Factors affecting the bioaccessibility of β-carotene in lipid-based microcapsules: Digestive conditions, the composition, structure and physical state of microcapsules
Graphical abstract
Introduction
β-Carotene is one of the most important carotenoids and can be used as a pigment in the food industry (Sáiz-Abajo, González-Ferrero, Moreno-Ruiz, Romo-Hualde, & González-Navarro, 2013). In the past decades, β-carotene has been studied widely mainly due to its provitamin-A activity and strong antioxidant activity. It has been demonstrated that β-carotene may help to reduce the risk of developing chronic diseases (e.g. cancer, cardiovascular diseases) and age related diseases (Liang et al., 2013b, Saini et al., 2015). Besides, the deficiency of β-carotene may result in vision-disability in human and increase mortality due to a weakened innate immunity and adaptive immunity (Saini et al., 2015). Therefore, β-carotene can be used as a promising functional food ingredient and it’s important to take proper amounts of β-carotene from diets, including vegetables (e.g. yellow pepper, carrots) and fruits (e.g. mangoes).
However, the bioavailability of β-carotene from plants is usually poor and the absorption may be below 10% (Boileau, Moore, & J.W. Erdman, 1999), which is mainly attributed to the resistance of carotene–protein complexes and the plant cell walls to achieve adequate release of β-carotene (Erdman et al., 1993, Rein et al., 2013). The low bioavailability from natural sources has led to the development of extraction and isolation of β-carotene for the delivery as supplements or in fortified food (Donhowe & Kong, 2014). Pure β-carotene is easy to be degraded due to its sensitivity to oxygen, light, and temperature. Encapsulating β-carotene into appropriate delivery vehicles is a useful method to protect β-carotene from degradation. Lipid-based microcapsules, consisting of a lipophilic core (oil phase) and a shell of surface active material (interfacial layer) (Fig. 1), are the main delivery systems for protecting lipophilic β-carotene. Common lipid-based microcapsules include emulsions [e.g. conventional emulsions (Salvia-Trujillo et al., 2013, Yi et al., 2014c), nanoemulsions (Qian et al., 2012a, Qian et al., 2012b, Rao et al., 2013, Yi et al., 2014c), microemulsions (Ariviani et al., 2015, Roohinejad et al., 2015), multilayer emulsions (Liu et al., 2016, Mao et al., 2013) and Pickering emulsions (Liu and Tang, 2016, Shao and Tang, 2016)], hydrogel particles (Mun et al., 2015a, Mun et al., 2015b, Mun et al., 2016, Zhang et al., 2016b), nanoparticles (Yi et al., 2014b, Yi et al., 2014a, Yi et al., 2015a), liposomes (Moraes et al., 2013, Tan et al., 2016, Tan et al., 2014a, Toniazzo et al., 2014), water dispersible powders (Donhowe et al., 2014, Guadarrama-Lezama et al., 2012, Liang et al., 2013a), etc. It has been proved that lipid-based microcapsules would be promising vehicles which could improve the bioavailability of β-carotene. For example, the water dispersible powder has been shown to enhance the absorption of β-carotene in the human body (Thürmann et al., 2002, Zhou et al., 1996). The administration of β-carotene water dispersible powder produced higher blood β-carotene concentration (3.84 ± 0.60 μmol/L, dose: 7.2 mg/d) in comparison to an intake of β-carotene from natural sources (0.42 ± 0.33 μmol/L, dose: 6 mg/d). In the last two decades, food scientists are striving hard to develop novel lipid-based microcapsules to enhance β-carotene bioavailability.
