ion, respectively; and (iii) the
Conclusions
In this study, pectin concentration, pectin DM, and sugar variety had the potential to change the characteristics of digestive fluids and CBA in juice model systems. Apparent viscosity showed differences in the initial and mouth phases in which higher pectin concentration (MMP-4) and lower DM (MMP-2 and LMP-2) could cause higher apparent viscosity. There was no marked difference for the apparent viscosity of all systems in the stomach and the small intestine phase, showing that viscosity had
CRediT authorship contribution statement
Jianing Liu: Conceptualization, Data curation, Writing - original draft, Visualization, Investigation. Jinfeng Bi: Conceptualization, Supervision, Resources. Xuan Liu: Conceptualization, Methodology, Resources, Supervision, Writing - review & editing. Dazhi Liu: Software, Validation, Writing - review & editing. Xinye Wu: Data curation, Resources. Jian Lyu: Supervision, Resources. Yingying Ding: Writing - review & editing.
Declarations of Competing Interest
None.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (no. 31671868), the National Key Research and Development Program of China (no. 2016YFD0400302-3) and the Central Public-interest Scientific Institution Basal Research Fund (no. S2019RCJC02).
References (72)
- et al.
Bioaccessibility of bioactive compounds from fruits and vegetables after thermal and nonthermal processing
Trends Food Sci. Technol.
(2017) - et al.
Impact of high hydrostatic pressure and thermal treatment on the stability and bioaccessibility of carotenoid and carotenoid esters in astringent persimmon (Diospyros kaki Thunb, var. Rojo Brillante)
Food Res. Int.
(2019) - et al.
Calcium and acid induced gelation of (amidated) low methoxyl pectin
Food Hydrocoll.
(2006) - et al.
Effect of pectin concentration and properties on digestive events involved on micellarization of free and esterified carotenoids
Food Hydrocoll.
(2016) - et al.
Effects of pectin on lipid digestion and possible implications for carotenoid bioavailability during pre-absorptive stages: a review
Food Res. Int.
(2017) - et al.
Study of the interactions between pectin in a blueberry puree and whey proteins: functionality and application
Food Hydrocoll.
(2019) - et al.
Cell wall polysaccharides from pulp and peel of cubiu: a pectin-rich fruit
Carbohydr. Polym.
(2017) - et al.
Magnesium affects spinach carotenoid bioaccessibility, in vitro, depending on intestinal bile and pancreatic enzyme concentrations
Food Chem.
(2018) - et al.
In vitro bioaccessibility of free and esterified carotenoids in cajá frozen pulp-based beverages
J. Food Compos. Anal.
(2018) - et al.
In vitro digestion testing of lipid-based delivery systems: calcium ions combine with fatty acids liberated from triglyceride rich lipid solutions to form soaps and reduce the solubilization capacity of colloidal digestion products
Int. J. Pharm.
(2013)
Impact of pectin properties on lipid digestion under simulated gastrointestinal conditions: comparison of citrus and banana passion fruit (Passiflora tripartita, var. mollissima) pectins
Food Hydrocoll.
Characterization of the global structure of low methoxyl pectin in solution
Food Hydrocoll.
Structural modifications of sugar beet pectin and the relationship of structure to functionality
Food Hydrocoll.
Biomarkers of carotenoid bioavailability
Food Res. Int.
Relevance and challenges in modeling human gastric and small intestinal digestion
Trends Biotechnol.
Rheological properties of natural low-methoxyl pectin extracted from sunflower head
Food Hydrocoll.
In vitro human digestion models for food applications
Food Chem.
In situ gelling pectin formulations for oral drug delivery at high gastric pH
Int. J. Pharm.
FT-IR study of plant cell wall model compounds: pectic polyasaccharides and hemicelluloses
Carbohydr. Polym.
Pectin gelling in acidic gastric condition increases rheological properties of gastric digesta and reduces glycaemic response in mice
Carbohydr. Polym.
Changes in β-carotene bioaccessibility and concentration during processing of carrot puree
Food Chem.
Recent advances in the bioaccessibility and bioavailability of carotenoids and effects of other dietary lipophiles
J. Food Compos. Anal.
Effect of high pressure homogenization (HPH) on the physical stability of tomato juice
Food Res. Int.
FT-IR spectroscopy, a reliable method for routine analysis of the degree of methylesterification of pectin in different fruit-and vegetable-based matrices
Food Chem.
Carotenoid bioaccessibility in fruit- and vegetable-based food products as affected by product (micro)structural characteristics and the presence of lipids: a review
Trends Food Sci. Technol.
Effects of high pressure homogenization on pectin structural characteristics and carotenoid bioaccessibility of carrot juice
Carbohydr. Polym.
FT-IR spectroscopy as a tool for measuring degree of methyl esterification in pectins isolated from ripening papaya fruit
Postharvest Biol. Technol.
Pectin structure and biosynthesis
Curr. Opin. Plant Biol.
Carotenoid bioaccessibility and the relation to lipid digestion: a kinetic study
Food Chem.
Quantifying structural characteristics of partially de-esterified pectins
Food Hydrocoll.
Xanthophyll carotenoids are more bioaccessible from fruits than dark green vegetables
Nutr. Res.
Lycopene and β-carotene transfer to oil and micellar phases during in vitro digestion of tomato and red carrot based-fractions
Food Res. Int.
Role of structural barriers for carotenoid bioaccessibility upon high pressure homogenization
Food Chem.
Determination of the degree of esterification of pectinates with decyl and benzyl ester groups by diffuse reflectance infrared fourier transform spectroscopy (drifts) and curve-fitting deconvolution method
Carbohydr. Polym.
Comparative study on lipid digestion and carotenoid bioaccessibility of emulsions, nanoemulsions and vegetable-based in situ emulsions
Food Hydrocoll.
Deliberate processing of carrot purées entails tailored serum pectin structures
Innov. Food Sci. Emerg. Technol.
Cited by (8)
Recent advances in the effects of food microstructure and matrix components on the bioaccessibility of carotenoids
2024, Trends in Food Science and TechnologyNovel Pickering emulsion gels stabilized solely by phenylalanine amidated pectin: Characterization, stability and curcumin bioaccessibility
2023, International Journal of Biological MacromoleculesGelling properties and interaction analysis of fish gelatin–low-methoxyl pectin system with different concentrations of Ca<sup>2+</sup>
2020, LWTCitation Excerpt :Since non-methylesterified GalA residues can form complexes with divalent cations, the DM of pectin is the principal factor determining its maximum binding capacity with Ca2+, Zn2+, and Fe2+ ions (Rousseau et al., 2019). Importantly, an LMP pectin may reduce the bio-accessibility of minerals for intestinal absorption, as well as affect carotenoid availability (Liu et al., 2020; Rousseau et al., 2019). However, mineral bio-accessibility has been shown to improve with decreased pectin electrostatic interactions (Kyomugasho, Willemsen, Christiaens, Van Loey, & Hendrickx, 2015).
Bioaccessibility and stability of plant secondary metabolites in pharmaceutical and food matrices
2023, Advances in Plant Biotechnology: In Vitro Production of Secondary Metabolites of Industrial InterestResearch Progress on Factors Affecting Intestinal Absorption and Metabolism of Carotenoids
2023, Journal of Chinese Institute of Food Science and TechnologyProtective effect of hierarchical emulsions stabilised by oil/water droplets in lutein delivery
2022, International Journal of Food Science and Technology