Skip to main content
Log in

Comparative survival of exopolysaccharide encapsulated Lactobacillus plantarum and Pediococcus pentosaceus in simulated gastrointenstinal conditions and storage time

  • Original Paper
  • Published:
Journal of Food Measurement and Characterization Aims and scope Submit manuscript

Abstract

The objective of the present study was to evaluate the effect of microbial exopolysaccharide (EPS) encapsulation of lactic acid bacteria on enhancing their viability during exposure to the simulated conditions of the gasterointestinal tract. Lactobacillus plantarum (NR_104573.1) and Pediococcus pentosaceus (NR_042058.1) isolated from wheat bran sourdough were encapsulated by spray-drying with various ratios of EPS, whey protein concentrate, carboxymethyl cellulose and pectin. The viability, kinetics and survival under stress conditions were compared between the samples after 120 min of incubation and over 28 days of storage. HPLC was used for compositional assessment in terms of monosaccharide constituents, revealing that glucose, arabinose and xylose were the major components of the EPS produced by L. plantarum and P. pentosaceus. ANOVA demonstrated a significantly reduced logarithmic cycle of bacterial population in the control samples and free cells compared to the encapsulated L. plantarum and P. pentosaceus after 2 h in simulated gastric fluid conditions and bile salt solution. Encapsulation yields in the presence of WPC, CMC and pectin with and without EPS were about 85 and 80% for L. plantarum, and it was 81 and 75% for P. pentosaceus, respectively. Also, the viability number of L. plantarum and P. pentosaceus free cells decreased over 28 days of storage from 12.41 to 7.28 and 12.11 to 6.96 log Cfu/mL, respectively. Finally, by assessing the kinetics of the bacteria with three mathematical models, the Ritger–Peppas kinetics model was found to be a suitable correlation model for the data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. I.W. Sutherland, Novel and established applications of microbial polysaccharides. Trends Biotechnol. 16, 41–46 (1998)

    CAS  PubMed  Google Scholar 

  2. B. Vu, M. Chen, R.J. Crawford, E.P. Ivanova, Bacterial extracellular polysaccharides involved in biofilm formation. Molecules. 14, 2535–2554 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  3. C. Liu, J. Lu, L. Lu, Y. Liu, F. Wang, M. Xiao, Isolation, structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour. Technol. 101, 5528–5533 (2010)

    CAS  PubMed  Google Scholar 

  4. A. Abedfar, M. Hossininezhad, A. Sadeghi, M. Raeisi, J. Feizy, Investigation on “spontaneous fermentation” and the productivity of microbial exopolysaccharides by Lactobacillus plantarum and Pediococcus pentosaceus isolated from wheat bran sourdough. LWT Food Sci. Technol. 96, 686–693 (2018)

    CAS  Google Scholar 

  5. M.Y. Chen, W. Zheng, Q.Y. Dong, Z.H. Li, L.E. Shi, Z.X. Ananta, Activity of encapsulated Lactobacillus bulgaricus in alginate-whey protein microspheres. Braz. Arch. Biol. Technol. 57, 736–741 (2014)

    CAS  Google Scholar 

  6. L.E. Shi, Z.H. Li, D.T. Li, M. Xu, H.Y. Chen, Z.L. Zhang, Z.X. Tang, Encapsulation of probiotic Lactobacillus bulgaricus in alginate–milk microspheres and evaluation of the survival in simulated gastrointestinal conditions. J. Food Eng. 117, 99–104 (2013)

    CAS  Google Scholar 

  7. A.K. Anal, W.F. Stevens, C. Remunan-Lopez, Ionotropic cross-linked chitosan microspheres for controlled release of ampicillin. Int. J. Pharm. 312, 166–173 (2006)

    CAS  PubMed  Google Scholar 

  8. E. Ananta, M. Volkert, D. Knorr, Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. Int. Dairy J. 15, 399–409 (2005)

    CAS  Google Scholar 

  9. L.E. Shi, W. Zheng, Y. Zhang, Z.X. Tang, Milk-alginate microspheres: Protection and delivery of Enterococcus faecalis HZNU P2. LWT Food Sci. Technol. 65, 840–844 (2016)

