Effect of biopolymer encapsulation on the digestibility of lipid and cholesterol oxidation products in beef during in vitro human digestion

doi:10.1016/j.foodchem.2014.06.009

Food Chemistry

Volume 166, 1 January 2015, Pages 254-260

https://doi.org/10.1016/j.foodchem.2014.06.009 Get rights and content

Highlights

•
Lipid digestibility of beef decreased with biopolymers encapsulation.
•
Lipid oxidation value of beef decreased with biopolymers encapsulation.
•
COPs of beef decreased with biopolymers encapsulation.

Abstract

In this study, beef patties were encapsulated with 3% chitosan, pectin, onion powder, or green tea powder and the beef patties were then passed through an in vitro human digestion model. The total lipid digestibility was lowest (p < 0.05) in beef patties encapsulated with chitosan and pectin after digestion in the small intestine. Thiobarbituric acid reactive substance (TBARS) values were significantly lower (p < 0.05) for beef patties encapsulated with chitosan and pectin, when compared with the control, after digestion in the small intestine. In contrast, the 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radical–scavenging activity was highest (p < 0.05) in beef patties encapsulated with onion powder and green tea powder after digestion in the small intestine. The total cholesterol oxidation product (COP) content was significantly lower (p < 0.05) in beef patties encapsulated with biopolymers than in the control after digestion in the small intestine.

Introduction

Because meat and meat products are some of the most important sources of dietary fat, modifying the lipid profile of such products could reduce their nutritional quality (Trindade, Mancini-Filho, & Villavicencio, 2010). The consumption of oxidised lipids or cholesterol plays an important role in both human health and meat quality. In general, many cholesterol oxidation products (COPs) are cytotoxic, atherogenic, mutagenic and carcinogenic (Hur, Min, Nam, Lee, & Ahn, 2013a). COPs are present in low amounts in raw foods of animal origin, but their concentration increases dramatically after high-temperature treatment in highly processed food products containing cooked meat, and after exposure to light, metals, natural sensitizers and oxygen (Boselli, Rodriguez-Estrada, Fedrizzi, & Caboni, 2009). Several studies have demonstrated the role of COPs in the rapid progression of coronary heart disease and atherosclerosis; COPs cause endothelial cell damage, which initiates a complex series of pathological changes that ultimately lead to plaque formation (Li and Mehta, 2005, Poli et al., 2009, Sevanian et al., 1995).

In addition, several studies have reported that biopolymers can be hypocholesterolemic in both animal and human models. It has been suggested that inhibiting cholesterol absorption in the gastrointestinal tract is a major mechanism underlying the cholesterol-lowering activity of biopolymers. The cholesterol-lowering effect of chitosan is one of its most extensively studied bioactivities (Anrakua et al., 2011). Data suggests that chitosan not only exerts cholesterol-lowering effects but also enhances resistance to oxidative stress (Anrakua et al., 2011). Santhosh, Sini, Anandan, and Mathew (2006) also reported that the administration of chitosan prevented the oxidation of hepatotoxic lipids in rats. Pectin has a gel-forming capacity and therefore binds to cholesterol and bile acids in the gut and promotes their excretion; thus, it exerts cholesterol-lowering effects (Mudgil & Barak, 2013). Marounek, Volek, Synytsya, and Copikova (2007) reported that pectin and other gel-forming polysaccharides increase viscosity and affect the processes of digestion and absorption in the small intestine. Several studies have reported the production of oxidised lipids and cholesterol in cooked meats. However, little is known about the effects of biopolymer encapsulation on lipid or cholesterol oxidation during digestion. Therefore, the aim of this study was to investigate the effects of biopolymer encapsulation on the digestibility of lipids and COPs in beef patties during in vitro human digestion.

Section snippets

Sample preparation

All experiments were performed using five replicates from 10 different patty samples. Chitosan (10% w/w) was dissolved in 90 g acetate buffer solution (100 mM acetic acid: sodium acetate, pH 3.0, 0–150 mM NaCl); 10% (w/w) pectin, onion powder and green tea powder, were dissolved in phosphate-buffered solution (2 M monobasic sodium phosphate and 2 M dibasic sodium phosphate, pH 7.0). All solutions were stirred for 12 h using a magnetic stirrer.

