Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of Silk Fibroin Biomaterial Coating on Cell Viability and Intestinal Adhesion of Probiotic Bacteria

  • Kwon, Gicheol (R&D Center, Chong Kun Dang Healthcare) ;
  • Heo, Bohye (Probiotics Research Laboratory, Chong Kun Dang Bio Research Institute) ;
  • Kwon, Mi Jin (R&D Center, Chong Kun Dang Healthcare) ;
  • Kim, Insu (R&D Center, Chong Kun Dang Healthcare) ;
  • Chu, Jaeryang (Probiotics Research Laboratory, Chong Kun Dang Bio Research Institute) ;
  • Kim, Byung-Yong (R&D Center, Chong Kun Dang Healthcare) ;
  • Kim, Byoung-Kook (Probiotics Research Laboratory, Chong Kun Dang Bio Research Institute) ;
  • Park, Sung Sun (R&D Center, Chong Kun Dang Healthcare)
  • Received : 2021.03.18
  • Accepted : 2021.03.31
  • Published : 2021.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

Probiotics can be processed into a powder, tablet, or capsule form for easy intake. They are exposed to frequent stresses not only during complex processing steps, but also in the human body after intake. For this reason, various coating agents that promote probiotic bacterial stability in the intestinal environment have been developed. Silk fibroin (SF) is a material used in a variety of fields from drug delivery systems to enzyme immobilization and has potential as a coating agent for probiotics. In this study, we investigated this potential by coating probiotic strains with 0.1% or 1% water-soluble calcium (WSC), 1% SF, and 10% trehalose. Under simulated gastrointestinal conditions, cell viability, cell surface hydrophobicity, and cell adhesion to intestinal epithelial cells were then measured. The survival ratio after freeze-drying was highest upon addition of 0.1% WSC. The probiotic bacteria coated with SF showed improved survival by more than 10.0% under simulated gastric conditions and 4.8% under simulated intestinal conditions. Moreover, the cell adhesion to intestinal epithelial cells was elevated by 1.0-36.0%. Our results indicate that SF has positive effects on enhancing the survival and adhesion capacity of bacterial strains under environmental stresses, thus demonstrating its potential as a suitable coating agent to stabilize probiotics throughout processing, packaging, storage and consumption.

Keywords

References

  1. Morelli L, Capurso L. 2012. FAO/WHO Guidelines on probiotics. J. Clin. Gastroenterol. 46: S1-S2. https://doi.org/10.1097/mcg.0b013e318269fdd5
  2. Williams NT. 2010. Probiotics. Am. J. Health-Syst. Pharm. 67: 449-458. https://doi.org/10.2146/ajhp090168
  3. Szajewska H, Mrukowicz JZ. 2001. Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J. Pediatr. Gastroenterol. Nutr. 33: S17-S25. https://doi.org/10.1097/00005176-200110002-00004
  4. Sartor RB. 2004. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterol. 126: 1620-1633. https://doi.org/10.1053/j.gastro.2004.03.024
  5. George KR, Patra JK, Gouda S, Park Y, Shin HS, Das G. 2018. Benefaction of probiotics for human health: a review. J. Food Drug Anal. 26: 927-939. https://doi.org/10.1016/j.jfda.2018.01.002
  6. Sanders ME, Merenstein DJ, Reid G, Gibson GR, Rastall RA. 2019. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat. Rev. Gastroenterol. Hepatol. 16: 605-616. https://doi.org/10.1038/s41575-019-0173-3
  7. Sarao LK, Arora M. 2017. Probiotics, prebiotics, and microencapsulation: a review. Crit. Rev. Food Sci. Nutr. 57: 344-371. https://doi.org/10.1080/10408398.2014.887055
  8. de Vrese M, Schrezenmeir J. 2008. Probiotics, prebiotics and synbiotics. Adv. Biochem. Eng. Biotechnol. 111: 1-66.
