Probiotics to counteract biofilm-associated infections: promising and conflicting data

Abstract

There is both conflicting and promising evidence that administration of “good” bacteria, or probiotics, prevents biofilm-related infections. Despite data showing that probiotics contribute to maintaining a healthy gut, a review by Claudia Vuotto and colleagues from the IRCCS Fondazione Santa Lucia, Rome, Italy, suggests that the effects of probiotics on other conditions in which bacteria grow as aggregates in biofilms are unclear. Several lactic-acid producing bacteria benefit the host by reducing the growth of toxic bacteria and stimulating an immune response. However, for the treatment of biofilm-associated oral diseases, genitourinary and wound infections, the effects are highly dependent on the biofilm's composition and the probiotic strain that is used. Further studies are required to identify the most effective strains to eradicate such biofilms and tackle one of the most urgent challenges in anti-bacterial drug development.

Keywords

biofilm / genitourinary tract / gut / infections / oral cavity / probiotics / wounds

References

[1] Metchnikoff E. Optimistic study//Mitchell PC ed. The prolongation of life, 1910 New York 96.

[2] Podolsky S. Cultural divergence: Elie Metchnikoff's Bacillus bulgaricus therapy and his underlying concept of health. Bull Hist Med, 1998, 72(1): 1-27.

[3] Holzapfel WH, Haberer P, Snel J. Overview of gut flora and probiotics. Int J Food Microbiol, 1998, 41(2): 85-101.

[4] Rajilić-Stojanović M. Function of the microbiota. Best Pract Res Clin Gastroenterol, 2013, 27(1): 5-16.

[5] World Health Organization. World Health Organization Report of a Joint FAO/WHO Expert Consultation of Evaluations of Health and Nutritional Properties of Probiotics in Food Including Powder Milk and Live Lactic Acid Bacteria. Geneva: World Health Organization, 2001.

[6] Ng SC, Hart AL, Kamm MA. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis, 2009, 15(2): 300-310.

[7] Mikelsaar M, Lazar V, Onderdonk AB. Do probiotic preparations for humans really have efficacy. Microb Ecol Health Dis, 2011, 22: 10128.

[8] Bertazzoni E, Donelli G, Midtvedt T. Probiotics and clinical effects: is the number what counts. J Chemother, 2013, 25(4): 193-212.

[9] Podolsky SH. Metchnikoff and the microbiome. Lancet, 2012, 380(9856): 1810-1811.

[10] Guandalini S, Pensabene L, Zikri MA. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr, 2000, 30(1): 54-60.

[11] Johnston BC, Goldenberg JZ, Vandvik PO et al. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev 2011; ( 11): CD004827.

[12] Marseglia GL, Tosca M, Cirillo I. Efficacy of Bacillus clausii spores in the prevention of recurrent respiratory infections in children: a pilot study. Ther Clin Risk Manag, 2007, 3(1): 13-17.

[13] Alfaleh K, Anabrees J, Bassler D et al. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev 2011; ( 3): CD005496.

[14] Chapman TM, Plosker GL, Figgitt DP. VSL#3 probiotic mixture: a review of its use in chronic inflammatory bowel diseases. Drugs, 2006, 66(10): 1371-1387.

[15] Wall GC, Schirmer LL, Anliker LE. Pharmacotherapy for acute pouchitis. Ann Pharmacother, 2011, 45(9): 1127-1137.

[16] Donelli G, Vuotto C, Mastromarino P . Phenotyping and genotyping are both essential to identify and classify a probiotic microorganism. Microb Ecol Health Dis 2013; 24: 10.3402/mehd.v24i0.20105.

[17] Aires J, Butel MJ. Proteomics, human gut microbiota and probiotics. Expert Rev Proteomics, 2011, 8(2): 279-288.

[18] Louis P, O’Byrne CP. Life in the gut: microbial responses to stress in the gastrointestinal tract. Sci Prog, 2010, 93(Pt 1): 7-36.

[19] Kamada N, Chen GY, Inohara N. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol, 2013, 14(7): 685-690.

[20] Ruemmele FM, Bier D, Marteau P. Clinical evidence for immunomodulatory effects of probiotic bacteria. J Pediatr Gastroenterol Nutr, 2009, 48(2): 126-141.

[21] Vieira AT, Teixeira MM, Martins FS. The role of probiotics and prebiotics in inducing gut immunity. Front Immunol, 2013, 4: 445.

[22] Mastromarino P, Vitali B, Mosca L. Bacterial vaginosis: a review on clinical trials with probiotics. New Microbiol, 2013, 36(3): 229-238.

