Original Research Article
Effects of pectins and sugars on β-carotene bioaccessibility in an in vitro simulated digestion model

https://doi.org/10.1016/j.jfca.2020.103537Get rights and content

Highlights

  • Lower pectin concentration caused higher β-carotene bioaccessibility.

  • Medium methoxyl pectin resulted in higher β-carotene bioaccessibility.

  • Sucrose could achieve the highest β-carotene bioaccessibility than other sugars.

  • Viscosity showed no marked difference in all the systems during digestion.

Abstract

There is lack of information about the effects of pectin and sugars on carotenoid delivery in a simple juice model system. Therefore, the effect of pectin and sugars on β-carotene bioaccessibility (CBA) and the characteristics of digestive fluids in juice model systems were studied. Carotenoid retention ratio (CRR) in the small intestine and the characteristics of digestive fluids, including color parameters and rheological properties, were investigated to gain insight into the mechanism that can alter carotenoid bioaccessibility. Results illustrated that higher pectin concentration, medium methoxyl pectin (MMP), and low methoxyl pectin (LMP) increased the initial apparent viscosity. However, there was no marked difference for the apparent viscosity of all systems in the stomach and small intestine phases. Generally, systems with sugars had higher CRR than those with pectin. Lower pectin concentration increased CBA. Systems with MMP had higher CBA than those containing high methoxyl pectin (HMP) and LMP; therefore, the effects of degree of methoxylation (DM) were not proportional to CBA. Among systems with different sugars, sucrose could achieve the highest CBA (4.59%). A comprehensive investigation of the effects of pectin and sugars on carotenoid delivery during digestion will be a theoretical guidance to improve nutritional qualities of juice products.

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 Osingle bondH 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, Cdouble bondO stretching vibration of methyl esters of carboxyl groups, and asymmetric Cdouble bondO 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)

  • M. Espinal-Ruiz et al.

    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.

    (2016)
  • M.L. Fishman et al.

    Characterization of the global structure of low methoxyl pectin in solution

    Food Hydrocoll.

    (2015)
  • T. Funami et al.

    Structural modifications of sugar beet pectin and the relationship of structure to functionality

    Food Hydrocoll.

    (2011)
  • F. Granado-Lorencio et al.

    Biomarkers of carotenoid bioavailability

    Food Res. Int.

    (2017)
  • A. Guerra et al.

    Relevance and challenges in modeling human gastric and small intestinal digestion

    Trends Biotechnol.

    (2012)
  • X. Hua et al.

    Rheological properties of natural low-methoxyl pectin extracted from sunflower head

    Food Hydrocoll.

    (2015)
  • S.J. Hur et al.

    In vitro human digestion models for food applications

    Food Chem.

    (2011)
  • K. Itoh et al.

    In situ gelling pectin formulations for oral drug delivery at high gastric pH

    Int. J. Pharm.

    (2007)
  • M. Kacurakova et al.

    FT-IR study of plant cell wall model compounds: pectic polyasaccharides and hemicelluloses

    Carbohydr. Polym.

    (2000)
  • D.S. Khramova et al.

    Pectin gelling in acidic gastric condition increases rheological properties of gastric digesta and reduces glycaemic response in mice

    Carbohydr. Polym.

    (2019)
  • G. Knockaert et al.

    Changes in β-carotene bioaccessibility and concentration during processing of carrot puree

    Food Chem.

    (2012)
  • R.E. Kopec et al.

    Recent advances in the bioaccessibility and bioavailability of carotenoids and effects of other dietary lipophiles

    J. Food Compos. Anal.

    (2018)
  • M.T.K. Kubo et al.

    Effect of high pressure homogenization (HPH) on the physical stability of tomato juice

    Food Res. Int.

    (2013)
  • C. Kyomugasho et al.

    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.

    (2015)
  • L. Lemmens et al.

    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.

    (2014)
  • X. Liu et al.

    Effects of high pressure homogenization on pectin structural characteristics and carotenoid bioaccessibility of carrot juice

    Carbohydr. Polym.

    (2019)
  • G.D. Manrique et al.

    FT-IR spectroscopy as a tool for measuring degree of methyl esterification in pectins isolated from ripening papaya fruit

    Postharvest Biol. Technol.

    (2002)
  • D. Mohnen

    Pectin structure and biosynthesis

    Curr. Opin. Plant Biol.

    (2008)
  • L. Mutsokoti et al.

    Carotenoid bioaccessibility and the relation to lipid digestion: a kinetic study

    Food Chem.

    (2017)
  • D.E. Ngouémazong et al.

    Quantifying structural characteristics of partially de-esterified pectins

    Food Hydrocoll.

    (2011)
  • O.F. O’Connell et al.

    Xanthophyll carotenoids are more bioaccessible from fruits than dark green vegetables

    Nutr. Res.

    (2007)
  • P. Palmero et al.

    Lycopene and β-carotene transfer to oil and micellar phases during in vitro digestion of tomato and red carrot based-fractions

    Food Res. Int.

    (2014)
  • P. Palmero et al.

    Role of structural barriers for carotenoid bioaccessibility upon high pressure homogenization

    Food Chem.

    (2016)
  • C.S. Pappas et al.

    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.

    (2004)
  • L. Salvia-Trujillo et al.

    Comparative study on lipid digestion and carotenoid bioaccessibility of emulsions, nanoemulsions and vegetable-based in situ emulsions

    Food Hydrocoll.

    (2019)
  • J.S.J. Santiago et al.

    Deliberate processing of carrot purées entails tailored serum pectin structures

    Innov. Food Sci. Emerg. Technol.

    (2016)
  • Cited by (8)

    • Gelling properties and interaction analysis of fish gelatin–low-methoxyl pectin system with different concentrations of Ca<sup>2+</sup>

      2020, LWT
      Citation 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 Interest
    • Research Progress on Factors Affecting Intestinal Absorption and Metabolism of Carotenoids

      2023, Journal of Chinese Institute of Food Science and Technology
    View all citing articles on Scopus
    View full text