  9. Tripathi MK, Giri SK. 2014. Probiotic functional foods: survival of probiotics during processing and storage. J. Funct. Foods. 9: 225-241. https://doi.org/10.1016/j.jff.2014.04.030
  10. Fiocco D, Longo A, Arena MP, Russo P, Spano G, Capozzi V. 2020. How probiotics face food stress: they get by with a little help. Crit. Rev. Food Sci. Nutr. 60: 1552-1580. https://doi.org/10.1080/10408398.2019.1580673
  11. Anselmo AC, McHugh KJ, Webster J, Langer R, Jaklenec A. 2016. Layer-by-layer encapsulation of probiotics for delivery to the microbiome. Adv. Mater. 28: 9486-9490. https://doi.org/10.1002/adma.201603270
  12. Burgain J, Gaiani C, Linder M, Scher J. 2011. Encapsulation of probiotic living cells: from laboratory scale to industrial applications. J. Food Eng. 104: 467-483. https://doi.org/10.1016/j.jfoodeng.2010.12.031
  13. Yucel FC, Amadei F, Dhayal SK, Cardenas M, Tanaka M, Risbo J. 2019. Hybrid coating of alginate microbeads based on protein-biopolymer multilayers for encapsulation of probiotics. Biotechnol. Prog. 35: 1-12.
  14. Kim KM, Yang SJ, Kim DS, Lee CW, Kim HY, Lee S, et al. 2020. Probiotic properties and immune-stimulating effect of the Jeju lava seawater mineral-coated probiotics. LWT-Food Sci. Technol. 126: 1-6.
  15. Xiao Y, Lu C, Liu Y, Kong L, Bai H, Mu H, et al. 2020. Encapsulation of Lactobacillus rhamnosus in hyaluronic acid-based hydrogel for pathogen-targeted delivery to ameliorate enteritis. ACS Appl. Mater. Interfaces 12: 36967-36977. https://doi.org/10.1021/acsami.0c11959
  16. Gerez CL, de Valdez GF, Gigante ML, Grosso CRF. 2012. Whey protein coating bead improves the survival of the probiotic Lactobacillus rhamnosus CRL 1505 to low pH. Lett. Appl. Microbiol. 54: 552-556. https://doi.org/10.1111/j.1472-765X.2012.03247.x
  17. Ding WK, Shah NP. 2009. Effect of various encapsulating materials on the stability of probiotic bacteria. J. Food Sci. 74: 100-107.
  18. Pliszczak D, Bourgeois S, Bordes C, Valour JP, Mazoyer MA, Orecchioni AM, et al. 2011. Improvement of an encapsulation process for the preparation of pro- and prebiotics-loaded bioadhesive microparticles by using experimental design. Eur. J. Pharm. Sci. 44: 83-92. https://doi.org/10.1016/j.ejps.2011.06.011
  19. Apostolou E, Kirjavainen PV, Saxelin M, Rautelin H, Valtonen V, Salminen SJ, et al. 2001. Good adhesion properties of probiotics: a potential risk for bacteremia? FEMS Immunol. Med. Microbiol. 31: 35-39. https://doi.org/10.1016/S0928-8244(01)00237-1
  20. Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A. 2019. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl. Microbiol. Biotechnol. 103: 6463-6472. https://doi.org/10.1007/s00253-019-09978-7
  21. Falah F, Vasiee A, Behbahani BA, Yazdi FT, Moradi S, Mortazavi SA, et al. 2019. Evaluation of adherence and anti-infective properties of probiotic Lactobacillus fermentum strain 4-17 against Escherichia coli causing urinary tract infection in humans. Microb. Pathog. 131: 246-253. https://doi.org/10.1016/j.micpath.2019.04.006
  22. Mondal M, Trivedy K, Nirmal Kumar S. 2007. The silk proteins, sericin and fibroin in silkworm, Bombyx mori Linn, - a review. Casp. J. Environ. Sci. 5: 63-76.