[23] Alexandre Y, Le Blay G, Boisramé-Gastrin S. Probiotics: a new way to fight bacterial pulmonary infections. Med Mal Infect, 2014, 44(1): 9-17.

[24] Shida K, Nomoto K. Probiotics as efficient immunopotentiators: translational role in cancer prevention. Indian J Med Res, 2013, 138(5): 808-814.

[25] Serban DE. Gastrointestinal cancers: influence of gut microbiota, probiotics and prebiotics. Cancer Lett, 2014, 345(2): 258-270.

[26] Saha S, Tomaro-Duchesneau C, Tabrizian M. Probiotics as oral health biotherapeutics. Expert Opin Biol Ther, 2012, 12(9): 1207-1220.

[27] Bizzini B, Pizzo G, Scapagnini G. Probiotics and oral health. Curr Pharm Des, 2012, 18(34): 5522-5531.

[28] Teughels W, Newman MG, Coucke W. Guiding periodontal pocket recolonization: a proof of concept. J Dent Res, 2007, 86(11): 1078-1082.

[29] Riccia DN, Bizzini F, Perilli MG. Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis, 2007, 13(4): 376-385.

[30] Maekawa T., Hajishengallis G.. Topical treatment with probioticLactobacillus brevisCD2 inhibits experimental periodontal inflammation and bone loss. Journal of Periodontal Research, 2014, 49(6): 785-791.

[31] Tsubura S, Mizunuma H, Ishikawa S. The effect of Bacillus subtilis mouth rinsing in patients with periodontitis. Eur J Clin Microbiol Infect Dis, 2009, 28(11): 1353-1356.

[32] Mayanagi G, Kimura M, Nakaya S. Probiotic effects of orally administered Lactobacillus salivarius WB21-containing tablets on periodontopathic bacteria: a double-blinded, placebo-controlled, randomized clinical trial. J Clin Periodontol, 2009, 36(6): 506-513.

[33] Grant SS, Hung DT. Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence, 2013, 4(4): 273-283.

[34] Longbottom C, Ekstrand K, Zero D. Novel preventive treatment options. Monogr Oral Sci, 2009, 21: 156-163.

[35] Gopal PK, Prasad J, Smart J. In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int J Food Microbiol, 2001, 67(3): 207-216.

[36] Kravtsov EG, Yermolayev AV, Anokhina IV. Adhesion characteristics of Lactobacillus is a criterion of the probiotic choice. Bull Exp Biol Med, 2008, 145(2): 232-234.

[37] Lasaro MA, Salinger N, Zhang J. F1C fimbriae play an important role in biofilm formation and intestinal colonization by the Escherichia coli commensal strain Nissle 1917. Appl Environ Microbiol, 2009, 75(1): 246-251.

[38] Xu H, Jeong HS, Lee HY. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett Appl Microbiol, 2009, 49(4): 434-442.

[39] Lebeer S, Verhoeven TL, Claes IJ. FISH analysis of Lactobacillus biofilms in the gastrointestinal tract of different hosts. Lett Appl Microbiol, 2011, 52(3): 220-226.

[40] Cheow WS, Hadinoto K. Biofilm-like Lactobacillus rhamnosus probiotics encapsulated in alginate and carrageenan microcapsules exhibiting enhanced thermotolerance and freeze–drying resistance. Biomacromolecules, 2013, 14(9): 3214-3222.

[41] Jones SE, Versalovic J. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol, 2009, 9: 35.

[42] Samot J, Lebreton J, Badet C. Adherence capacities of oral lactobacilli for potential probiotic purposes. Anaerobe, 2011, 17(2): 69-72.

[43] Zakaria Gomaa E. Antimicrobial and anti-adhesive properties of biosurfactant produced by lactobacilli isolates, biofilm formation and aggregation ability. J Gen Appl Microbiol, 2013, 59(6): 425-436.

[44] Lebeer S, Verhoeven TL, Perea Vélez M. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol, 2007, 73(21): 6768-6775.

[45] Muscariello L, Marino C, Capri U. CcpA and three newly identified proteins are involved in biofilm development in Lactobacillus plantarum. J Basic Microbiol, 2013, 53(1): 62-71.

[46] Kolenbrander PE, Palmer RJ Jr, Periasamy S. Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol, 2010, 8(7): 471-480.

[47] Stamatova I, Meurman JH. Probiotics and periodontal disease. Periodontol 2000, 2009, 51: 141-151.

[48] Allaker RP, Douglas CW. Novel anti-microbial therapies for dental plaque-related diseases. Int J Antimicrob Agents, 2009, 33(1): 8-13.

[49] Näse L, Hatakka K, Savilahti E. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res, 2001, 35(6): 412-420.

