Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics
Abstract
:1. Introduction
2. Probiotics
2.1. Probiotics, Basic Concepts
2.2. Probiotics as an Alternative Therapy
3. Biofilms of Lactobacillus
3.1. Biofilms, Basic Concepts
3.2. Biofilms and Lactobacillus rhamnosus
3.3. Biofilms and Lactobacillus plantarum
3.4. Biofilms and Lactobacillus reuteri
3.5. Biofilms and Lactobacillus fermentum
4. Development of New Technologies (Probiotic Encapsulation)
5. Conclusions and Projections
Author Contributions
Conflicts of Interest
References
- FAO/WHO. Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food; FAO/WHO: London, UK, 2002. [Google Scholar]
- Ayala, G.; Escobedo-Hinojosa, W.I.; Cruz-Herrera, C.F.; Romero, I. Exploring alternative treatments for Helicobacter pylori infection. World J. Gastroenterol. 2014, 20, 1450–1469. [Google Scholar] [CrossRef] [PubMed]
- Lepargneur, J.P.; Rousseau, V. Protective role of the Doderlein flora. J. Gynecol. Obstet. Biol. Reprod. 2002, 31, 485–494. [Google Scholar]
- Costerton, J.W.; Stewwart, P.S.; Greenberg, E.P. Bacterial biofilms: A common cause of persistent infections. Science 1999, 284, 1318–1322. [Google Scholar] [CrossRef] [PubMed]
- Sarxelin, M.; Tynkkynen, S.; Mattila-sandholm, T.; Vos, W.M. Probiotic and other functional microbes: From markets to mechanisms. Curr. Opin. Microbiol. 2005, 16, 204–211. [Google Scholar]
- Lewis, K. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 2001, 45, 999–1007. [Google Scholar] [CrossRef] [PubMed]
- Shauder, S.; Shokat, K.; Surette, M.G.; Bassler, B.L. The luxS family of bacterial autoinducers: Biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 2001, 41, 463–476. [Google Scholar] [CrossRef]
- Phillips, P.L.; Yang, Q.; Davis, S.; Sampson, E.M.; Azeke, J.I.; Hamad, A. Antimicrobial dressing efficacy against mature Pseudomonas aeruginosa biofilm on porcine skin explants. Int. Wound J. 2013, 12, 469–483. [Google Scholar] [CrossRef] [PubMed]
- Martín, M.J.; Morales, M.E.; Gallardo, V.; Ruiz, M.A. Técnicas de microencapsulación: Una propuesta para microencapsular probióticos. ARS Pharm. 2009, 50, 43–50. [Google Scholar]
- Cheow, W.S.; Hadinoto, K. Biofilm-Like Lactobacillus rhamnosus probiotics encapsulated in alginate and carrageenan microcapsules exhibiting enhanced thermotolerance and freeze-drying resistance. Biomacromolecules 2013, 14, 3214–3222. [Google Scholar] [CrossRef] [PubMed]
- Metchnikoff, E. Optimistic Studies of the Prolongation of Life; Putman’s Sons: New York, NY, USA, 1998; pp. 161–183. [Google Scholar]
- Menrad, K. Markey and marketing of functional food in Europe. J. Food Eng. 2003, 56, 181–188. [Google Scholar] [CrossRef]
- Krasaekoopt, W.; Bhandari, B.; Deeth, H. Evaluation of encapsulation techniques of probiotics for yoghurt. Int. Dairy J. 2003, 13, 3–13. [Google Scholar] [CrossRef]
- Lane, D.P.; Crawford, L.V. T antigen bound to a host protein in SV40-transformed cells. Nature 1979, 278, 261–263. [Google Scholar] [CrossRef] [PubMed]
- Fuller, R.; Brooker, B.E. Lactobacilli which attach to the crop epithelium of the fowl. Am. J. Clin. Nutr. 1974, 27, 1305–1312. [Google Scholar] [PubMed]