In order to design β-carotene lipid-based microcapsules with high bioavailability, factors that affect the bioavailability of β-carotene must be understood. Similar with most nutraceuticals, β-carotene bioavailability is influenced by two categories of factors: host-related factors and dietary factors (Gibson, 2007). In the human body, host-related factors mainly refer to the gastrointestinal tract (GIT) conditions, e.g. pH, enzymes, biosurfactants, mucin, ions, etc. Generally, their effects on nutraceuticals bioavailability are often ignored during in vivo studies (Gibson, 2007). However, their influence cannot be neglected during in vitro trials. During the development of β-carotene fortifiers, quick and cost-efficient in vitro digestion studies are often carried out for estimating β-carotene bioaccessibility before subsequent in vivo studies. From the recent reports, it can be found that a variety of GIT conditions of in vitro digestion models influence the bioaccessibility of β-carotene significantly. Therefore, digestive conditions should be set reasonably and close to the true physicochemical conditions in the human body as far as possible, thus providing reliable results that can be comparable to those from in vivo studies. To achieve the goal above, it is required to understand the mechanisms of the influence of various digestive conditions on the bioaccessibility of β-carotene. The dietary factors of carotenoids include the composition and structure of the food matrix, the state of carotenoids (dissolved or crystallized) and other food ingredients (e.g. fat, dietary fiber, minerals) ingested within meals. The influence of dietary factors on the bioavailability of botanical carotenoids has been reviewed by van het Hof et al. (2000) and Yonekura and Nagao (2007). However, the influence of dietary factors on the bioavailability of carotenoids in the lipid-based microcapsule has not been reviewed yet. The influence of characteristics of delivery systems on the bioavailability of β-carotene in lipid-based microcapsules has been widely investigated in recent years. The purpose of this review is to summarize the current advances in the influence of digestive conditions as well as the composition, structure and physical state of lipid-based microcapsules on the bioaccessibility of β-carotene in during in vitro digestion.
Comprehension of β-carotene absorption is the starting point for understanding the influence mechanisms of factors on β-carotene bioavailability. Therefore, the absorption of β-carotene in lipid-based microcapsules is described in the first section. In addition, the most widely used in vitro digestion models for estimating the bioaccessibility of β-carotene are also concluded in this section. The influence of simulated digestive conditions, the composition of lipid-based microcapsules, the structure of lipid-based microcapsules and the physical state of lipid-based microcapsules on the bioaccessibility of β-carotene during in vitro digestion studies have been discussed in the second, third, fourth and fifth sections, respectively. Simultaneously, the possible mechanisms involved are elucidated.
Section snippets
Mechanical and thermal process
Prior to intestinal absorption, β-carotene must first be released from food matrix. Release depends on the extent of structural degradation of the food matrix, which may be aided by thermal or mechanical processing prior to digestion (Parker, 1996, Yeum and Russell, 2002). For botanical β-carotene, it has been proven by several studies that the physical disruption by means of heat or mechanical processing improves release and absorption (Hedren et al., 2002, Hu et al., 2000, Lemmens et al., 2010
The effect of digestive conditions on the bioaccessibility of β-carotene in lipid-based microcapsules
When evaluating the β-carotene bioaccessibility by in vitro digestion models, it is important to choose digestive conditions carefully since their discrepancy may lead to great difference in results. In this section, we highlight the current findings in the effects of the digestive conditions on the digestion and the bioaccessibility of β-carotene in lipid-based microcapsules.
The effect of the composition of lipid-based microcapsules on the bioaccessibility of β-carotene
β-Carotene lipid-based microcapsules consist of core material (i.e. β-carotene) in a lipophilic shells or carriers (oil phase, e.g. triglycerides, liposomes etc.) surrounded by a shell of surface active material (interfacial layer) (Fig. 1). Similar to dietary factors on the bioavailability of β-carotene from natural sources, the characteristics of the composition of the delivery systems play critical roles in the biological fate of β-carotene encapsulated in lipid-based microcapsules. In this
The effect of the structure of lipid-based microcapsules on the bioaccessibility of β-carotene
The structure of lipid-based microcapsules determines the disruption and digestion of delivery systems and the release of β-carotene within the GIT. In this section, we highlight the most important structural characteristics of lipid-based microcapsules that can regulate the bioaccessibility of encapsulated β-carotene.
The effect of the physical state of lipid-based microcapsules on the bioaccessibility of β-carotene
According to the physical state, lipid-based microcapsules can be divided into 3 types: liquid, semi-solid and solid. Liquid formulations include emulsions, liposomes, micelles, etc.; semi-solid formulations include gels, hydrogel beads, etc.; and solid formulations include water-dispersible powders, etc.
