Self-Assembled Micelles Based on OSA-Modified Starches for

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Article Cite This: J. Agric. Food Chem. 2019, 67, 6614−6624

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Self-Assembled Micelles Based on OSA-Modified Starches for Enhancing Solubility of β‑Carotene: Effect of Starch Macromolecular Architecture Quanquan Lin,†,‡,§,∥ Rong Liang,†,⊥ Fang Zhong,*,†,§,⊥ Aiqian Ye,*,‡,∥ Yacine Hemar,‡ Zhi Yang,# and Harjinder Singh‡ †

Key Laboratory of Synthetic and Biological Colloids, Ministry of Education, Jiangnan University, Wuxi 214122, China Riddet Institute, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand § School of Food Science and Technology, Jiangnan University, Wuxi 214122, China ∥ School of Food Science and Bioengineering, Zhejiang Gongshang University, Hangzhou, Zhejiang 310018, China ⊥ School of Chemical and Material Engineering, Jiangnan University, Wuxi 214122, China # Biology and Soft Matter Division, Neutron Sciences Directorate, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States

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‡

S Supporting Information *

ABSTRACT: Self-assembled micelles based on octenyl succinic anhydride (OSA)-modified starch were prepared to enhance the solubility of β-carotene. The critical micelle concentration (CMC) was lower for OSA-modified starch with a lower molecular weight (Mw) or higher degree of substitution (DS). Above the CMC, OSA-modified starch assembled into spherical micelles with an average hydrodynamic diameter of H6-OSA5% > H12-OSA5%, which suggested that OSA-modified starches with a larger Mw formed micelles at a higher concentration. This result was in agreement with a study conducted by Lei et al.25 At a given DS, increase in the Mw of OSA-modified starch may imply a reduction in the relative hydrophobicity, which led to lower the interfacial tension and further made it difficult to form micelles in the case of OSA-modified starches with larger Mw. However, Tizzotti et al.27 found the opposite; i.e., OSAmodified starches with a larger macromolecular size formed micelles at lower concentrations for a given DS. These authors considered that an increase in the average number of OSA groups per starch chain, induced by increasing the Mw while keeping the DS constant, contributed to micelles forming more readily for OSA-modified starches with larger Mw. These different results can be attributed to the different structures of the polymers used. The effect of the Mw on the self-assembly of polymers is probably a result of the competition between the two opposing effects, enhanced by a greater average number of OSA groups per starch chain and decreased by a reduction in relative hydrophobicity. For OSA-modified starches with similar Mw, an increase in the DS (from 2.54 ± 0.04 to 4.16 ± 0.01%) significantly decreased the CMC from 0.084 to 0.058% (Table 1), indicating that the number of OSA groups is a primary factor in the micellization process. It has been reported that the driving force in the formation of micelles is the hydrophobic interactions among the OSA groups.25 The results in this current study are consistent with previous studies,21,25,27,35,36 which also showed that a higher DS of hydrophobic groups in the polymers leads to micelle formation at a lower concentration. Particle Size of OSA-Modified Starch Self-Assembly. The size of the self-assembled micelles is important to the appearance (e.g., transparency), stability, and encapsulation capacity of an OSA-modified starch solution. As an example, the particle size distribution of micelles formed by H12OSA5%, as measured by DLS, was represented as both the intensity-weighted particle concentration and the volumeweighted particle concentration versus the particle diameter (Figure 3). The intensity distribution is very sensitive to the

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RESULTS AND DISCUSSION Characterization of OSA-Modified Starches. The Mw distribution and the concentration signal of the OSA-modified starches versus the elution volume are shown in Figure 1. The

Figure 1. Weight-average Mw and concentration signal versus elution volume of OSA-modified starches. Solid line, concentration signal; dashed line, Mw distribution.

Mw and the DS are given in Table 1. All samples had a wide Mw distribution (Figure 1), and the weight-average Mw decreased with increasing acid hydrolysis time (Table 1). The DSs of the H1-OSA5%, H6-OSA5%, and H12-OSA5% were all around 2.5%, with no significant difference (p > 0.05), suggesting that the Mw had no influence on the esterification of starches with the same amount of added OSA. When the added OSA was increased from 5 to 9%, the DS of the starch increased from 2.54 ± 0.04 to 4.16 ± 0.01% at an acid 6616

DOI: 10.1021/acs.jafc.9b00355 J. Agric. Food Chem. 2019, 67, 6614−6624

Article

Journal of Agricultural and Food Chemistry Table 1. Weight-Average Mw, DS, and CMC of OSA-Modified Starchesa starch native starch H1-OSA5% H6-OSA5% H12-OSA5% H12-OSA9%

hydrolysis time (h) 1 6 12 12

addition of OSA (g/starch)

Mw (×104 g/mol) 5550.0 1243.0 60.27 19.24 19.60

5 5 5 9

± ± ± ± ±

277.5a 10.0b 0.06c 0.07d 0.05d

DS (%)

CMC (%)

± ± ± ±

0.140 0.107 0.084 0.058

2.60 2.57 2.54 4.16

0.02b 0.01b 0.04b 0.01a

a

Different superscript letters indicate significant differences (p < 0.05) in the same column.

Figure 3. Particle size distribution of starch micelles formed by 5% of H12-OSA5%.