- Lee, Y.K.; Salminen, S. Handbook of Probiotics and Prebiotics, 2nd ed.; Johns Wiley & Sons: Hoboken, NJ, USA, 2008; p. 5. [Google Scholar]
- Salinitro, J.P.; Blake, I.G.; Muirhead, P.A. Isolation and identification of fecal bacteria from adult swine. Appl. Environ. Microb. 1977, 33, 79–84. [Google Scholar]
- Holzapfel, W.H.; Haberer, P.; Geisen, R.; Björkroth, J.; Schillinger, U. Taxonomy and important features of probiotic microorganisms in food and nutrition. Am. J. Clin. Nutr. 2001, 73, 365–373. [Google Scholar]
- Figueroa-González, I.; Quijano, G.; Ramírez, G.; Cruz-Guerrero, A. Probiotics and prebiotics—Perpectives and challenges. J. Sci. Food Agric. 2011, 91, 1341–1348. [Google Scholar] [CrossRef] [PubMed]
- Preedy, V.; Ross, R. Probiotics and Prebiotics for promoting health: Through gut microbiota. In Probiotics, Prebiotics, and Synbiotics: Bioactive Foods in Health Promotion, 1st ed.; Ross, R., Preedy, V., Eds.; Elsevier: London, UK, 2016; Volume 1, p. 79. [Google Scholar]
- Chenoll, E.; Casinos, B.; Bataller, E.; Astals, P.; Echevarría, J.; Iglesias, J.R.; Balbarie, P.; Ramón, D.; Genovés, S. Novel probiotic Bifidobacterium bifidum CECT 7366 strain active against the pathogenic bacterium Helicobacter pylori. Appl. Environ. Microbiol. 2011, 77, 1335–1343. [Google Scholar] [CrossRef] [PubMed]
- Johnson-Henry, K.C.; Mitchell, D.J.; Avitzur, Y.; Galindo-Mata, E.; Jones, N.L.; Sherman, P.M. Probiotics reduce bacterial colonization and gastric inflammation in H. pylori-infected mice. Dig. Dis. Sci. 2004, 49, 1095–1102. [Google Scholar] [CrossRef] [PubMed]
- Patel, A.; Shah, N.; Prajapati, J.B. Clinical appliance of probiotics in the treatment of Helicobacter pylori infection—A brief review. J. Microbiol. Immunol. Infect. 2013, 47, 429–437. [Google Scholar] [CrossRef] [PubMed]
- Mastroeni, P.; Maskell, D. Salmonella Infections: Clinical, Immunological, and Molecular Aspects; Cambridge University Press: Cambridge, UK, 2006. [Google Scholar]
- Castillo, N.A.; Moreno de LeBlanc, A.; Maldonado, C.; Perdigón, G. Probiotics: Analternative strategy for combating salmonelosis Immune mechanisms involved. Food Res. Int. 2012, 45, 831–841. [Google Scholar] [CrossRef]
- Hart, C.; Batt, R.; Saunders, J. Diarrhoea caused by Escherichia coli. Ann. Trop. Paediatr. 1993, 13, 121–131. [Google Scholar] [CrossRef] [PubMed]
- Reid, G.; Burton, J. Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect. 2002, 4, 319–324. [Google Scholar] [CrossRef]
- Krogfelt, K.; Bergmans, H.; Klemm, P. Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect. Immun. 1990, 58, 1995–1998. [Google Scholar] [PubMed]
- Adlerberth, I.; Ahrne, S.; Johansson, M.L.; Molin, G.; Hanson, L.A.; Wold, A.E. A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29. Appl. Environ. Microbiol. 1996, 62, 2244–2251. [Google Scholar] [PubMed]
- Wanke, M.; Szajewska, H. Probiotics for preventing healthcare-associated diarrhea in children: A meta-analysis of randomized controlled trials. Pediatr. Polska 2014, 89, 8–16. [Google Scholar] [CrossRef]