A beef chuck roll was ground twice through a 3-mm plate,

Results and discussion

The effect of biopolymer encapsulation on the total lipid digestibility of beef patties is shown in Fig. 1. After digestion in the mouth and stomach, there was no significant difference (p < 0.05) in the total lipid digestibility between all beef patty samples. However, the total lipid digestibility increased (p < 0.05) dramatically in all samples after digestion in the small intestine. Beef patties encapsulated with biopolymers showed significantly lower (p < 0.05) total lipid digestibility than the

Conclusions

In conclusion, this study demonstrated that lipid digestibility and COP production were increased by in vitro human digestion and that biopolymer encapsulation could reduce lipid oxidation and COP production. These effects were mainly due to biopolymers that not only have antioxidant activity, but also have lipid-, bile acid-, or cholesterol-binding effects. Several studies have demonstrated that a large proportion of the consumption of oxidised lipids or cholesterol was related directly to

Acknowledgements

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2012R1A1A1010007).

References (37)

D. Ahn et al.
Analysis of cholesterol oxides in egg yolk and turkey meat
Poultry Science
(1999)
M. Beysseriat et al.
Preliminary study of the influence of dietary fiber on the properties of oil-in-water emulsions passing through an in vitro human digestion model
Food Hydrocolloids
(2006)
E. Boselli et al.
Cholesterol photosensitised oxidation of beef meat under standard and modified atmosphere at retail conditions
Meat Science
(2009)
J.M. Broncano et al.
Effect of different cooking methods on lipid oxidation and formation of free cholesterol oxidation products (COPs) in Latissimus dorsi muscle of Iberian pigs
Meat Science
(2009)
M.E.A. Elhalwagy et al.
Prophylactic effect of green tea polyphenols against liver and kidney injury induced by fenitrothion insecticide
Pesticide Biochemistry and Physiology
(2008)
J. Folch et al.
A simple method for the isolation and purification of total lipids from animal tissues
Journal of Biological Chemistry
(1957)
S.J. Hur et al.
Influence of initial emulsifier type on microstructural changes occurring in emulsified lipids during in vitro digestion
Food Chemistry
(2009)
S.J. Hur et al.
Formation of cholesterol oxidation products (COPs) in animal products
Food Control
(2007)
C.-H. Jeong et al.
Antioxidant activities from the aerial parts of Platycodon grandiflorum
Food Chemistry
(2010)
D. Lairon et al.
Digestible and indigestible carbohydrates: Interactions with postprandial lipid metabolism
The Journal of Nutritional Biochemistry
(2007)

J.D. Lambert et al.

The antioxidant and pro-oxidant activities of green tea polyphenols: A role in cancer prevention

Archives of Biochemistry and Biophysics

(2010)

J.H. Meyer et al.

GI transit and absorption of solid food: Multiple effects of guar

The American Journal of Clinical Nutrition

(1988)

S.-K. Moon et al.

Quercetin exerts multiple inhibitory effects on vascular smooth muscle cells: Role of ERK1/2, cell-cycle regulation, and matrix metalloproteinase-9

Biochemical and Biophysical Research Communications

(2003)

D. Mudgil et al.

Composition, properties and health benefits of indigestible carbohydrate polymers as dietary fiber: A review

International Journal of Biological Macromolecules

(2013)

K. Murota et al.

Antioxidative flavonoid quercetin: Implication of its intestinal absorption and metabolism

Archives of Biochemistry and Biophysics

(2003)

G. Poli et al.

Cholesterol oxidation products in the vascular remodeling due to atherosclerosis

Molecular Aspects of Medicine

(2009)

G. Ranaldi et al.

The effect of chitosan and other polycations on tight junction permeability in the human intestinal Caco-2 cell line(1)

Journal of Nutritional Biochemistry

(2002)

S. Santhosh et al.

Effect of chitosan supplementation on antitubercular drugs-induced hepatotoxicity in rats

Toxicology

(2006)

Cited by (37)

