4,830
Views
28
CrossRef citations to date
0
Altmetric
Original Article

Survival and stability of free and encapsulated probiotic bacteria under simulated gastrointestinal and thermal conditions

ORCID Icon, ORCID Icon, , , , , & show all
Pages 1899-1912 | Received 12 Sep 2019, Accepted 16 Sep 2020, Published online: 26 Oct 2020

References

  • Hill, C.; Guarner, F.; Reid, G.; Gibson, G.-R.; Merenstein, D.-J.; Pot., B.; Calder, P.-C. Expert Consensus Document: The Int. Scientific Association for Probiotics and Prebiotics Consensus Statement on the Scope and Appropriate Use of the Term Probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11(8), 506.
  • Hashemi, M.; Gheisari, H.-R.; Shekarforoush, S. Preparation and Evaluation of Low‐calorie Functional Ice Cream Containing Inulin, Lactulose and Bifidobacterium Lactis. Int. J. Dairy Technol. 2015, 68(2), 183–189. DOI: 10.1111/1471-0307.12173.
  • Burgain, J.; Gaiani, C.; Linder, M.; Scher, J. Encapsulation of Probiotic Living Cells: From Laboratory Scale to Industrial Applications. J. Food Eng. 2011, 104(4), 467–483.
  • Champagne, C.-P.; da Cruz, A.-G.-M. Daga Strategies to Improve the Functionality of Probiotics in Supplements and Foods Current. Opin. Food Sci. 2018, 22, 160–166. DOI: 10.1016/j.cofs.2018.04.008.
  • Aryana, K.-J.; Olson, D.-W. A 100-year Review: Yogurt and Other Cultured Dairy Products. J Dairy sci. 2017, 100(12), 9987–10013.
  • Kanmani, P.; Kumar, R.-S.; Yuvaraj, N.; Paari, K.-A.; Pattukumar, V.; Arul, V. Cryopreservation and Microencapsulation of a Probiotic in Alginate-chitosan Capsules Improves Survival in Simulated Gastrointestinal Conditions. Biotechnol. Bioprocess Eng. 2011, 16(6), 1106–1114. DOI: 10.1007/s12257-011-0068-9.
  • Chotiko, A.; Sathivel, S. Development of a Combined Low-methoxyl-pectin and Rice-bran-extract Delivery System to Improve the Viability of Lactobacillus Plantarum under Acid and Bile Conditions. LWT-Food Sci. Technol. 2016, 66, 420–427. DOI: 10.1016/j.lwt.2015.10.058.
  • Shi, L.-E.; Li, Z.-H.; Li, D.-T.; Xu, M.; Chen, H.-Y.; Zhang, Z.-L.; Tang, Z.-X. Encapsulation of Probiotic Lactobacillus Bulgaricus in Alginate–milk Microspheres and Evaluation of the Survival in Simulated Gastrointestinal Conditions. J. Food Eng. 2013, 117(1), 99–104. DOI: 10.1016/j.jfoodeng.2013.02.012.
  • Terpou, A.; Papadaki, A.; Lappa, I. K.; Kachrimanidou, V.; Bosnea, L. A.; Kopsahelis, N. Probiotics in Food Systems: Significance and Emerging Strategies Towards Improved Viability and Delivery of Enhanced Beneficial Value. Nutrients. 2019, 11(7), 1591. DOI: 10.3390/nu11071591.
  • Mirzaei, H.; Pourjafar, H.; Homayouni, A. Effect of Calcium Alginate and Resistant Starch Microencapsulation on the Survival Rate of Lactobacillus Acidophilus La5 and Sensory Properties in Iranian White Brined Cheese. Food Chem. 2012, 132(4), 1966–1970. DOI: 10.1016/j.foodchem.2011.12.033.
  • Boudou, T.; Crouzier, T.; Ren, K.; Blin, G.; Picart, C. Multiple Functionalities of Polyelectrolyte Multilayer Films: New Biomedical Applications. Adv.Mate. 2010, 22(4), 441–467.