    CAS  Google Scholar 

  10. Q.Y. Dong, M.Y. Chen, Y. Xin, X.Y. Qin, Z. Cheng, L.E. Shi, Z.X. Tang, Alginate-based and protein‐based materials for probiotics encapsulation: a review. Int. J. Food Sci. Technol. 48, 1339–1351 (2013)

    CAS  Google Scholar 

  11. S. Rokka, P. Rantamaki, Protecting probiotic bacteria by microencapsulation: challenges for industrial applications. Eur. Food Res. Technol. 231, 1–12 (2010)

    CAS  Google Scholar 

  12. B.M. Corcoran, R.P. Ross, G.F. Fitzgerald, C. Stanton, Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J. Appl. Microbiol. 96, 1024–1039 (2004)

    CAS  PubMed  Google Scholar 

  13. M. Girard, S.L. Turgeon, S.F. Gauthier, Interbiopolymer complexing between β-lactoglobulin and low-and high-methylated pectin measured by potentiometric titration and ultrafiltration. Food Hydrocoll. 16, 585–591 (2002)

    CAS  Google Scholar 

  14. F. Dal Bello, C.I. Clarke, L.A.M. Ryan, H. Ulmer, T.J. Schober, K. Ström, J. Sjögren, D. Van Sinderen, J. Schnürer, E.K. Arendt, Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. J Cereal Sci. 45, 309–318 (2007)

    CAS  Google Scholar 

  15. Y. Boza, L.P. Neto, F.A.A. Costa, A.R.P. Scamparini, Exopolysaccharide production by encapsulated Beijerinckia cultures. Process Biochem. 39, 1201–1209 (2004)

    CAS  Google Scholar 

  16. R. Tallon, P. Bressollier, M.C. Urdaci, Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Res. Microbiol. 154, 705–712 (2003)

    CAS  PubMed  Google Scholar 

  17. Y. Lv, X. Yang, Y. Zhao, Y. Ruan, Y. Yang, Z. Wang, Separation and quantification of component monosaccharides of the tea polysaccharides from Gynostemma pentaphyllum by HPLC with indirect UV detection. Food Chem 112, 742–746 (2009)

    CAS  Google Scholar 

  18. H. Stepan, E. Staudacher, Optimization of monosaccharide determination using anthranilic acid and 1-phenyl-3-methyl-5-pyrazolone for gastropod analysis. Anal. Biochem. 418, 24–29 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. M.E. Rodríguez-Huezo, R. Durán-Lugo, L.A. Prado-Barragán, F. Cruz-Sosa, C. Lobato-Calleros, J. Alvarez-Ramírez, E.J. Vernon-Carter, Pre-selection of protective colloids for enhanced viability of Bifidobacterium bifidum following spray-drying and storage, and evaluation of aguamiel as thermoprotective prebiotic. Food Res. Int. 40, 1299–1306 (2007)

    Google Scholar 

  20. R. Altamirano-Fortoul, R. Moreno-Terrazas, A. Quezada-Gallo, C.M. Rosell, Viability of some probiotic coatings in bread and its effect on the crust mechanical properties. Food Hydrocoll. 29, 166–174 (2012)

    CAS  Google Scholar 

  21. Z. Tang, X. Huang, P.M. Sabour, J.R. Chambers, Q. Wang, Preparation and characterization of dry powder bacteriophage K for intestinal delivery through oral administration. LWT Food Sci. Technol. 60, 263–270 (2015)

    CAS  Google Scholar 

  22. L.E. Shi, Z.H. Li, Z.L. Zhang, T.T. Zhang, W.M. Yu, M.L. Zhou, Z.X. Tang, Encapsulation of Lactobacillus bulgaricus in carrageenan-locust bean gum coated milk microspheres with double layer structure. LWT Food Sci. Technol. 54, 147–151 (2013)

    CAS  Google Scholar 

  23. A. Picot, C. Lacroix, Encapsulation of bifidobacteria in whey protein-based microcapsules and survival in simulated gastrointestinal conditions and in yoghurt. Int. Dairy J. 14, 505–515 (2004)