Physical state plays a significant role in the digestion time and disintegration degree of foods. Generally, liquid foods don’t undergo the mastication in the mouth while semi-solid and solid
Conclusion
There is a growing trend in developing β-carotene supplements with high bioavailability, and lipid-based microcapsules could be promising vehicles. This article provides an overview of the absorption of β-carotene in lipid-based microcapsules, and reviews in vitro digestion models that have been developed to evaluate the bioaccessibility of β-carotene. Attention should be paid to the simulated digestive conditions since they have been proved to affect the results significantly. We put special
Acknowledgements
This research was supported by the National Natural Science Foundation of China (No. 31401533, 31571891), the National Key R&D Program of China (2016YFD0400801), and the National 125 Program 2013AA102207. The research is also supported by program of “Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province”.
References (149)
- et al.
Development and evaluation of lipid nanocarriers for quercetin delivery: A comparative study of solid lipid nanoparticles (SLN), nanostructured lipid carriers (NLC), and lipid nanoemulsions (LNE)
LWT-food Science and Technology
(2014) - et al.
Bioavailability of β-carotene isomers from raw and cooked carrots using an in vitro digestion model coupled with a human intestinal Caco-2 cell model
Food Research International
(2010) - et al.
Divalent minerals decrease micellarization and uptake of carotenoids and digestion products into Caco-2 cells
The Journal of Nutrition
(2011) - et al.
Dietary and host-related factors influencing carotenoid bioaccessibility from spinach (spinacia oleracea)
Food Chemistry
(2011) - et al.
Carotenoids in biological emulsions: Solubility, surface-to-core distribution, and release from lipid droplets
Journal of Lipid Research
(1996) - et al.
Chylomicron β-carotene and retinyl palmitate responses are dramatically diminished when men ingest β-carotene with medium-chain rather than long-chain triglycerides
The Journal of Nutrition
(1998) Importance of phospholipids, pancreatic phospholipase A2, and fatty acid for the digestion of dietary fat: In vitro experiments with the porcine enzymes
Gastroenterology
(1980)- et al.
Characterization of mucin–lipid droplet interactions: Influence on potential fate of fish oil-in-water emulsions under simulated gastrointestinal conditions
Food Hydrocolloids
(2016) Barrier properties of mucus
Advanced Drug Delivery Reviews
(2009)- et al.
Effect of divalent minerals on the bioaccessibility of pure carotenoids and on physical properties of gastro-intestinal fluids
Food Chemistry
(2016)
All-trans β-carotene appears to be more bioavailable than 9-cis or 13-cis β-carotene in gerbils given single oral doses of each isomer
The Journal of Nutrition
Characterization and in vitro bioavailability of β-carotene: Effects of microencapsulation method and food matrix
LWT-food Science and Technology
Carotenoid uptake and secretion by CaCo-2 cells β-carotene isomer selectivity and carotenoid interactions
Journal of Lipid Research
Impact of pectin properties on lipid digestion under simulated gastrointestinal conditions: Comparison of citrus and banana passion fruit (Passiflora tripartita var. mollissima) pectins
Food Hydrocolloids
In vitro micellarization and intestinal cell uptake of cis isomers of lycopene exceed those of all-trans lycopene
The Journal of Nutrition
Computational modeling of gastric digestion and the role of food material properties
Trends in Food Science & Technology
Discrimination in absorption or transport of beta-carotene isomers after oral supplementation with either all-trans-or 9-cis-beta-carotene
The American Journal of Clinical Nutrition
Preparation and characterization of non-aqueous extracts from chilli (Capsicum annuum L.) and their microencapsulates obtained by spray-drying
Journal of Food Engineering
What do we (need to) know about the kinetic properties of nanoparticles in the body?
