Elsevier

Food Hydrocolloids

Volume 77, April 2018, Pages 187-203
Food Hydrocolloids

Factors affecting the bioaccessibility of β-carotene in lipid-based microcapsules: Digestive conditions, the composition, structure and physical state of microcapsules

https://doi.org/10.1016/j.foodhyd.2017.09.034Get rights and content

Highlights

  • Metabolism of β-carotene in lipid-based microcapsules has been proposed.

  • Effects of simulated digestive conditions on β-carotene bioaccessibility have been summarized.

  • Effects of composition of lipid-based microcapsules on β-carotene bioacessibility have been reviewed.

  • Effects of structure of lipid-based microcapsules on β-carotene bioaccessibility have been described.

  • Effects of physical state of lipid-based microcapsules on β-carotene bioaccessibility have been summarized.

Abstract

β-Carotene is considered as a promising functional food ingredient. However, the application of β-carotene is limited by its low solubility in water, sensitivity to oxygen, light and temperature, and low oral bioavailability. Lipid-based microcapsules can be used as delivery systems to improve the bioavailability of β-carotene in addition to encapsulation and protection. This review begins by summarizing the absorption of β-carotene in lipid-based microcapsules and in vitro digestion models used in the study of β-carotene bioaccessibility. It then puts the special emphasis on the effects and potential mechanisms of simulated digestive conditions (e.g. digestive enzymes, surface-active components, mineral ions, pH, mucin, flow profiles and mechanical forces), the composition (e.g. β-carotene, oil phase, interfacial layer and gel matrix), structure (e.g. particle size, particle charge) and physical state of lipid-based microcapsules on the bioaccessibility of β-carotene during in vitro digestion. The studies presented in this review show that both the simulated digestive conditions and the characteristics (composition and structure) of lipid-based microcapsules affect the β-carotene bioaccessibility by impacting the structure stability of delivery systems, digestion of lipid and the transfer of β-carotene to mixed micelles. It can be concluded that appropriate digestive parameters should be chosen depending on the nature of the sample being tested, and that the bioaccessibility of β-carotene can be regulated by rational selection of the composition and structure fabrication of microcapsules. Such information can be used for the design of digestion models and development of β-carotene supplements with high bioavailability.

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)

  • D.M. Deming et al.

    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

    (2002)
  • E.G. Donhowe et al.

    Characterization and in vitro bioavailability of β-carotene: Effects of microencapsulation method and food matrix

    LWT-food Science and Technology

    (2014)
  • A. During et al.

    Carotenoid uptake and secretion by CaCo-2 cells β-carotene isomer selectivity and carotenoid interactions

    Journal of Lipid Research

    (2002)
  • 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 Hydrocolloids

    (2016)
  • M.L. Failla et al.

    In vitro micellarization and intestinal cell uptake of cis isomers of lycopene exceed those of all-trans lycopene

    The Journal of Nutrition

    (2008)
  • M.J. Ferrua et al.

    Computational modeling of gastric digestion and the role of food material properties

    Trends in Food Science & Technology

    (2011)
  • J.M. Gaziano et al.

    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

    (1995)
  • A.Y. Guadarrama-Lezama et al.

    Preparation and characterization of non-aqueous extracts from chilli (Capsicum annuum L.) and their microencapsulates obtained by spray-drying

    Journal of Food Engineering

    (2012)
  • W.I. Hagens et al.

    What do we (need to) know about the kinetic properties of nanoparticles in the body?

    Regulatory Toxicology and Pharmacology

    (2007)
  • K.H. van het Hof et al.

    Dietary factors that affect the bioavailability of carotenoids

    The Journal of Nutrition

    (2000)
  • Z. Hou et al.

    Investigation into the in vitro release properties of β-carotene in emulsions stabilized by different emulsifiers

    LWT-food Science and Technology

    (2014)
  • X. Hu et al.

    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

    (2000)
  • M. Hu et al.

    Role of calcium and calcium-binding agents on the lipase digestibility of emulsified lipids using an in vitro digestion model

    Food Hydrocolloids

    (2010)
  • F. Jalal et al.

    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

    (1998)
  • K.A. Janes et al.

    Chitosan nanoparticles as delivery systems for doxorubicin

    Journal of Controlled Release

    (2001)
  • G. Levin et al.