- Delgado, S.; O’Sullivan, E.; Fitzgerald, G.; Mayo, B. Subtractive screening for probiotic properties of lactobacillus species from the human gastrointestinal tract in the search for new probiotics. J. Food Sci. 2007, 72, 310–315. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.; Griffiths, M.W.; Wu, P.; Wang, H.; Zhang, X.; Li, P. Enterococcus faecium LM-2, a multi-bacteriocinogenic strain naturally occurring in “Byaslag”, a traditional cheese of Inner Mongolia in China. Food Control 2011, 22, 283–289. [Google Scholar] [CrossRef]
- Gobbato, N.; Maldonado, C.; Perdigón, G. Study of some of the mechanisms involved in the prevention against Salmonella enteritidis serovar Typhimurium infection by lactic acid bacteria. Food Agric. Immunol. 2008, 19, 11–23. [Google Scholar] [CrossRef]
- Spinler, J.K.; Rossa, C.L.; Savidgea, T.C. Probiotics as adjunctive therapy for preventing Clostridium difficile infection—What are we waiting for? Anaerobe 2016. [Google Scholar] [CrossRef] [PubMed]
- Madden-Fuentes, R.J.; Arshad, M.; Ross, S.S.; Seed, P.C. Efficacy of Fluoroquinolone/Probiotic combination therapy for recurrent urinary tract infection in children: A retrospective analysis. Clin. Ther. 2015, 37, 2143–2147. [Google Scholar] [CrossRef] [PubMed]
- Zobell, C.; Meyer, K. Reduction of nitrates by representatives of the Brucella group. Proc. Soc. Exp. Biol. Med. 1931, 29, 116–118. [Google Scholar] [CrossRef]
- Probert, H.; Gibson, G. Bacterial biofilms in the human gastrointestinal tract. Curr. Issues Intest. Microbiol. 2002, 3, 23–27. [Google Scholar] [PubMed]
- Donlan, R.M.; Costerton, J.W. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15, 167–193. [Google Scholar] [CrossRef] [PubMed]
- Donlan, R.M. Biofilms: Microbial life on surfaces. Emerg. Infect. Dis. 2002, 8, 881–890. [Google Scholar] [CrossRef] [PubMed]
- Terraf, M.C.; Juarez, M.S.; Nader-Macias, M.E.; Silva, C. Screening of biofilm formation by beneficial vaginal lactobacilli and influence of culture media components. J. Appl. Microbiol. 2012, 113, 1517–1529. [Google Scholar] [CrossRef] [PubMed]
- Stoodley, P.; Sauer, K.; Davies, D.G.; Costerton, J.W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 2002, 56, 187–209. [Google Scholar] [CrossRef] [PubMed]
- Chmielewski, R.A.N.; Frank, J.F. A predictive model for heat inactivation of Listeria monocytogenes biofilm on buna-N rubber. LWT Food Sci. Technol. 2006, 39, 11–19. [Google Scholar] [CrossRef]
- Costerton, J.W.; Lewandowski, Z.; Debeer, D.; Caldwell, D.; Korber, D. Biofilms, the customized microniche. J. Bacteriol. 1994, 176, 2137–2142. [Google Scholar] [PubMed]
- Sauer, K.; Camper, A.K.; Ehrlich, G.D.; Costerton, J.W.; Davies, D.G. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Bacteriology 2002, 184, 1140–1154. [Google Scholar] [CrossRef]
- Post, J.C.; Stoodley, P.; Hall-Stoodley, L.; Ehrlich, G.D. The role of biofilms in otolaryngologic infections. Curr. Opin. Otolaryngol. Head Neck Surg. 2004, 12, 185–190. [Google Scholar] [CrossRef] [PubMed]
- Lebeer, S.; Verhoeven, T.L.A.; Perea Velez, M.; Vanderleyden, J.; De Keersmaecker, S.C.J. Impact of enviromental and genetic factor son biofilms formation by the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 2007, 73, 6768–6775. [Google Scholar] [CrossRef] [PubMed]
