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Enhanced Colon-Targeted Release of Propolis by pH-driven Encapsulation using Folic Acid Modified Carboxymethyl Chitosan

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Abstract

Propolis is a natural bioactive compound that is being explored as a nutraceutical because of its potential health benefits. In this study, propolis-loaded biopolymer nanoparticles were fabricated from folic acid-modified carboxymethyl chitosan (FA-CMCS) using the pH-driven method. The mean diameter of the propolis-loaded FA-CMCS nanoparticles was about 180 nm, and transmission electron microscopy showed they had a spherical shape. Fourier transform infrared spectroscopy analysis demonstrated that hydrogen bonding, electrostatic, and hydrophobic interactions were the major driving forces responsible for nanoparticle formation. The nanoparticles had good colloidal stability at pH 2.0, 3.0, 7.0, and 8.0 but exhibited some aggregation at intermediate pH values. The nanoparticles were also stable to salt addition up to 400 mM NaCl. Propolis-loaded FA-CMCS nanoparticles exhibited improved antioxidant properties compared to pure propolis and propolis-free nanoparticles. A simulated digestion model (fed state conditions) indicated that different amounts of propolis were released in different gastrointestinal regions: around 25%, 15%, and 25% in the stomach, small intestine, and colon, respectively. Our results suggest that the nanoparticles fabricated in this study have potential as colloidal delivery systems for sustained release of propolis in the human gut.

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References

  1. Y. Xu, L. Luo, B. Chen, Y. Fu, Front. Biol. China. 4(4), 385 (2009). https://doi.org/10.1007/s11515-009-0053-2

    Article  Google Scholar 

  2. J.M. Sforcin, V. Bankova, A.K. Kuropatnicki, Evid-Based. Compl. Alt. 2017, 2702106 (2017). https://doi.org/10.1155/2017/2702106

    Article  Google Scholar 

  3. S. Rajpara, M.S. Wilkinson, C.M. King, D.J. Gawkrodger, J.S. English, B.N. Statham, C. Green, J.E. Sansom, M.M.U. Chowdhury, H.L. Horne, A.D. Ormerod, Contact Dermatitis 61(5), 287 (2009). https://doi.org/10.1111/j.1600-0536.2009.01629.x

    Article  PubMed  Google Scholar 

  4. J.M. Sforcin, Phytother. Res. 30(6), 894 (2016). https://doi.org/10.1002/ptr.5605

    Article  PubMed  Google Scholar 

  5. S.I. Anjum, A. Ullah, K.A. Khan, M. Attaullah, H. Khan, H. Ali, M.A. Bashir, M. Tahir, M.J. Ansari, H.A. Ghramh, N. Adgaba, C.K. Dash, Saudi. J. Biol. Sci. 26(7), 1695 (2018). https://doi.org/10.1016/j.sjbs.2018.08.013

    Article  CAS  Google Scholar 

  6. Y. Frion-Herrera, D. Gabbia, A. Diaz-Garcia, O. Cuesta-Rubio, M. Carrara, Fitoterapia 136, 104173 (2019). https://doi.org/10.1016/j.fitote.2019.104173

    Article  CAS  PubMed  Google Scholar 

  7. N.L. Vukovic, A.D. Obradovic, M.D. Vukic, D. Jovanovic, P.M. Djurdjevic, Food Res. Int. 106, 71 (2018). https://doi.org/10.1016/j.foodres.2017.12.056

    Article  CAS  PubMed  Google Scholar 

  8. T.C.A. Erika, C.D.S. Maria, M.S.O. José, U.K. Regianne, E.S.A. Rodolfo, A.V. Danilo, C.S. Valdemir, B.E. Pierre, D.B. Irinaldo, G.D.N. Ticiano, J. Pharm. Anal. 7(5), 280 (2017). https://doi.org/10.1016/j.jpha.2017.03.004

    Article  Google Scholar 

  9. V. Tzankova, D. Aluani, Y. Yordanov, M. Kondeva-Burdina, P. Petrov, V. Bankova, R. Simeonova, V. Vitcheva, F. Odjakov, A. Apostolov, B. Tzankov, K. Yoncheva, Rev. Bras. Farmacogn. 29(3), 364 (2018). https://doi.org/10.1016/j.bjp.2018.12.006