Stabilized soy protein emulsion enriched with silicon and containing or not methylcellulose as novel technological alternatives to reduce animal fat digestion
2023, Food Research International
During the last decade, the consumption of animal saturated fat has been associated with an increased risk of chronic disease. Experience shows that changing the dietary habits of the population is a complicated and slow process, so technological strategies offer new possibilities for the development of functional foods. The present work is focused on studying the impact of using a food-grade non-ionic hydrocolloid (methylcellulose; MC) and/or the inclusion of silicon (Si) as a bioactive compound in pork lard emulsions stabilized with soy protein concentrate (SPC), on the structure, rheology, lipid digestibility and Si bioaccesibility during in vitro gastrointestinal digestion (GID). Four emulsions (SPC, SPC/Si, SPC/MC and SPC/MC/Si) were prepared with a final biopolymer (SPC and/or MC) concentration of 4% and 0.24% Si. The results showed a lower degree of lipid digestion in SPC/MC compared with SPC, specifically at the end of the intestinal phase. Moreover, Si partially reduced fat digestion only when incorporated into the SPC-stabilized emulsion, while this effect was lost in SPC/MC/Si. This was probably due to its retention inside the matrix emulsion, which resulted in lower bioaccesibility than in SPC/Si. Additionally, the correlation between the flow behavior index (n) and the lipid absorbable fraction was significant, suggesting that n can be a predictive marker of the extent of lipolysis. Concretely, our results revealed that SPC/Si and SPC/MC can be used as pork fat digestion reducers and thus, they can replace pork lard in the reformulation of animal products with potential health benefits.
Ca<sup>2+</sup>/pH-triggered gelation of Pickering emulsion in vitro digestion: Visualization and sustained-release performance
2023, Food Hydrocolloids
The emulsion gels transformed by Pickering emulsions have great potential as a novel platform for oral drug delivery. In this study, an innovative alginate-based fluorescent colloidal particle was synthesized by Ugi reaction with alginate and carbon dots, which can stabilize Pickering emulsion at the present of Ca²⁺. The Pickering emulsions were converted to emulsion gels during gastric digestion. The microstructure of interfacial film was characterized in situ with confocal laser scanning microscopy. In the process of simulated gastrointestinal digestion, phase conversion of the Pickering emulsion was observed directly in situ by an automatic living cell imaging system. The results showed that clear fluorescent interfacial films can be visualized after simulated oral digestion, and fluorescent spheres were appeared after gastrointestinal digestion, indicating that Pickering emulsions were transformed into emulsion gels. Moreover, results on cell viability and cell uptake showed that the Pickering emulsion had good biocompatibility, which could be taken up by Caco-2 cells and could sustain the release of the drug. The formation of emulsion gels delays the digestion rate and improves the stability of encapsulated curcumin (CUR). In particular, in situ visualization technique also has promising applications in the digestion process and cellular uptake.
Analysis of changes in antibiotic resistance in the human body using an in vitro digestion model incorporating human gut microbiota
2023, Heliyon
Residual antibiotics may affect human health by increasing challenges related to infection treatment due to antibiotic resistance development. Hence, determining whether residual antibiotics in the body can lead to antibiotic resistance is important. We developed a model to predict possible antibiotic resistance caused by residual antibiotics by simulating human digestion in vitro. Increased antibiotic resistance was found to be dependent on the digestion process. Ethical prediction of antibiotic resistance using fewer animals and no humans was possible by simulating the internal environment. Thus, preliminary studies to monitor antibiotic resistance that can affect human health may be safely conducted using this model.
Interactive effects of dietary cholesterol and phospholipids on growth and metabolism of juvenile swimming crab, Portunus trituberculatus
2022, Animal Feed Science and Technology
Citation Excerpt :
The results of present study demonstrated that dietary cholesterol and phospholipid supplementation could improve the antioxidant capacity of swimming crab. The antioxidant mechanism of dietary cholesterol and phospholipid were still unknown, but presumably, the antioxidant mechanism of dietary cholesterol is determined by cholesterol oxidation products (COPs), and the antioxidant mechanism of dietary phospholipid is due to amino groups and the cooperative effect of the hydroxy group, and those groups are all in the side chain (Tocher et al., 2008; Hur et al., 2015). Fatty acid compositions in tissues can partially or completely reflect the fatty acid composition of the experimental diets (Han et al., 2016; Sun et al., 2017).