  • de Araújo Etchepare, M.; Raddatz, G. C.; de Moraes Flores, É. M.; Zepka, L. Q.; Jacob-Lopes, E.; Barin, J. S.; Ferreira Grosso, C. R.; de Menezes, C. R. Effect of Resistant Starch and Chitosan on Survival of Lactobacillus Acidophilus Microencapsulated with Sodium Alginate. LWT - Food Science and Technology. 2016, 65, 511–517. DOI: 10.1016/j.lwt.2015.08.039.
  • Zanjani, M. A. K.; Ehsani, M. R.; Ghiassi Tarzi, B.; Sharifan, A. Promoting Lactobacillus Casei and Bifidobacterium Adolescentis Survival by Microencapsulation with Different Starches and Chitosan and Poly L‐lysine Coatings in Ice Cream. J. Food Process. Preserv. 2018, 42(1), e13318. DOI: 10.1111/jfpp.13318.
  • Ahmad, M.; Mudgil, P.; Maqsood, S. Camel Whey Protein Microparticles for Safe and Efficient Delivery of Novel Camel Milk Derived Probiotics. LWT. 2019, 108, 81–88. DOI: 10.1016/j.lwt.2019.03.008.
  • Yeung, T.-W.; Arroyo-Maya, I.-J.; McClements, D.-J.; Sela, D.-A. Microencapsulation of Probiotics in Hydrogel Particles: Enhancing Lactococcus Lactis Subsp. Cremoris LM0230 Viability Using Calcium Alginate Beads. Food Funct. 2016, 7(4), 1797–1804. DOI: 10.1039/C5FO00801H.
  • Praepanitchai, O.-A.; Noomhorm, A.; Anal, A.-K. Survival and Behavior of Encapsulated Probiotics (Lactobacillus Plantarum) in Calcium-Alginate-Soy Protein Isolate-Based Hydrogel Beads in Different Processing Conditions (Ph and Temperature) and in Pasteurized Mango Juice. Biomed Res. Int. 2019. DOI: 10.1155/2019/9768152.
  • Singh, M.; Sharma, D.; Chauhan, R.; Goel, G. Skimmed Milk-based Encapsulation for Enhanced Stability and Viability of Lactobacillus Gastricus BTM 7 under Simulated Gastrointestinal Conditions. Probiotics Antimicrob. Proteins. 2019, 11(3), 850–856. DOI: 10.1007/s12602-018-9472-1.
  • Ding, W. K.; Shah, N. P. Survival of Free and Microencapsulated Probiotic Bacteria in Orange and Apple Juices. Int. Food Res. J. 2008, 15(2), 219–232.
  • Kim, S. J.; Cho, S. Y.; Kim, S. H.; Song, O. J.; Shin, I. S.; Cha, D. S.; Park, H. J. Effect of Microencapsulation on Viability and Other Characteristics in Lactobacillus Acidophilus ATCC 43121. LWT Food Sci. Technol. 2008, 41(3), 493–500. DOI: 10.1016/j.lwt.2007.03.025.
  • Brinques, G. B.; Ayub, M. A. Z. Effect of Microencapsulation on Survival of Lactobacillus Plantarum in Simulated Gastrointestinal Conditions, Refrigeration, and Yogurt. J. Food Eng. 2011, 103(2), 123–128. DOI: 10.1016/j.jfoodeng.2010.10.006.
  • Ashwar, B.-A.; Gani, A.; Gani, A.; Shah, A.; Masoodi, F.-A. Production of RS4 from Rice Starch and Its Utilization as an Encapsulating Agent for Targeted Delivery of Probiotics. Food Chem. 2018, 239, 287–294. DOI: 10.1016/j.foodchem.2017.06.110.
  • Pour, -M.-M.; Saberi-Riseh, R.; Mohammadinejad, R.; Hosseini, A. Investigating the Formulation of Alginate-gelatin Encapsulated Pseudomonas Fluorescens (VUPF5 and T17-4 Strains) for Controlling Fusarium Solani on Potato. Int. J. Biol. Macromol. 2019, 133, 603–613. DOI: 10.1016/j.ijbiomac.2019.04.071.