  23. Qi Y, Wang H, Wei K, Yang Y, Zheng RY, Kim IS, et al. 2017. A review of structure construction of silk fibroin biomaterials from single structures to multi-level structures. Int. J. Mol. Sci. 18: 237. https://doi.org/10.3390/ijms18030237
  24. Nguyen TP, Nguyen QV, Nguyen VH, Le TH, Huynh VQN, Vo DVN, et al. 2019. Silk fibroin-based biomaterials for biomedical. Polymers. 11: 1-25. https://doi.org/10.3390/polym11010001
  25. Chouhan D, Mandal BB. 2020. Silk biomaterials in wound healing and skin regeneration therapeutics: from bench to bedside. Acta Biomater. 103: 24-51. https://doi.org/10.1016/j.actbio.2019.11.050
  26. Byun EB, Sung NY, Kim JH, Choi JI, Matsui T, Byun MW, et al. 2010. Enhancement of anti-tumor activity of gamma-irradiated silk fibroin via immunomodulatory effects. Chem.-Biol. Interact. 186: 90-95. https://doi.org/10.1016/j.cbi.2010.03.032
  27. Coeuret V, Segolene D, Bernardeau M, Gueguen M, Vernoux JP. 2003. Isolation, characterisation and identification of lactobacilli focusing mainly on cheeses and other dairy products. EDP Sciences 83: 269-306.
  28. Devereux R, Wilkinson SS. 2004. Amplification of ribosomal RNA sequences, pp. 509-522. In Akkermans ADL, Elsas JDV, Bruijn FJD (eds.), Mol. Microb. Ecol. Manual. Springer, Dordrecht.
  29. Nogueira GM, Rodas ACD, Leite CAP, Giles C, Higa OZ, Polakiewicz B, et al. 2010. Preparation and characterization of ethanol-treated silk fibroin dense membranes for biomaterials application using waste silk fibers as raw material. Bioresour. Technol. 101: 8446-8451. https://doi.org/10.1016/j.biortech.2010.06.064
  30. Celik OF, O'Sullivan DJ. 2013. Factors influencing the stability of freeze-dried stress-resilient and stress-sensitive strains of bifidobacteria. Int. J. Dairy Sci. 96: 3506-3516. https://doi.org/10.3168/jds.2012-6327
  31. Hansen LT, Allan-Wojtas PM, Jin YL, Paulson AT. 2002. Survival of Ca-alginate microencapsulated Bifidobacterium spp. in milk and simulated gastrointestinal conditions. Food Microbiol. 19: 35-45. https://doi.org/10.1006/fmic.2001.0452
  32. Zuberer DA. 1994. Recovery and enumeration of viable bacteria. pp. 119-144. In Bottomley PJ, Angle JS, Weaver RW (eds.), Methods of Soil Analysis: Part 2 Microbiological and Biochemical Properties. Wiley, New Jersey, USA
  33. Krausova G, Hyrslova I, Hynstova I. 2019. In vitro evaluation of adhesion capacity, hydrophobicity, and auto-aggregation of newly isolated potential probiotic strains. Fermentation 5: 100. https://doi.org/10.3390/fermentation5040100
  34. Bustos I, Garcia-Cayuela T, Hernandez-Ledesma B, Pelaez C, Requena T, Martinez-Cuesta MC. 2012. Effect of flavan-3-ols on the adhesion of potential probiotic lactobacilli to intestinal cells. J. Agric. Food Chem. 60: 9082-9088. https://doi.org/10.1021/jf301133g
  35. Hirano J, Yoshida T, Sugiyama T, Koide N, Mori I, Yokochi T. 2003. The effect of Lactobacillus rhamnosus on enterohemorrhagic Escherichia coli infection of human intestinal cells in vitro. Microbiol. Immunol. 47: 405-409. https://doi.org/10.1111/j.1348-0421.2003.tb03377.x