    Liver accumulation of soluble all-trans or 9-cis β-carotene in rats and chicks

    Comparative Biochemistry and Physiology Part A: Physiology

    (1994)
  • R. Liang et al.

    Effect of relative humidity on the store stability of spray-dried beta-carotene nanoemulsions

    Food Hydrocolloids

    (2013)
  • Y. Li et al.

    Control of lipase digestibility of emulsified lipids by encapsulation within calcium alginate beads

    Food Hydrocolloids

    (2011)
  • Y. Li et al.

    Factors affecting lipase digestibility of emulsified lipids using an in vitro digestion model: Proposal for a standardised pH-stat method

    Food Chemistry

    (2011)
  • Y. Li et al.

    Inhibition of lipase-catalyzed hydrolysis of emulsified triglyceride oils by low-molecular weight surfactants under simulated gastrointestinal conditions

    European Journal of Pharmaceutics and Biopharmaceutics

    (2011)
  • Q. Lin et al.

    Effects of calcium on lipid digestion in nanoemulsions stabilized by modified starch: Implications for bioaccessibility of β-carotene

    Food Hydrocolloids

    (2017)
  • F. Liu et al.

    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

    (2016)
  • F. Liu et al.

    Utilization of interfacial engineering to improve physicochemical stability of β-carotene emulsions: Multilayer coatings formed using protein and protein–polyphenol conjugates

    Food Chemistry

    (2016)
  • K.J. MacGregor et al.

    Influence of lipolysis on drug absorption from the gastro-intestinal tract

    Advanced Drug Delivery Reviews

    (1997)
  • J. Maldonado-Valderrama et al.

    The role of bile salts in digestion

    Advances in Colloid and Interface Science

    (2011)
  • D.J. McClements

    Edible lipid nanoparticles: Digestion, absorption, and potential toxicity

    Progress in Lipid Research

    (2013)
  • D.J. McClements

    Encapsulation, protection, and release of hydrophilic active components: Potential and limitations of colloidal delivery systems

    Advances in Colloid and Interface Science

    (2015)
  • D.J. McClements et al.

    Structured emulsion-based delivery systems: Controlling the digestion and release of lipophilic food components

    Advances in Colloid and Interface Science

    (2010)
  • M. Mukherjee

    Human digestive and metabolic lipases—a brief review

    Journal of Molecular Catalysis B: Enzymatic

    (2003)
  • S. Mun et al.

    Control of β-carotene bioaccessibility using starch-based filled hydrogels

    Food Chemistry

    (2015)
  • S. Mun et al.

    Control of lipid digestion and nutraceutical bioaccessibility using starch-based filled hydrogels: Influence of starch and surfactant type

    Food Hydrocolloids

    (2015)
  • S. Mun et al.

    Influence of methylcellulose on attributes of β-carotene fortified starch-based filled hydrogels: Optical, rheological, structural, digestibility, and bioaccessibility properties

    Food Research International

    (2016)
  • L. Mutsokoti et al.

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

    Food Chemistry

    (2017)
  • L. O’Sullivan et al.

    Effects of cooking on the profile and micellarization of 9-cis-, 13-cis-and all-trans-β-carotene in green vegetables

    Food Research International

    (2010)
  • C. Qian et al.

    Nanoemulsion delivery systems: Influence of carrier oil on β-carotene bioaccessibility

    Food Chemistry

    (2012)
  • C. Qian et al.

    Physical and chemical stability of β-carotene-enriched nanoemulsions: Influence of pH, ionic strength, temperature, and emulsifier type

    Food Chemistry

    (2012)
  • O. Rezhdo et al.

    Characterization of colloidal structures during intestinal lipolysis using small-angle neutron scattering

    Journal of Colloid and Interface Science

    (2017)
  • J. Amyoony

    The influence of guar gum on lipid emulsion digestion and beta-carotene bioaccessibility

    (2014)
  • S. Ariviani et al.

    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

    (2015)
  • J.-C. Bakala-N’Goma et al.

    Toward the establishment of standardized in vitro tests for lipid-based formulations. 5. lipolysis of representative formulations by gastric lipase

    Pharmaceutical Research

    (2015)
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