    CAS  Google Scholar 

  24. H. Michida, S. Tamalampudi, S.S. Pandiella, C. Webb, H. Fukuda, A. Kondo, Effect of cereal extracts and cereal fiber on viability of Lactobacillus plantarum under gastrointestinal tract conditions. Biochem. Eng. J. 28, 73–78 (2006)

    Google Scholar 

  25. Y. Ma, J.C. Pacan, Q. Wang, P.M. Sabour, X. Huang, Y. Xu, Enhanced alginate microspheres as means of oral delivery of bacteriophage for reducing Staphylococcus aureus intestinal carriage. Food Hydrocoll. 26, 434–440 (2012)

    CAS  Google Scholar 

  26. W.P. Charteris, P.M. Kelly, L. Morelli, J.K. Collins, Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J. Appl. Microbiol. 84, 759–768 (1998)

    CAS  PubMed  Google Scholar 

  27. Y. He, Z. Wu, L. Tu, Y. Han, G. Zhang, C. Li, Encapsulation and characterization of slow-release microbial fertilizer from the composites of bentonite and alginate. Appl Clay Sci. 109, 68–75 (2015)

    Google Scholar 

  28. L.X. Pan, X.J. Fang, Z. Yu, Y. Xin, X.Y. Liu, L.E. Shi, Z.X. Tang, Encapsulation in alginate–skim milk microspheres improves viability of Lactobacillus bulgaricus in stimulated gastrointestinal conditions. Int. J. Food Sci. Nutr. 64, 380–384 (2013)

    CAS  PubMed  Google Scholar 

  29. S. Benita, Kinetic model identification of drug release from microcapsules using the nonlinear regression search procedure. Appl. Biochem. Biotechnol. 10, 255–258 (1984)

    CAS  PubMed  Google Scholar 

  30. T. Higuchi, Mechanism of sustained-action medication. Theoretical analysis of rate of release of solid drugs dispersed in solid matrices. ‎J. Pharm. Sci. 52, 1145–1149 (1963)

    CAS  PubMed  Google Scholar 

  31. P.L. Ritger, N.A. Peppas, A simple equation for description of solute release I. Fickian and non-Fickian release from non-swellable devices in the form of slabs, spheres, cylinders or discs. J. Control. Release. 5, 23–36 (1987)

    CAS  Google Scholar 

  32. S. Argin, P. Kofinas, Y.M. Lo, The cell release kinetics and the swelling behavior of physically crosslinked xanthan–chitosan hydrogels in simulated gastrointestinal conditions. Food Hydrocoll. 40, 138–144 (2014)

    CAS  Google Scholar 

  33. H. İspirli, E. Dertli, Isolation and identification of exopolysaccharide producer lactic acid bacteria from Turkish yogurt. J Food Process. Preserv. 42, 13351 (2018)

    Google Scholar 

  34. L. Ai, Q. Guo, H. Ding, B. Guo, W. Chen, S.W. Cui, Structure characterization of exopolysaccharides from Lactobacillus casei LC2W from skim milk. Food Hydrocoll. 56, 134–143 (2016)

    CAS  Google Scholar 

  35. Y. Wang, C. Li, P. Liu, Z. Ahmed, P. Xiao, X. Bai, Physical characterization of exopolysaccharide produced by Lactobacillus plantarum KF5 isolated from Tibet Kefir. Carbohydr. Polym. 82, 895–903 (2010)

    CAS  Google Scholar 

  36. G. Hebrard, V. Hoffart, E. Beyssac, J.M. Cardot, M. Alric, M. Subirade, Coated whey protein/alginate microparticles as oral controlled delivery systems for probiotic yeast. J. Microencapsul. 27, 292–302 (2010)

    CAS  PubMed  Google Scholar 

  37. M. Hosseini Nezhad, M.A. Hussain, M.L. Britz, Stress responses in probiotic Lactobacillus casei. Crit. Rev. Food Sci. Nutr. 55, 740–749 (2015)