Cholesterol and phospholipid play an important role in growth, molt and reproduction for crustaceans, although dietary optimum requirement of cholesterol and phospholipids has been determined for Portunus trituberculatus, but it is still unclear whether there was an interaction on each other. Therefore, an eight-week feeding trial was conducted to evaluate the interactive effects of dietary cholesterol and phospholipid levels on growth performance, fatty acid composition in hepatopancreas and the expression of genes related to cholesterol and phospholipid metabolism of Portunus trituberculatus. Six isonitrogenous and isolipid diets were formulated to contain two cholesterol levels (0 % and 0.5 %) and three phospholipid levels (0 %, 2 % and 4 %). The results indicated that specific growth rate (SGR) significantly increased with the increase of dietary phospholipid levels, however, there were no interactive effects between dietary cholesterol and phospholipid on percent weight gain (PWG) and SGR (P > 0.05). The concentration of total-cholesterol (T-CHO) and triacylglycerol (TAG) in hemolymph significantly affected by the interaction between cholesterol and phospholipid (P < 0.05), crabs fed diets with 0.5 % cholesterol supplementation had higher low-density lipoprotein cholesterol (LDL-C) concentration in hemolymph than those fed diets without cholesterol supplementation regardless of phospholipid supplementation (P < 0.05). TAG and LDL-C concentration in hepatopancreas were significantly affected by the interaction between cholesterol and phospholipid (P < 0.05), crabs fed diets with 0.5 % cholesterol supplementation had significantly higher T-CHO and LDL-C concentration in hepatopancreas than those fed diets without cholesterol supplementation (P < 0.05). There was a significant interaction between dietary cholesterol and phospholipid on activity of catalase (CAT) and the concentration of glutathione (GSH) and malondialdehyde (MDA) in hepatopancreas (P < 0.05), and crabs fed diets with cholesterol supplementation had higher superoxide dismutase (SOD) and total antioxidant capacity (T-AOC) in hepatopancreas than those fed diets without cholesterol supplementation (P < 0.05). Moreover, EPA, LC-PUFA, n-3 PUFA, n-3/n-6 PUFA and DHA/EPA in hepatopancreas were significantly affected by the interaction between dietary cholesterol and phospholipid (P < 0.05). The expression of adenosine triphosphate binding cassette transporter G1 (abcg1), C-type 1 class Niemann-Pick protein (npc1), scavenger receptor B (srb) and low-density lipoprotein receptor (ldlr) were up-regulated by dietary cholesterol and phospholipid levels (P < 0.05). In conclusion, the results indicated that dietary appropriate cholesterol and phospholipid levels could significantly improve growth performance and promote cholesterol metabolism.
Effect of age-related in vitro human digestion with gut microbiota on antioxidative activity and stability of vitamins
2022, LWT
Citation Excerpt :
All solutions were filtered with a 0.22 μm membrane filter before measuring their antioxidant activities or injecting them into the HPLC column. Previous studies have reported changes in the digestibility and bioaccessibility of foods and pharmaceuticals during gastric intestinal digestion using an in vitro digestion model (Hur, Lee, & Lee, 2015; Hur, Lim, Decker, & McClements, 2011; Lee, Kim, Yoon, & Hur, 2018; Lee, Lee, & Hur, 2021). Unlike the previous in vitro digestion procedures that did not consider digestion condition by ages, the in vitro human digestion procedure in this study considered the in vitro digestion conditions depends on ages including adults and elderly individuals: motility, amount of digestive enzymes, and composition ratio of gut microbiota (Fig. 1).
We aimed to determine the effect of age (adults vs elderly) on the antioxidant activity, digestibility, and stability of vitamins (vitamin C, vitamin B₆, and vitamin B₁₂) during in vitro human digestion. Antioxidant activity and digestibility of vitamin C were not influenced by age, digestion phase, or the gut microbiota, though its stability decreased in the presence of the gut microbiota. The activities of vitamins B₆ and B₁₂ differed by age, digestion phase, and the presence of the gut microbiota. Notably, the antioxidant activity and stability of vitamin B₆ were reduced under low pH and gut microbiota, respectively. Vitamin B₁₂ levels increased with age and in the presence of the gut microbiota. Together, vitamin C showed as a strong antioxidant regardless of age. Further, these findings could help develop strategies to increase the bioavailability of the vitamin B₆ and B₁₂ in the human body by accounting for age and human digestive conditions.
Alternative experimental approaches to reduce animal use in biomedical studies
2022, Journal of Drug Delivery Science and Technology
We review experimental approaches that can be used instead of in vivo studies involving vertebrate animal models and human clinical trials. The existing alternative experimental approaches were classified as in vitro digestion models, invertebrate models, organs-on-a-chip, in silico models, and toxicity tests. In vitro models mimicking the digestive system may help assess pharmacokinetics without the use of animal models. In addition, invertebrate models can be easily applied in genetics research and toxicity assays owing to their advantages, such as effortless handling, low cost, small size, and simple anatomy. Organs-on-a-chip and in silico models can simulate the physiological activity in biological organs and can be useful for monitoring human diseases. Moreover, these alternative models can be adopted as screening platforms to assess candidate drugs during the preclinical phase through rapid and simple monitoring of physiological response to drugs. Therefore, these alternative experimental approaches can contribute to ethical reduction of animal use in biological studies.

View all citing articles on Scopus

View full text

Effect of biopolymer encapsulation on the digestibility of lipid and cholesterol oxidation products in beef during in vitro human digestion

Highlights

Abstract

Introduction

Section snippets

Sample preparation

Results and discussion

Conclusions

Acknowledgements

Poultry Science

Food Hydrocolloids

Meat Science

Meat Science

Pesticide Biochemistry and Physiology

Journal of Biological Chemistry

Food Chemistry

Food Control

Food Chemistry

The Journal of Nutritional Biochemistry

Archives of Biochemistry and Biophysics

The American Journal of Clinical Nutrition

Biochemical and Biophysical Research Communications

International Journal of Biological Macromolecules

Archives of Biochemistry and Biophysics

Molecular Aspects of Medicine

Journal of Nutritional Biochemistry

Toxicology