As seen in Figure 4A, the volume mean diameter of micelles formed from H1-OSA5% decreased markedly from 416.6 ± 268.8 to 15.8 ± 9.4 nm when the starch concentration was increased from 0.05 to 1%. Further increases in the starch concentration ( H6-OSA5% > H12-OSA5%, indicating that the Rg of the β-carotene-free micelles was significantly positively (p < 0.05) correlated with the Mw of the starch. The trend in the Rg of the β-carotene-free micelles was consistent with that in the Dh of these micelles. With a similar Mw, the Rg of the βcarotene-free micelles was slightly smaller for H12-OSA9% than for H12-OSA5% at all starch concentrations. Although there was no significant change in the Dh with increasing DS, the Rg of the β-carotene-free micelles formed from OSAmodified starch with higher DS was smaller because of the formation of more compact micelles with enhanced intermolecular hydrophobic interactions among the starch molecules. In addition, there was a slight but significant increase (p < 0.05) in the Rg of all micelles after the incorporation of βcarotene (Table 2), which could be attributed to the enlargement of the hydrophobic core. Interestingly, Yu and Huang,23 reported that the incorporation of curcumin did not induce any changes in the Rg of OSA-modified starch micelles, as determined by SAXS. This may reflect different sizes of the lipophilic bioactive components; the Mw of β-carotene is 1.45 times greater than that of curcumin. Besides, the trends in the Rg of all the β-carotene-loaded micelles were the same as those in the β-carotene-free micelles when the concentration, Mw, or DS of the OSA-modified starch was changed (Table 2). In detail, the Rg decreased when the concentration or DS of the starch was increased; whereas it increased when the Mw of the starch was increased. Finally, it is worth noting, that the aggregates of starch micelles or higher-order assemblies with a

Figure 10. Guinier plots of the scattering data of starch micelles. (A) β-Carotene-free micelles; (B) β-carotene-loaded micelles. The Guinier fit curves are shown as a solid red line in each plot.

Table 2. Effect of Concentration, Mw, and DS of OSA-Modified Starches on the Radius of Gyration (Rg, nm) of Micelles with and without Loaded β-Carotene β-carotenea −

+

starch concentration (%) 1 2 5 1 2 5

H1-OSA5% 8.45 8.11 5.68 8.78 8.17 5.74

± ± ± ± ± ±

0.19 0.16 0.06 0.09 0.08 0.04

H6-OSA5% 6.65 5.90 4.40 6.42 6.05 4.48

± ± ± ± ± ±

0.14 0.02 0.02 0.08 0.02 0.02

H12-OSA5% 5.54 5.01 3.86 5.66 5.01 3.93

± ± ± ± ± ±

0.15 0.01 0.01 0.06 0.01 0.01

H12-OSA9% 5.57 4.69 3.53 5.66 4.94 3.67

± ± ± ± ± ±

0.06 0.00 0.01 0.03 0.01 0.01

− indicates without β-carotene; + indicates with β-carotene.

a

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DOI: 10.1021/acs.jafc.9b00355 J. Agric. Food Chem. 2019, 67, 6614−6624

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Journal of Agricultural and Food Chemistry

scattering; TEM, transmission electron microscopy; XRD, Xray diffraction

large particle size (>100 nm) could not be measured by SAXS due to the limit of the high q range. In summary, OSA-modified starch formed micelles at above the CMC, which correlated positively with the Mw but negatively with the DS of the starch. Both DLS and SAXS showed that the particle size of the starch micelles decreased with increasing concentration or decreasing Mw. A greater DS led to a smaller Rg of the starch micelles. The OSA-modified starch micelles markedly increased the apparent solubility of βcarotene in the aqueous phase through hydrophobic interactions between the core of the micelles and β-carotene. The incorporation of β-carotene enlarged the hydrophobic core and induced a significant increase in the Rg of the micelles determined by SAXS, and it may also promote the aggregation of micelles or the formation of higher-order assemblies resulting in a marked increase in the Dh determined by DLS. The encapsulation capacity of the OSA-modified starch micelles showed a positive relationship with the concentration, Mw, and DS of the starch. From a practical viewpoint, this work provides fundamental support for the design of innovative delivery systems for lipophilic bioactive compounds in the food industry.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.9b00355.

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REFERENCES

XRD spectra of β-carotene powder, powder of βcarotene-free micelles, and powder of β-carotene-loaded micelles formed by 5% of OSA-modified starch (H12OSA9%) (PDF)

AUTHOR INFORMATION

Corresponding Authors

*Tel.: +86 510 85197876; E-mail: [email protected]. *Tel.: +64 6 350 5072; E-mail: [email protected]. ORCID

Rong Liang: 0000-0002-1578-2047 Fang Zhong: 0000-0002-5850-4960 Funding

This research was supported by the National Key R&D Program of China (2016YFD0400801) and the National Natural Science Foundation of China (31571891 and 31801589). It was also supported by a program of the “Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province”, China, a national first-class discipline program of Food Science and Technology (JUFSTR20180204), and the Riddet Institute, a New Zealand Centre of Research Excellence, funded by the Tertiary Education Commission. Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED CMC, critical micelle concentration; Dh, hydrodynamic diameter; DLS, dynamic light scattering; DS, degree of substitution; FTIR, Fourier transform infrared; I337/I334, excitation fluorescence intensity ratio of pyrene; Mw, molecular weight; OSA, octenyl succinic anhydride; Rg, radius of gyration; Rh, hydrodynamic radius; SAXS, small-angle X-ray 6623

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DOI: 10.1021/acs.jafc.9b00355 J. Agric. Food Chem. 2019, 67, 6614−6624