- Bujnakova, D.; Kmet, V. Functional properties of Lactobacillus strains isolated from dairy products. Folia Microbiol. 2012, 57, 263–267. [Google Scholar] [CrossRef] [PubMed]
- Kubota, H.; Senda, S.; Nomura, N.; Tokuda, H.; Uchiyama, H. Biofilm formation by lactic acid bacteria and resistance to environmental stress. J. Biosci. Bioeng. 2008, 106, 381–386. [Google Scholar] [CrossRef] [PubMed]
- Kubota, H.; Senda, S.; Tokuda, H.; Uchiyama, H.; Nomura, N. Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiol. 2009, 26, 592–597. [Google Scholar] [PubMed]
- Jones, S.; Versalovic, J. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 2009, 9, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Ambalam, P.; Kiran, K.; Nilsson, I.; Wadstrom, T.; Ljungh, A. Bile stimulates cell surface hydrophobicity, Congo red binding and biofilm formation of Lactobacillus strains. FEMS Microbiol. Lett. 2012, 333, 10–19. [Google Scholar] [CrossRef] [PubMed]
- Aoudia, N.; Rieu, A.; Briandet, R.; Deschamps, J.; Chluba, J.; Jego, G.; Garrido, C.; Guzzo, J. Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: Effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol. 2016, 53, 51–59. [Google Scholar] [CrossRef] [PubMed]
- Fernández, M.; Smid, E.; Abee, T.; Nierop, M. Characterization of biofilms formed by Lactobacillus plantarum WCFS1 and food spoilage isolates. Int. J. Food Microbiol. 2015, 207, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Walencka, E.; Rozalska, S.; Sadowska, B.; Rozalska, B. The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol. 2008, 53, 61–66. [Google Scholar] [CrossRef] [PubMed]
- Fracchia, L.; Cavallo, M.; Allegrone, G.; Martinotti, M. A Lactobacillus derived biosurfactant inhibits biofilm formation of human pathogenic Candida albicans biofilm producers. Curr. Res. Technol. Educ. Top. Appl. Microbiol. Microb. Biotechnol. 2010, 2, 827–837. [Google Scholar]
- Ramos, A.; Sesto Cabral, M.; Noseda, D.; Bosch, A.; Yantorno, O.; Valdez, J. Antipathogenic properties of Lactobacillus plantarum on Pseudomonas aeruginosa: The potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair Regen. 2012, 20, 552–562. [Google Scholar] [CrossRef] [PubMed]
- Alander, M.; Satokari, R.; Korpela, R.; Saxelin, M.; Vilpponen-Salmela, T.; Mattila-Sandholm, T.; von Wright, A. Persistence of Colonization of Human Colonic Mucosa by a Probiotic Strain, Lactobacillus rhamnosus GG, after Oral Consumption. Appl. Environ. Microbiol. 1999, 65, 351–354. [Google Scholar] [PubMed]
- Leeber, S.; Verhoeven, T.L.A.; Francius, G.; Shoofs, G.; Lambrichts, I.; Dufrene, Y.; Vnaderleyden, J.; De Keersmaecker, S.C.J. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl. Environ. Microbiol. 2009, 75, 3554–3563. [Google Scholar] [CrossRef] [PubMed]
- Velez, M.P.; Verhoeven, T.L.A.; Draing, C.; Von Aulock, S.; Pfitzenmaier, M.; Geyer, A.; Lambrichts, I.; Grangette, C.; Pot, B.; Vanderleyden, J.; et al. Functional analysis of D-Alanylation, in the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 2007, 73, 3595–3604. [Google Scholar] [CrossRef] [PubMed]