    Article  CAS  Google Scholar 

  10. T. Ozdal, F.D. Ceylan, N. Eroglu, M. Kaplan, E.O. Olgun, E. Capanoglu, Food Res. Int. 122, 528 (2019). https://doi.org/10.1016/j.foodres.2019.05.028

    Article  CAS  PubMed  Google Scholar 

  11. M. Sahlan, D. Dienayati, D. Hamdi, S. Zahra, H. Hermansyah, M. Chulasiri, Makara. J. Technol. 21(1), 1 (2017). https://doi.org/10.7454/mst.v21i1.3072

    Article  Google Scholar 

  12. M.P. Nori, C.S. Favaro-Trindade, S.M.D. Alencar, M. Thomazini, J.C.D.C. Balieiro, C.J.C. Castillo, LWT-Food Sci. Technol. 44(2), 429 (2011). https://doi.org/10.1016/j.lwt.2010.09.010

    Article  CAS  Google Scholar 

  13. C. Jansen-Alves, D.S.V. Maia, F.D. Krumreich, M.M. Crizel-Cardoso, J.B. Fioravante, W.P. da Silva, C.D. Borges, R.C. Zambiazi, Food Hydrocoll. 87, 703 (2018). https://doi.org/10.1016/j.foodhyd.2018.09.004

    Article  CAS  Google Scholar 

  14. M. Sahlan, T. Supardi, Int. J. Pharm. Bio. Sci. 4(1), 297 (2013)

    CAS  Google Scholar 

  15. K. Pan, Q. Zhong, Food Hydrocoll. 52, 600 (2015). https://doi.org/10.1016/j.foodhyd.2015.08.014

    Article  CAS  Google Scholar 

  16. Z. Shariatinia, Int. J. Biol. Macromol. 120, 1406 (2018). https://doi.org/10.1016/j.ijbiomac.2018.09.131

    Article  CAS  PubMed  Google Scholar 

  17. S. Kalliola, E. Repo, V. Srivastava, F. Zhao, J.P. Heiskanen, J.A. Sirvio, H. Liimatainen, M. Sillanpaa, Langmuir 34(8), 2800 (2018). https://doi.org/10.1021/acs.langmuir.7b03959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. J. Xiao, S. Nian, Q. Huang, Food Hydrocoll. 51, 166 (2015). https://doi.org/10.1016/j.foodhyd.2015.05.012

    Article  CAS  Google Scholar 

  19. S.S. Vaghani, M.M. Patel, C.S. Satish, Carbohyd. Res. 347(1), 76 (2012). https://doi.org/10.1016/j.carres.2011.04.048

    Article  CAS  Google Scholar 

  20. H. Tu, Y. Qu, X. Hu, Y. Yin, H. Zheng, P. Xu, F. Xiong, Carbohyd. Polym. 82(2), 440 (2010). https://doi.org/10.1016/j.carbpol.2010.04.086

    Article  CAS  Google Scholar 

  21. H. Zhang, Y. Fu, F. Niu, Z. Li, C. Ba, B. Jin, G. Chen, X. Li, Food Hydrocoll. 81, 104 (2018). https://doi.org/10.1016/j.foodhyd.2018.02.019

    Article  CAS  Google Scholar 

  22. M. Wang, Y. Fu, G. Chen, Y. Shi, X. Li, H. Zhang, Y. Shen, Food Hydrocoll. 77, 577 (2018). https://doi.org/10.1016/j.foodhyd.2017.10.036

    Article  CAS  Google Scholar 

  23. Y. Li, S. Zhang, X. Meng, X. Chen, G. Ren, Carbohyd. Polym. 83(1), 130 (2011). https://doi.org/10.1016/j.carbpol.2010.07.030

