Elsevier

Food Hydrocolloids

Volume 118, September 2021, 106752
Food Hydrocolloids

Fabricating hydrophilic particles with oleic acid and bovine serum albumin to improve the dispersibility and bioaccessibility of fucoxanthin in water

https://doi.org/10.1016/j.foodhyd.2021.106752Get rights and content

Highlights

  • OA and BSA can form stable hydrophilic particles when OA/BSA molar ratios are 13:1 to 30:1.

  • The embedding rate of OA-BSA particles to fucoxanthin (FUCO) was over 98%.

  • The FUCO-OA-BSA particles exhibited good water dispersibility.

  • The bioaccessibility of FUCO was over 60% after encapsulation with OA-BSA particles.

  • The OA–BSA increased serum and hepatic levels of FUCO by 6.66 and 4.39 times, respectively.

Abstract

Biomacromolecules and dietary lipids are known to efficiently improve the hydrophilicity and intestinal absorption, respectively, of carotenoids. In this work, to simultaneously promote the dispersibility and bioaccessibility of fucoxanthin (FUCO) in a hydrophilic environment, a water-soluble delivery carrier was constructed using oleic acid (OA) and bovine serum albumin (BSA), based on the method of pH-switchable molecular self-assembly. The hydrophilic OA–BSA particles were prepared under the optimized conditions (pH shifting from 11.0 to 7.0, BSA 2.0 mg/mL, and OA/BSA molar ratios 13:1 to 30:1), with the particle sizes ranging from 120.0 nm to 160.0 nm and the Zeta-potential ranging from −35.0 mV to −45.0 mV. The fabricated OA–BSA particles were subsequently employed to entrap FUCO in water. When the FUCO/BSA molar ratio was 10:1, the transparent aqueous dispersions of the FUCO–OA–BSA complexes, with particle sizes <200.0 nm and Zeta-potentials over −30.0 mV, were obtained and a FUCO embedding rate of more than 96% was achieved. Furthermore, Fourier transform infrared spectroscopy and scanning electron microscopy results confirmed that the FUCO was completely encapsulated within the OA–BSA particles and that spherical particles with smooth surfaces were formed. In addition, in vitro simulated gastro-intestinal digestion revealed that the bioaccessibility of the FUCO reached more than 60% after its encapsulation within the OA–BSA particles. The in vivo test further confirmed that the OA–BSA particles could increase serum and hepatic responsive levels of FUCO by 6.66 and 4.39 times, respectively. These findings suggest that fatty acid-protein particles may be suitable for the hydrophilic delivery carriers of hydrophobic nutrients.

Introduction

Fucoxanthin (FUCO) (C42H58O6), a natural product of carotenoids, is abundant in brown algae and some microalgae (Dai et al., 2014; Liu, Li, Chen, Wan, & Wang, 2020). The many reported health benefits of FUCO include protection against obesity, diabetes, cancer, oxidation of the body, vascularization and inflammation (Miyashita & Hosokawa, 2017; Ravi, Kurrey, Manabe, Sugawara, & Baskaran, 2018; Rehman et al., 2020). However, FUCO is susceptible to light, oxygen, pH and thermal degradation because of its multiple conjugated double bonds (Quan, Kim, Pan, & Chung, 2013). Furthermore, as with other lipophilic carotenoids, the use of FUCO in the food industry is restricted due to its low water-solubility and bioavailability (Dai et al., 2014; Quan et al., 2013).

To overcome these obstacles, a number of encapsulation techniques have been successfully proposed (Rehman et al., 2020). Protein-based carriers are widely recognized as one of the most promising encapsulation technologies for the delivery of lipid soluble components, due to their biodegradation, biocompatibility and renewability (Tang, 2020), and there is significant evidence that complexation with protein can effectively improve the water dispersibility, stability and, even, the bioactivities of liposoluble constituents (Elzoghby, Samy, & Elgindy, 2012; Tang, 2020). For instance, compared with curcumin alone, the water solubility, antioxidant and anti-microbiological qualities of gelatin-encapsulated curcumin were significantly enhanced (Gómez-Estaca, Balaguer, López-Carballo, Gavara, & Hernández-Muñoz, 2017). In another study, when lutein-loaded emulsions were prepared with whey protein isolate, it was found that the lutein had decreased by only 4% after storage at 4 °C for four weeks (Zhao, Shen, & Guo, 2018). In addition, FUCO encapsulated by protein was found to exhibit higher levels of stability, antioxidant activity and anti-proliferative activity (Li et al., 2018). However, low bioavailability remains a challenge in liposoluble nutrients (Liu, Huang, et al., 2020).