- Leccese, M.; Juárez, M.; Rault, L.; Le Loir, Y.; Even, S.; Nader-Macías, M. Biofilms of vaginal Lactobacillus rhamnosus CRL 1332: Kinetics of formation and matrix chatecterization. Arch. Microbiol. 2016, 198, 689–700. [Google Scholar]
- Lebeer, S.; Keersmaecker, S.; Tine, L.; Fadda, A.; Marchal, K.; Vanderlen, J. Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus. Appl. Environ. Microbiol. 2008, 74, 4711–4718. [Google Scholar] [CrossRef] [PubMed]
- Simoes, M.; Bennett, R.; Rosa, E. Understanding antimicrobial activities of phytochemicals against multidrug resistant bacteria and biofilms. Nat. Prod. Rep. 2009, 26, 746–757. [Google Scholar] [CrossRef] [PubMed]
- Kinoshita, H.; Uchida, H.; Kawai, Y. Cell surface Lactobacillus plantarum LA 318 glyceraldehyde-3-phosphate dehydrogenase (GAPDH) adheres to human colonic mucin. J. Appl. Microbiol. 2008, 104, 1667–1674. [Google Scholar] [CrossRef] [PubMed]
- Anderson, R.; Cookson, A.; McNabb, W.; Kelly, W.; Roy, N. Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS. Microbiol. Lett. 2010, 309, 184–192. [Google Scholar] [CrossRef] [PubMed]
- Kaushik, J.; Kumar, A.; Duary, R.; Mohanty, A.; Grover, S. Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS ONE 2009, 4, e8099. [Google Scholar] [CrossRef] [PubMed]
- Sengupta, R.; Altermann, E.; Anderson, R.; McNabb, W.; Moughan, P.; Roy, N. The Role of Cell Surface Architecture of Lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediat. Inflamm. 2013, 2013, 237921. [Google Scholar] [CrossRef] [PubMed]
- Sugimura, Y.; Hagi, T.; Hoshino, T. Correlation between in vitro mucus adhesion and the in vivo colonization ability of lactic acid bacteria: Screening of new candidate carp probiotics. Biosci. Biotechnol. Biochem. 2011, 75, 511–515. [Google Scholar] [CrossRef] [PubMed]
- Vastano, V.; Pagano, A.; Fusco, A.; Merola, G.; Sacco, M.; Donnarumma, G. The Lactobacillus plantarum Eno A1 Enolase is involved in immunostimulation of Caco-2 Cells and in biofilm development. Adv. Exp. Med. Biol. 2016, 897, 33–44. [Google Scholar] [PubMed]
- Calasso, M.; Di Cagno, R.; De Angelis, M.; Campanella, D.; Minervini, F.; Gobbetti, M. Effects of the peptide pheromone Plantaricin A and cocultivation with Lactobacillus sanfranciscensis DPPMA174 on the exoproteome and the adhesion capacity of Lactobacillus plantarum DC400. Environ. Microbiol. 2013, 79, 2657–2669. [Google Scholar] [CrossRef] [PubMed]
- De Angelis, M.; Siragusa, S.; Campanella, D.; Di Cagno, R.; Gobbetti, M. Comparative proteomic analysis of biofilm and planktonic cells of Lactobacillus plantarum DB200. Proteomics 2015, 15, 2244–2257. [Google Scholar] [CrossRef] [PubMed]
- Su, M.S.; Gänzle, M. Novel two-component regulatory systems play a role in biofilm formation of Lactobacillus reuteri rodent isolate 100-23. Microbiology 2014, 160, 795–806. [Google Scholar] [CrossRef] [PubMed]
- McMillan, A.; Dell, M.; Zellar, M.; Cribby, S.; Martz, S. Disruption of urogenital biofilms by lactobacilli. Colloids Surf. B 2011, 86, 58–64. [Google Scholar] [CrossRef] [PubMed]
- Frese, S.; Benson, A.; Tannock, G.; Loach, D.; Kim, J. The Evolution of host specialization in the vertebrate Gut symbiont Lactobacillus reuteri. PLoS Genet. 2011, 7, e1001314. [Google Scholar] [CrossRef] [PubMed]