  36. Alemka A, Clyne M, Shanahan F, Tompkins T, Corcionivoschi N, Bourke B. 2010. Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect. Immun. 78: 2812-2822. https://doi.org/10.1128/IAI.01249-09
  37. Zacarias MF, Souza TC, Zaburlin N, Cara DC, Reinheimer J, Nicoli J, et al. 2017. Influence of technological treatments on the functionality of Bifidobacterium lactis INL1, a breast milk-derived probiotic. J. Food Sci. 82: 2462-2470. https://doi.org/10.1111/1750-3841.13852
  38. Ainsley Reid A, Vuillemard JC, Britten M, Arcand Y, Farnworth E, Champagne CP. 2005. Microentrapment of probiotic bacteria in a Ca2+ -induced whey protein gel and effects on their viability in a dynamic gastro-intestinal model. J. Microencapsul. 22: 603-619. https://doi.org/10.1080/02652040500162840
  39. Zheng X, Fu N, Huang S, Jeantet R, Chen XD. 2016. Exploring the protective effects of calcium-containing carrier against dryinginduced cellular injuries of probiotics using single droplet drying technique. Food Res. Int. 90: 226-234. https://doi.org/10.1016/j.foodres.2016.10.034
  40. Nogueira GM, de Moraes MA, Rodas ACD, Higa OZ, Beppu MM. 2011. Hydrogels from silk fibroin metastable solution: formation and characterization from a biomaterial perspective. Mater. Sci. Eng. C 31: 997-1001. https://doi.org/10.1016/j.msec.2011.02.019
  41. de la Cruz Pech-Canul A, Ortega D, Garcia-Triana A, Gonzalez-Silva N, Solis-Oviedo RL. 2020. A brief review of edible coating materials for the microencapsulation of probiotics. Coatings. 10: 1-34. https://doi.org/10.3390/coatings10010001
  42. Zhang DD, Dai LX. 2013. Preparation and characterization of electrospun poly(vinyl alcohol)/silk fibroin nanofibers as a potential drug delivery system. Open J. Adv. Mater. Res. 709: 215-220. https://doi.org/10.4028/www.scientific.net/AMR.709.215
  43. Bernet MF, Brassart D, Neeser JR, Servin AL. 1993. Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl. Environ. Microbiol. 59: 4121-4128. https://doi.org/10.1128/AEM.59.12.4121-4128.1993
  44. Andrews GP, Laverty TP, Jones DS. 2009. Mucoadhesive polymeric platforms for controlled drug delivery. Eur. J. Pharm. Biopharm. 71: 505-518. https://doi.org/10.1016/j.ejpb.2008.09.028
  45. de Wouters T, Jans C, Niederberger T, Fischer P, Ruhs PA. 2015. Adhesion potential of intestinal microbes predicted by physico-chemical characterization methods. PLoS One 10: e0136437. https://doi.org/10.1371/journal.pone.0136437
  46. Duary RK, Rajput YS, Batish VK, Grover S. 2011. Assessing the adhesion of putative indigenous probiotic lactobacilli to human colonic epithelial cells. Indian J. Med. Res. 134: 664-671. https://doi.org/10.4103/0971-5916.90992
  47. Hojjati M, Behabahani BA, Falah F. 2020. Aggregation, adherence, anti-adhesion and antagonistic activity properties relating to surface charge of probiotic Lactobacillus brevis gp104 against Staphylococcus aureus. Microb. Pathog. 147: 104420. https://doi.org/10.1016/j.micpath.2020.104420
  48. Grigoryan S, Bazukyan I, Trchounian A. 2018. Aggregation and adhesion activity of lactobacilli isolated from fermented products in vitro and in vivo: a potential probiotic strain. Probiotics Antimicrob. Proteins 10: 269-276. https://doi.org/10.1007/s12602-017-9283-9