    CAS  PubMed  Google Scholar 

  38. K. Abdhul, M. Ganesh, S. Shanmughapriya, M. Kanagavel, K. Anbarasu, K. Natarajaseenivasan, Antioxidant activity of exopolysaccharide from probiotic strain Enterococcus faecium (BDU7) from Ngari. Int. J. Biol. Macromol. 70, 450–454 (2014)

    CAS  PubMed  Google Scholar 

  39. A. Sohail, M.S. Turner, A. Coombes, T. Bostrom, B. Bhandari, Survivability of probiotics encapsulated in alginate gel microbeads using a novel impinging aerosols method. Int. J. Food Microbiol. 145, 162–168 (2011)

    CAS  PubMed  Google Scholar 

  40. D. Guerin, J.C. Vuillemard, M. Subirade, Protection of bifidobacteria encapsulated in polysaccharide-protein gel beads against gastric juice and bile. J. Food Prot. 66, 2076–2084 (2003)

    CAS  PubMed  Google Scholar 

  41. K. Feng, R.M. Huang, R.Q. Wu, Y.S. Wei, M.H. Zong, R.J. Linhardt, H. Wu, A novel route for double-layered encapsulation of probiotics with improved viability under adverse conditions. Food Chem. 310, 125977 (2020)

    CAS  PubMed  Google Scholar 

  42. M. Afzaal, F. Saeed, M.U. Arshad, M.T. Nadeem, M. Saeed, T. Tufail, The effect of encapsulation on the stability of probiotic bacteria in ice cream and simulated gastrointestinal conditions. Probiotics Antimicrob Proteins. 11, 1348–1354 (2019)

    CAS  PubMed  Google Scholar 

  43. W.K. Ding, N.P. Shah, Effect of various encapsulating materials on the stability of probiotic bacteria. J. Food Sci. 74, 100–107 (2009)

    Google Scholar 

  44. A.B. Shori, Microencapsulation improved probiotics survival during gastric transit. HAYATI J. Biosci. 24, 1–5 (2017)

    Google Scholar 

  45. P. Darjani, M.H. Nezhad, R. Kadkhodaee, E. Milani, Influence of prebiotic and coating materials on morphology and survival of a probiotic strain of Lactobacillus casei exposed to simulated gastrointestinal conditions. LWT Food Sci. Technol. 73, 162–167 (2016)

    CAS  Google Scholar 

  46. Q. Zou, J. Zhao, X. Liu, F. Tian, H. Zhang, H. Zhang, W. Chen, Microencapsulation of Bifidobacterium bifidum F-35 in reinforced alginate microspheres prepared by emulsification/internal gelation. Int. J. Food Sci. Technol. 46, 1672–1678 (2011)

    CAS  Google Scholar 

  47. B. Ismail, K.M. Nampoothiri, Exopolysaccharide production and prevention of syneresis in starch using encapsulated probiotic Lactobacillus plantarum. Food Technol. Biotechnol. 48, 484–489 (2010)

    CAS  Google Scholar 

  48. M. Afzaal, F. Saeed, H. Ateeq, A. Ahmed, A. Ahmad, T. Tufail, Z. Ismail, F.M. Anjum, Encapsulation of Bifidobacterium bifidum by internal gelation method to access the viability in cheddar cheese and under simulated gastrointestinal conditions. Food Sci. Nutr. 8, 1–9 (2020)

    Google Scholar 

  49. C. González-Ferrero, J.M. Irache, B. Marín-Calvo, L. Ortiz-Romero, R. Virto-Resano, C.J. González-Navarro, Encapsulation of probiotics in soybean protein-based microparticles preserves viable cell concentration in foods all along the production and storage processes. J. Microencapsul. 37, 242–253 (2020)

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marzieh Hosseininezhad.

Ethics declarations

Conflict of interest

The authors declare that they have no relevant conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abedfar, A., Hosseininezhad, M., Sadeghi, A. et al. Comparative survival of exopolysaccharide encapsulated Lactobacillus plantarum and Pediococcus pentosaceus in simulated gastrointenstinal conditions and storage time. Food Measure 15, 594–603 (2021). https://doi.org/10.1007/s11694-020-00664-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11694-020-00664-1

Keywords

Navigation