- Walter, J.; Brittonb, R.; Roosc, S. Host-microbial symbiosis in the vertébrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc. Natl. Acad. Sci. USA 2011, 108, 4645–4652. [Google Scholar] [CrossRef] [PubMed]
- Wegmann, U.; MacKenzie, D.; Zheng, J.; Goesmann, A.; Roos, S.; Swarbreck, D.; Walter, J.; Crossman, L.; Juge, N. The pan-genome of Lactobacillus reuteri strains originating from the pig gastrointestinal tract. BMC Genom. 2015, 16, 1023–1041. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olson, J.; Rager, T.; Navarro, J.; Mashburn-Warren, L.; Goodman, S.; Besner, G. Harvesting the benefits of biofilms: A novel probiotic delivery system for the prevention of necrotizing enterocolitis. J. Pedriatr. Surg. 2016, 51, 936–941. [Google Scholar] [CrossRef] [PubMed]
- Mikelsaar, M.; Zilmer, M. Lactobacillus fermentum ME-3-an antimicrobial an antioxidative. Microb. Ecol. Health D 2009, 21, 1–27. [Google Scholar] [CrossRef] [PubMed]
- Rybalchenko, O.V.; Bondarenko, V.M.; Orlova, O.G.; Markov, A.G.; Amasheh, S. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation. Arch. Microbiol. 2015, 197, 1027–1032. [Google Scholar] [CrossRef] [PubMed]
- Heinemann, C.; van Hylckama Vlieg, J.; Janssen, D.; Busscher, H.; van der Mei, H.; Reid, G. Purification and characterization of a surface-binding protein from Lactobacillus fermentum RC-14 that inhibits adhesion of Enterococcus faecalis 1131. FEMS Microbiol. Lett. 2000, 190, 177–180. [Google Scholar] [CrossRef] [PubMed]
- Anukam, K.; Reid, G. Lactobacillus plantarum and Lactobacillus fermentum with probiotic potentials isolated from the vagina of healthy Nigerian women. Res. J. Microbiol. 2007, 2, 81–87. [Google Scholar]
- Kaur, B.; Balgir, P.; Mittu, B.; Chauhan, A.; Kumar, B. Purification and physicochemical characterization of anti-Gardnerella vaginalis bacteriocin hv6b produced by Lactobacillus fermentum isolate from human vaginal ecosystem. Am. J. Biochem. Mol. Biol. 2013, 3, 91–100. [Google Scholar] [CrossRef]
- De Vos, P.; Fass, M.; Spasojevic, M.; Sikkema, J. Encapsulation for preservation of functionality and targeted delivery of bioactive food components. Int. Dairy J. 2010, 20, 292–302. [Google Scholar] [CrossRef]
- Zárate, G.; Juárez, M.; Nader-Macías, M. Effect of some pharmaceutical excipients on the survival of probiotic vaginal lactobacilli. Can. J. Microbiol. 2005, 51, 483–489. [Google Scholar] [CrossRef] [PubMed]
- Klayraung, S.; Viernstein, H.; Okonogi, S. Development of tablet containing probiotics: Effects of formulation and processing parameters on bacterial viability. Int. J. Pharm. 2008, 370, 54–60. [Google Scholar] [CrossRef] [PubMed]
- Burgain, J.; Gaiani, C.; Linder, M.; Scher, J. Encapsulation of probiotic living cells: From laboratory scale to industrial applications. J. Food Eng. 2011, 104, 467–493. [Google Scholar] [CrossRef]
- Kiew, T.; Cheow, W.; Hadinoto, K. Importance of biofilm age and growth medium on the viability of probiotics capsules containing Lactobacillus rhamnosus GG biofilm. Food Sci. Technol. 2014, 59, 956–963. [Google Scholar] [CrossRef]