An increasing number of studies have shown that lipid-based systems can effectively promote the bioavailability of liposoluble nutritional components (Chen, Liang, Yokoyama, et al., 2020). Hitherto, several lipid-based systems have been developed, such as dietary lipids, lipid nanoparticles, microemulsions and nanoemulsions (Shishir, Xie, Sun, Zheng, & Chen, 2018). Plasma lutein levels delivered with wheat germ oil were reportedly four-fold higher than those of the control group (Gorusupudi & Baskaran, 2013), while the oral bioavailability of astaxanthin in humans has been enhanced four times by the incorporation of diglycerol monooelate and glycerol dioleate and polysorbate 80 (Mercke Odeberg, Lignell, Pettersson, & Höglund, 2003). In addition, previous studies have shown that the bioavailability of carotenoid can exceed 70% after encapsulation within linolenic oil nanoemulsion (Sotomayor-Gerding et al., 2016). Therefore, it seems clear that lipids do play a significant role in promoting the intestinal absorption of fat-soluble substances.

Proteins have been proven to interact with lipids and their complexes can improve the water dispersibility or bioavailability of hydrophobic molecules (Gaber et al., 2017). Moreover, proteins and lipids can form emulsions to encapsulate hydrophobic molecules by high-pressure homogenization (Rostamabadi, Falsafi, & Jafari, 2019). For example, when lycopene-loaded nanoemulsions were prepared by high-pressure homogenization using sesame oil as the oil phase and lactoferrin as the emulsifier, the lycopene nanoemulsion exhibited greater stability and the lycopene bioaccessibility was found to be approximately 25% (Zhao et al., 2020). In small lipids, such as fatty acids, proteins and lipids can form complexes via molecular self-assembly. It has been reported that protein can bind a small concentration of fatty acid at its specific binding site to form a fatty acid-protein complex via the self-assembly method (Pedersen, Frislev, Pedersen, & Otzen, 2020). For example, compared with oleic acid (OA)-free bovine serum albumin (BSA), OA–BSA complexes (molar ratio 4:1) were found to be more effective in improving the water dispersibility and encapsulation efficiency of astaxanthin (Liu, Huang, et al., 2020). Moreover, the serum response value of FUCO embedded by OA–BSA complexes in mice was 3.94 times than that of FUCO encapsulated by OA-free BSA (Liu, Qiao, et al., 2019). Interestingly, if the ratio of fatty acids is further increased, fatty acids and protein can form hydrophilic “core-shell” particles, in which the hydrophobic core tends to incorporate hydrophobic compounds (Pedersen et al., 2020).

The main purpose of this work was to establish hydrophilic particles with OA and BSA that could improve the dispersibility and bioaccessibility of FUCO in a hydrophilic environment. First, to demonstrate the self-assembly regularities of fatty acids and proteins, the effects of fabrication conditions were investigated, including protein concentration, pH and OA/BSA molar ratios on the formation of OA–BSA particles. Subsequently, the fabricated OA–BSA particles were employed to encapsulate FUCO in water, during which time, the physicochemical properties of the FUCO-loaded OA–BSA particles were characterized and the bioaccessibility of the encapsulated FUCO was also analyzed.