  • El-Shafei, K.; Elshaghabee, -F.-M.-F.; El-Sayed, H.-S.; Kassem, J.-M. Assessment the Viability Properties of Lactobacillus Casei Strain Using Labneh as a Carrier. Acta Scientiarum Polonorum Technologia Alimentaria. 2018, 17(3), 267–276.
  • Moghaddas Kia, E.; Ghasempour, Z.; Ghanbari, S.; Pirmohammadi, R.; Ehsani, A. Development of Probiotic Yogurt by Incorporation of Milk Protein Concentrate (MPC) And‎ Microencapsulated Lactobacillus Paracasei‎ in Gellan-caseinate Mixture. Br. Food J. 2018, 120(7), 1516–1528. DOI: 10.1108/BFJ-12-2017-0668.
  • Horwitz, W.; Chichilo, P.; Reynolds, H. Official Methods of Analysis of the Association of Official Analytical Chemists. Off Methods Anal Assoc Off Anal Chem. 1970.
  • Karimi, R.; Mortazavian, A.-M.; Amiri-Rigi, A. Selective Enumeration of Probiotic Microorganisms in Cheese. Food Microbiol. 2012, 29(1), 1–9. DOI: 10.1016/j.fm.2011.08.008.
  • Akgun, A.; Yazici, F.; Gulec, H.-A. The Combined Effect of Probiotic Cultures and Incubation Final pH on the Quality of Buffalo Milk Yogurt during Cold Storage. Food Sci. Nutr. 2018, 6(2), 492–502. DOI: 10.1002/fsn3.580.
  • Pradeep Prasanna, P.-H.; Charalampopoulos, D. Encapsulation in an Alginate–goats’ Milk–inulin Matrix Improves Survival of Probiotic Bifidobacterium in Simulated Gastrointestinal Conditions and Goats’ Milk Yoghurt. Int. J. Dairy Technol. 2019, 72(1), 132–141. DOI: 10.1111/1471-0307.12568.
  • Volić, M.; Pajić-Lijaković, I.; Djordjević, V.; Knežević-Jugović, Z.; Pećinar, I.; Stevanović-Dajić, Z.; Bugarski, B. Alginate/soy Protein System for Essential Oil Encapsulation with Intestinal Delivery. Carbohydr. Polym. 2018, 200, 15–24. DOI: 10.1016/j.carbpol.2018.07.033.
  • Dias, C.-O.; de Almeida, J.-D.-S.-O.; Pinto, -S.-S.; de Oliveira Santana, F.-C.; Verruck, S.; Müller, C.-M.-O.; Amboni, R.-D.-D.-M.-C. Development and Physico-chemical Characterization of Microencapsulated Bifidobacteria in Passion Fruit Juice: A Functional Non-dairy Product for Probiotic Delivery. Food Biosci. 2018, 24, 26–36. DOI: 10.1016/j.fbio.2018.05.006.
  • Donthidi, A. R.; Tester, R. F.; Aidoo, K. E. Effect of Lecithin and Starch on Alginate-encapsulated Probiotic Bacteria. J. Microencapsulation. 2010, 27(1), 67–77.
  • Huo, W.; Xie, G.; Zhang, W.; Wang, W.; Shan, J.; Liu, H.; Zhou, X. Preparation of a Novel Chitosan-microcapsules/starch Blend Film and the Study of Its Drug-release Mechanism. Int. J. Biol. Macromol. 2016, 87, 114–122. DOI: 10.1016/j.ijbiomac.2016.02.049.
  • Rao, -K.-K.; Naidu, B.-V.-K.; Subha, M.-C.-S.; Sairam, M.; Aminabhavi, T.-M. Novel Chitosan-based pH-sensitive Interpenetrating Network Microgels for the Controlled Release of Cefadroxil. Carbohydr. Polym. 2006, 66(3), 333–344.