- Cheow, W.; Kiew, T.; Hadinoto, K. Controlled release of Lactobacillus rhamnosus biofilm probiotics from alginate-locust bean gum microcapsules. Carbohydr. Polym. 2014, 103, 587–595. [Google Scholar] [CrossRef] [PubMed]
- Cheow, W.; Kiew, T.; Hadinoto, K. Effect of adding resistant and waxy starches on cell density and survival of encapsulated biofilm of Lactobacillus rhamnosus GG probiotics. Food Sci. Technol. 2016, 69, 497–505. [Google Scholar] [CrossRef]
- Kailasapathy, K. Microencapsulation of probiotic bacteria: Technology and potential applications. Curr. Issues Intest. Microbiol. 2002, 3, 39–48. [Google Scholar] [PubMed]
- Rathore, S.; Mahendrakumar, P.; Liew, C.; Chan, L.; Sia, P. Microencapsulation of microbial cells. J. Food Eng. 2012, 116, 369–381. [Google Scholar] [CrossRef]
- Mortazavian, A.; Ehsani, M.; Azizi, A.; Razavi, S.; Sohrabvandi, S.; Reinheimer, J. Viability of calcium-alginate-microencapsulates probiotic bacteria in Iranian yogurt drink (Doogh) during refrigerated storage and under simulated gastrointestinal conditions. Aust. J. Dairy Technol. 2008, 63, 25–30. [Google Scholar]
- Chávarri, M.; Marañón, I.; Ares, R.; Ibáñez, F.; Marzo, F.; Villarán, C. Microencapsulation of a probiotic and prebiotic in alginate-chitosan capsules improves survival in simulated gastro-intestinal conditions. Int. J. Food Microbiol. 2010, 142, 185–189. [Google Scholar] [CrossRef] [PubMed]
- Khalil, M.; El-Sheekh, M.; El-Adawi, H.; El-Deeb, N.; Hussein, M. Efficacy of microencapsulated lactic acid bacteria in Helicobacter pylori eradication therapy. J. Res. Med. Sci. 2015, 20, 950–957. [Google Scholar] [CrossRef] [PubMed]
- Kammani, P.; Kumar, R.; Yuvaraj, N.; Paari, K.; Pattukumar, V.; Arul, V. Cryopreservation and microencapsulation of probiotic in alginate-chitosan capsules improves survival in simulated gastrointestinal conditions. Biotechnol. Bioprocess Eng. 2011, 16, 1106–1114. [Google Scholar] [CrossRef]
- Anal, A.; Bhopatk, D.; Tokura, S.; Tamura, H.; Stevens, W. Chitosan-Alginate multilayer beads for gastric passage and controlled intestinal release of protein. Drug Dev. Ind. Pharm. 2003, 29, 713–724. [Google Scholar] [CrossRef] [PubMed]
- Arora, S.; Budhiraja, R. Chitosan-alginate microcapsules of amoxicillin for gastric stability and mucoadhesion. J. Adv. Pharm. Technol. Res. 2012, 3, 68–74. [Google Scholar] [PubMed]
- Du, J.; Dai, J.; Liu, J.; Dankovichb, T. Novel pH-sensitive polyelectrolyte carboxymethyl Konjac glucomannan-chitosan beads as drug carriers. React. Funct. Polym. 2006, 66, 1055–1061. [Google Scholar] [CrossRef]
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Salas-Jara, M.J.; Ilabaca, A.; Vega, M.; García, A. Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics. Microorganisms 2016, 4, 35. https://doi.org/10.3390/microorganisms4030035
Salas-Jara MJ, Ilabaca A, Vega M, García A. Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics. Microorganisms. 2016; 4(3):35. https://doi.org/10.3390/microorganisms4030035
Chicago/Turabian StyleSalas-Jara, María José, Alejandra Ilabaca, Marco Vega, and Apolinaria García. 2016. "Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics" Microorganisms 4, no. 3: 35. https://doi.org/10.3390/microorganisms4030035