Regulatory Toxicology and Pharmacology
Dietary factors that affect the bioavailability of carotenoids
The Journal of Nutrition
Investigation into the in vitro release properties of β-carotene in emulsions stabilized by different emulsifiers
LWT-food Science and Technology
Intestinal absorption of β-carotene ingested with a meal rich in sunflower oil or beef tallow: Postprandial appearance in triacylglycerol-rich lipoproteins in women
The American Journal of Clinical Nutrition
Role of calcium and calcium-binding agents on the lipase digestibility of emulsified lipids using an in vitro digestion model
Food Hydrocolloids
Serum retinol concentrations in children are affected by food sources of beta-carotene, fat intake, and anthelmintic drug treatment
The American Journal of Clinical Nutrition
Chitosan nanoparticles as delivery systems for doxorubicin
Journal of Controlled Release
Liver accumulation of soluble all-trans or 9-cis β-carotene in rats and chicks
Comparative Biochemistry and Physiology Part A: Physiology
Effect of relative humidity on the store stability of spray-dried beta-carotene nanoemulsions
Food Hydrocolloids
Control of lipase digestibility of emulsified lipids by encapsulation within calcium alginate beads
Food Hydrocolloids
Factors affecting lipase digestibility of emulsified lipids using an in vitro digestion model: Proposal for a standardised pH-stat method
Food Chemistry
Inhibition of lipase-catalyzed hydrolysis of emulsified triglyceride oils by low-molecular weight surfactants under simulated gastrointestinal conditions
European Journal of Pharmaceutics and Biopharmaceutics
Effects of calcium on lipid digestion in nanoemulsions stabilized by modified starch: Implications for bioaccessibility of β-carotene
Food Hydrocolloids
Soy glycinin as food-grade Pickering stabilizers: Part. III. Fabrication of gel-like emulsions and their potential as sustained-release delivery systems for β-carotene
Food Hydrocolloids
Utilization of interfacial engineering to improve physicochemical stability of β-carotene emulsions: Multilayer coatings formed using protein and protein–polyphenol conjugates
Food Chemistry
Influence of lipolysis on drug absorption from the gastro-intestinal tract
Advanced Drug Delivery Reviews
The role of bile salts in digestion
Advances in Colloid and Interface Science
Edible lipid nanoparticles: Digestion, absorption, and potential toxicity
Progress in Lipid Research
Encapsulation, protection, and release of hydrophilic active components: Potential and limitations of colloidal delivery systems
Advances in Colloid and Interface Science
Structured emulsion-based delivery systems: Controlling the digestion and release of lipophilic food components
Advances in Colloid and Interface Science
Human digestive and metabolic lipases—a brief review
Journal of Molecular Catalysis B: Enzymatic
Control of β-carotene bioaccessibility using starch-based filled hydrogels
Food Chemistry
Control of lipid digestion and nutraceutical bioaccessibility using starch-based filled hydrogels: Influence of starch and surfactant type
Food Hydrocolloids
Influence of methylcellulose on attributes of β-carotene fortified starch-based filled hydrogels: Optical, rheological, structural, digestibility, and bioaccessibility properties
Food Research International
Carotenoid bioaccessibility and the relation to lipid digestion: A kinetic study
Food Chemistry
Effects of cooking on the profile and micellarization of 9-cis-, 13-cis-and all-trans-β-carotene in green vegetables
Food Research International
Nanoemulsion delivery systems: Influence of carrier oil on β-carotene bioaccessibility
Food Chemistry
Physical and chemical stability of β-carotene-enriched nanoemulsions: Influence of pH, ionic strength, temperature, and emulsifier type
Food Chemistry
Characterization of colloidal structures during intestinal lipolysis using small-angle neutron scattering
Journal of Colloid and Interface Science
The influence of guar gum on lipid emulsion digestion and beta-carotene bioaccessibility
Characterization and chemical stability evaluation of β-carotene microemulsions prepared by spontaneous emulsification method using VCO and palm oil as oil phase
International Food Research Journal
Toward the establishment of standardized in vitro tests for lipid-based formulations. 5. lipolysis of representative formulations by gastric lipase
Pharmaceutical Research
Cited by (0)
- 1
These authors contributed equally to this work.