    Article  CAS  Google Scholar 

  24. Y. Lu, P.S. Low, Adv. Drug Deliver. Rev. 64, 342 (2012). https://doi.org/10.1016/j.addr.2012.09.020

    Article  Google Scholar 

  25. Y. Tan, C. Liu, J. Mater. Sci. Mater. Med. 22(5), 1213 (2011). https://doi.org/10.1007/s10856-011-4302-y

    Article  CAS  PubMed  Google Scholar 

  26. F. Luo, Z. Fan, W. Yin, L. Yang, T. Li, L. Zhong, Y. Li, S. Wang, J. Yan, Z. Hou, Q. Zhang, Mater. Sci. Eng. C. 105, 110107 (2019). https://doi.org/10.1016/j.msec.2019.110107

    Article  CAS  Google Scholar 

  27. S. Sahu, S. Mallick, S. Santra, T. Maiti, S. Ghosh, P. Pramanik, J. Mater. Sci: Mater. Med. 21(5), 1587 (2010). https://doi.org/10.1007/s10856-010-3998-4

    Article  CAS  Google Scholar 

  28. Z. Hu, H. Zheng, D. Li, X. Xiong, M. Tan, D. Huang, X. Guo, X. Zhang, H. Yan, J. Wuhan Univ. Technol. 31, 446 (2015). https://doi.org/10.1007/s11595-016-1390-z

    Article  CAS  Google Scholar 

  29. Y. Luo, K. Pan, Q. Zhong, Int. J. Pharmaceut. 486(1–2), 59 (2015). https://doi.org/10.1016/j.ijpharm.2015.03.043

    Article  CAS  Google Scholar 

  30. D.J. McClements, S. Peng, Z. Li, L. Zou, W. Liu, C. Liu, J. Agric. Food Chem. 66(6), 1488 (2018). https://doi.org/10.1021/acs.jafc.7b05478

    Article  CAS  PubMed  Google Scholar 

  31. K. Pan, H. Chen, S.J. Baek, Q. Zhong, Food Chem. 246, 82 (2018). https://doi.org/10.1016/j.foodchem.2017.11.002

    Article  CAS  PubMed  Google Scholar 

  32. K. Pan, Y. Luo, Y. Gan, S.J. Baek, Q. Zhong, Soft Matter 10(35), 6820 (2014). https://doi.org/10.1039/c4sm00239c

    Article  CAS  PubMed  Google Scholar 

  33. L. Wang, Y. Zhang, J. Agric. Food Chem. 65(14), 2990 (2017). https://doi.org/10.1021/acs.jafc.7b00194

    Article  CAS  PubMed  Google Scholar 

  34. V.L. Singleton, R. Orthofer, R.M. Lamuela-Raventós, Methods Enzymol. 299, 152 (1999)

    Article  CAS  Google Scholar 

  35. H. Li, Z. Li, J. Zhao, B. Tang, Y. Chen, Y. Hu, Z. He, Y. Wang, Nanoscale Res. Lett. 9(1), 1 (2014). https://doi.org/10.1186/1556-276X-9-146

    Article  CAS  Google Scholar 

  36. F. Wang, D. Zhang, C. Duan, L. Jia, F. Feng, Y. Liu, Y. Wang, L. Hao, Q. Zhang, Carbohyd. Polym. 84(3), 1192 (2011). https://doi.org/10.1016/j.carbpol.2011.01.017

    Article  CAS  Google Scholar 

  37. H. Zhang, Y. Fu, Y. Xu, F. Niu, Z. Li, C. Ba, B. Jin, G. Chen, X. Li, Food Funct. 10(2), 635 (2019). https://doi.org/10.1039/c8fo01614c

    Article  CAS  PubMed  Google Scholar 

  38. I.F.F. Benzie, J. Strain, J. Anal. Biochem. 239(1), 70 (1996). https://doi.org/10.1006/abio.1996.0292

    Article  CAS  Google Scholar 

  39. P.H. Leung, S. Zhao, K.P. Ho, J.Y. Wu, Food Chem. 114(4), 1251 (2009). https://doi.org/10.1016/j.foodchem.2008.10.081