Section snippets

Materials

BSA (≥98.0% protein, CAS# 9048-46-8) was purchased from Sigma-Aldrich (St. Louis, MO, USA). Oleic acid was purchased from Sinopharm Chemical Reagent Co., Ltd. (Beijing, China). FUCO (≥98% purity, CAS# 3351-86-8) was obtained from Dexter Biotechnology Co., Ltd. (Chengdu, China). Pepsin (3000.0 U/mg protein), pancreatin (from porcine pancreas, 259.0 U/mg protein) was obtained from Aladdin Biochemical Technology Co., Ltd. (Shanghai, China). Hydrochloric acid, sodium hydroxide, ethanol and other

Effects of BSA concentration and OA/BSA molar ratio on the physicochemical properties of OA–BSA particles

It is believed that a rise in the number of protein macromolecules can increase the likelihood of aggregation in water (Sponton, Perez, Ramel, & Santiago, 2018). Moreover, according to recent studies, the binding mode between fatty acids and proteins is determined by their ratios during the process of molecular self-assembly, in which four to five fatty acid molecules enter specific binding sites of proteins to form ligand complexes. If the proportion of fatty acids becomes too high,

Conclusions

To facilitate the utilization of FUCO in a hydrophilic environment, in this work, a novel fatty acid-protein delivery vehicle was successfully fabricated by pH-driven self-assembly strategy. It was discovered that the molecular self-assembly of BSA and OA was affected by protein concentration, protein denaturation degree, protein-fatty acid binding ratio, and alkaline condition. Under the optimized conditions (pH shifting from 11.0 to 7.0, BSA 2.0 mg/mL, and OA/BSA molar ratios 13:1 to 30:1),

Author statement

Donghui Li: Writing - Original Draft Data Curation. Qian Zhang: Investigation and Methodology. Ling Huang: Formal Analysis. Zhaohua Chen: Formal Analysis. Chao Zou: Resources. Yu Ma: Software. Min-Jie Cao: Supervision and Validation. Guang-Ming Liu: Supervision and Validation. Yixiang Liu: Conceptualization and Writing - Review & Editing. Yanbo Wang: Manuscript Editing.

Declaration of competing interest

The authors declare no conflict of interest.

Acknowledgements

The present work was supported by Fujian Science Foundation for Distinguished Young Scholars (2020J06024) and National Key Research and Development Program of China (2019YFC1605003-3).

References (44)

  • Y. Liu et al.

    Re-assembled oleic acid-protein complexes as nano-vehicles for astaxanthin: Multispectral analysis and molecular docking

    Food Hydrocolloids

    (2020)
  • M. Liu et al.

    Fucoxanthin: A promising compound for human inflammation-related diseases

    Life Sciences

    (2020)
  • C. Liu et al.

    Formation, characterization, and application of chitosan/pectin-stabilized multilayer emulsions as astaxanthin delivery systems

    International Journal of Biological Macromolecules

    (2019)
  • G. Liu et al.

    Protein-lipid composite nanoparticles for the oral delivery of vitamin B12: Impact of protein succinylation on nanoparticle physicochemical andbiological properties

    Food Hydrocolloids

    (2019)
  • X. Li et al.

    β-Carotene and astaxanthin with human and bovine serum albumins

    Food Chemistry

    (2015)
  • H. Li et al.

    Stability, bioactivity, and bioaccessibility of fucoxanthin in zein-caseinate composite nanoparticles fabricated at neutral pH by antisolvent precipitation

    Food Hydrocolloids

    (2018)
  • H. Luo et al.

    Non-covalent assembly of albumin nanoparticles by hydroxyl radical: A possible mechanism of the nab technology and a one-step green method to produce protein nanocarriers

    Chemical Engineering Journal

    (2021)
  • Z. Ma et al.

    Comparative study of oil-in-water emulsions encapsulating fucoxanthin formulated by microchannel emulsification and high-pressure homogenization

    Food Hydrocolloids

    (2020)
  • J. Mercke Odeberg et al.

    Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations

    European Journal of Pharmaceutical Sciences

    (2003)
  • K. Miyashita et al.

    Fucoxanthin in the management of obesity and its related disorders

    Journal of Functional Foods

    (2017)
  • N. Oliyaei et al.

    Encapsulation of fucoxanthin in binary matrices of porous starch and halloysite

    Food Hydrocolloids

    (2020)
  • P.H.C. Paiva et al.

    Influence of protein conformation and selected hofmeister saltson bovine serum albumin/lutein complex formation

    Food Chemistry

    (2020)
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