  • Paşcalău, V.; Popescu, V.; Popescu, G.-L.; Dudescu, M.-C.; Borodi, G.; Dinescu, A.; Paul, M. The Alginate/k-carrageenan Ratio’s Influence on the Properties of the Cross-linked Composite Films. J. Alloys Compd. 2012, 536, 418–423. DOI: 10.1016/j.jallcom.2011.12.026.
  • Afzaal, M.; Saeed, F.; Arshad, M.-U.; Nadeem, M.-T.; Saeed, M.; Tufail, T. The Effect of Encapsulation on the Stability of Probiotic Bacteria in Ice Cream and Simulated Gastrointestinal Conditions. Probiotics and antimicrobial proteins, 11(4), 1348-1354.
  • Nualkaekul, S.; Lenton, D.; Cook, M. T.; Khutoryanskiy, V. V.; Charalampopoulos, D. Chitosan Coated Alginate Beads for the Survival of Microencapsulated Lactobacillus Plantarum in Pomegranate Juice. Carbohydr. Polym. 2012, 90(3), 1281–1287.
  • Teoh, P. L.; Mirhosseini, S. H.; Mustafa, S.; Manap, M. Y. A. Tolerance of Free and Encapsulated Probiotics Towards Heat Treatment and High Sodium Concentration. J Food Agric Environ. 2011, 9(1), 69–73.
  • Çabuk, B.; Harsa, Ş. T. Protection of Lactobacillus Acidophilus NRRL-B 4495 under in Vitro Gastrointestinal Conditions with Whey Protein/pullulan Microcapsules. J. Biosci. Bioeng. 2015, 120(6), 650–656. DOI: 10.1016/j.jbiosc.2015.04.014.
  • Mokhtari, S.; Khomeiri, M.; Jafari, S. M.; Maghsoudlou, Y.; Ghorbani, M. Descriptive Analysis of Bacterial Profile, Physicochemical and Sensory Characteristics of Grape Juice Containing Saccharomyces Cerevisiae Cell Wall-coated Probiotic Microcapsules during Storage. Int. J. Food Sci. Technol. 2017, 52(4), 1042–1048. DOI: 10.1111/ijfs.13370.
  • Nualkaekul, S., & Charalampopoulos, D. (2011). Survival of Lactobacillus plantarum in model solutions and fruit juices. International Journal of Food Microbiology, 146(2), 111–117 doi:10.1016/j.ijfoodmicro.2011.01.040
  • Rodrigues, D.; Sousa, S.; Rocha-Santos, T.; Silva, J.; Lobo, J. S.; Costa, P.; Amaral, M.; Pintado, M.; Gomes, A.; Malcata, F. Influence of L-cysteine, Oxygen and Relative Humidity upon Survival Throughout Storage of Probiotic Bacteria in Whey Protein-based Microcapsules. Int. Dairy J. 2011, 21(11), 869–876. DOI: 10.1016/j.idairyj.2011.05.005.
  • Yasmin, I.; Saeed, M.; Pasha, I.; Zia, M. A. Development of Whey Protein Concentrate-pectin-alginate Based Delivery System to Improve Survival of B. Longum BL-05 in Simulated Gastrointestinal Conditions. Probiotics Antimicrob. Proteins. 2019, 11(2), 413–426. DOI: 10.1007/s12602-018-9407-x.
  • Huq, T.; Fraschini, C.; Khan, A.; Riedl, B.; Bouchard, J.; Lacroix, M. Alginate Based Nanocomposite for Microencapsulation of Probiotic: Effect of Cellulose Nanocrystal (CNC) and Lecithin. Carbohydr. Polym. 2017, 168, 61–69.
  • Zeashan, M.; Afzaal, M.; Saeed, F.; Ahmed, A.; Tufail, T.; Ahmed, A.; Anjum, F. M. Survival and Behavior of Free and Encapsulated Probiotic Bacteria under Simulated Human Gastrointestinal and Technological Conditions. Food Sci. Nutr. 2020. DOI: 10.1002/fsn3.1531.