    Article  CAS  Google Scholar 

  40. K. Feng, C. Li, Y. Wei, M. Zong, H. Wu, S. Han, J. Colloid. Interf. Sci. 552, 186 (2019). https://doi.org/10.1016/j.jcis.2019.05.037

    Article  CAS  Google Scholar 

  41. Y. Zhang, X. Tan, T. Ren, C. Jia, Z. Yang, H. Sun, Carbohyd. Polym. 198, 76 (2018). https://doi.org/10.1016/j.carbpol.2018.06.055

    Article  CAS  Google Scholar 

  42. F. Jing, G. Li, Y. Wang, S. Zhu, R. Liu, J. He, J. Lei, Polym. Advan. Technol. 32(1), 343 (2020). https://doi.org/10.1002/pat.5090

    Article  CAS  Google Scholar 

  43. B.S. Esfandiarpour, K.S. Bagheri, H. Mirzadeh, Prog. Biomater. 5, 1 (2016). https://doi.org/10.1007/s40204-015-0044-0

    Article  CAS  Google Scholar 

  44. T. G. D. Nascimento, P. F. D. Silva, L. F. Azevedo, L. G. D. Rocha, P. Moraes, I. C. D., E. M. T. F. Lima, I. D. B. Junior, L. A. Grillo, C. B. Dornelas, E. J. Fonseca, J. O. E. D., A. T. Zhang,D. G. Watson (2016), Nanoscale Res. Lett. 11 (1), 301. https://doi.org/10.1186/s11671-016-1517-3

  45. Y. Wu, S. Sun, J. Zhao, Y. Li, Q. Zhou, J. Mol. Struct. 883–884, 48 (2008). https://doi.org/10.1016/j.molstruc.2007.12.009

    Article  CAS  Google Scholar 

  46. M.F. Fangio, D.E. Orallo, L.B. Gende, M.S. Churio, J. Apicult. Res. 58(4), 626 (2019). https://doi.org/10.1080/00218839.2019.1601318

    Article  Google Scholar 

  47. Y. Irigoiti, D.K. Yamul, A.S. Navarro, LWT-Food Sci. Technol. 143, 1 (2021). https://doi.org/10.1016/j.lwt.2021.111164

    Article  CAS  Google Scholar 

  48. K. Hu, D.J. McClements, Food Res. Int. 64, 329 (2014). https://doi.org/10.1016/j.foodres.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  49. W. Xiong, C. Ren, J. Li, B. Li, Food Funct. 9(7), 3788 (2018). https://doi.org/10.1039/c8fo00300a

    Article  CAS  PubMed  Google Scholar 

  50. C. Xiang, J. Gao, H. Ye, G. Ren, X. Ma, H. Xie, S. Fang, Q. Lei, W. Fang, Food Hydrocoll. 106, 1 (2020). https://doi.org/10.1016/j.foodhyd.2020.105926

    Article  CAS  Google Scholar 

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Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. School of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018, China

    Yuhang Wang, Yuying Fu, David Julian McClements & Teng Li

  2. Department of Food Science, University of Massachusetts, Amherst, MA, 01003, USA

    David Julian McClements

  3. School of Civil Engineering and Architecture, Zhejiang Sci-Tech University, Hangzhou, 310018, China

    Chujie Ba

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  1. Yuhang Wang
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  2. Yuying Fu
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  3. David Julian McClements
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Contributions

Y.W.: Conceptualization; Methodology; Investigation; Data curation; Formal analysis; Visualization; Writing—review & editing.

Y.F.: Conceptualization; Supervision; Formal analysis; Funding acquisition; Resources; Writing—review & editing.

D.J.M.: Writing—review & editing.

C.B.: Formal analysis; Investigation; Methodology; Visualization; Writing—original draft.

T.L.: Supervision; Data curation; Formal analysis; Writing—review & editing.

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Correspondence to Yuying Fu.

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Wang, Y., Fu, Y., McClements, D.J. et al. Enhanced Colon-Targeted Release of Propolis by pH-driven Encapsulation using Folic Acid Modified Carboxymethyl Chitosan. Food Biophysics 17, 386–396 (2022). https://doi.org/10.1007/s11483-022-09729-8

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