[50] Karuppaiah RM, Shankar S, Raj SK. Evaluation of the efficacy of probiotics in plaque reduction and gingival health maintenance among school children—a randomized control trial. J Int Oral Health, 2013, 5(5): 33-37.

[51] Campus G, Cocco F, Carta G. Effect of a daily dose of Lactobacillus brevis CD2 lozenges in high caries risk schoolchildren. Clin Oral Investig, 2014, 18(2): 555-561.

[52] Caglar E, Sandalli N, Twetman S. Effect of yogurt with Bifidobacterium DN-173 010 on salivary mutans streptococci and lactobacilli in young adults. Acta Odontol Scand, 2005, 63(6): 317-320.

[53] Sutula J, Coulthwaite L, Thomas L et al. The effect of a commercial probiotic drink on oral microbiota in healthy complete denture wearers. Microb Ecol Health Dis 2012; 23: 10.3402/mehd.v23i0.18404.

[54] Madhwani T, McBain AJ. Bacteriological effects of a Lactobacillus reuteri probiotic on in vitro oral biofilms. Arch Oral Biol, 2011, 56(11): 1264-1273.

[55] Teanpaisan R, Piwat S, Dahlén G. Inhibitory effect of oral Lactobacillus against oral pathogens. Lett Appl Microbiol, 2011, 53(4): 452-459.

[56] Twetman L, Larsen U, Fiehn NE. Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. Acta Odontol Scand, 2009, 67(5): 284-288.

[57] Lang C, Böttner M, Holz C. Specific Lactobacillus/Mutans Streptococcus co-aggregation. J Dent Res, 2010, 89(2): 175-179.

[58] Comelli EM, Guggenheim B, Stingele F. Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci, 2002, 110(3): 218-224.

[59] Chung J, Ha ES, Park HR. Isolation and characterization of Lactobacillus species inhibiting the formation of Streptococcus mutans biofilm. Oral Microbiol Immunol, 2004, 19(3): 214-216.

[60] Tahmourespour A, Salehi R, Kermanshahi RK. The anti-biofouling effect of Lactobacillus fermentum-derived biosurfactant against Streptococcus mutans. Biofouling, 2011, 27(4): 385-392.

[61] Söderling EM, Marttinen AM, Haukioja AL. Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol, 2011, 62(2): 618-622.

[62] Keller MK, Hasslöf P, Stecksén-Blicks C. Co-aggregation and growth inhibition of probiotic lactobacilli and clinical isolates of mutans streptococci: an in vitro study. Acta Odontol Scand, 2011, 69(5): 263-268.

[63] Tahmourespour A, Kermanshahi RK. The effect of a probiotic strain (Lactobacillus acidophilus) on the plaque formation of oral streptococci. Bosn J Basic Med Sci, 2011, 11(1): 37-40.

[64] Marttinen AM, Haukioja AL, Keskin M. Effects of Lactobacillus reuteri PTA 5289 and L. paracasei DSMZ16671 on the adhesion and biofilm formation of Streptococcus mutans. Curr Microbiol, 2013, 67(2): 193-199.

[65] Pham LC, van Spanning RJ, Röling WF. Effects of probiotic Lactobacillus salivarius W24 on the compositional stability of oral microbial communities. Arch Oral Biol, 2009, 54(2): 132-137.

[66] Schwendicke F, Dörfer C, Kneist S. Cariogenic effects of probiotic Lactobacillus rhamnosus GG in a dental biofilm model. Caries Res, 2014, 48(3): 186-192.

[67] Kõll-Klais P, Mändar R, Leibur E. Oral lactobacilli in chronic periodontitis and periodontal health: species composition and antimicrobial activity. Oral Microbiol Immunol, 2005, 20(6): 354-361.

[68] Krasse P, Carlsson B, Dahl C. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J, 2006, 30(2): 55-60.

[69] Shimauchi H, Mayanagi G, Nakaya S. Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: a randomized, double-blind, placebo-controlled study. J Clin Periodontol, 2008, 35(10): 897-905.

[70] Vivekananda M.R., Vandana K.L., Bhat K.G.. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. Journal of Oral Microbiology, 2010, 2(1): 5344.

[71] Zhu Y, Xiao L, Shen D. Competition between yogurt probiotics and periodontal pathogens in vitro. Acta Odontol Scand, 2010, 68(5): 261-268.

[72] Shah MP, Gujjari SK, Chandrasekhar VS. Evaluation of the effect of probiotic (inersan®) alone, combination of probiotic with doxycycline and doxycycline alone on aggressive periodontitis—a clinical and microbiological study. J Clin Diagn Res, 2013, 7(3): 595-600.

[73] Yanine N, Araya I, Brignardello-Petersen R. Effects of probiotics in periodontal diseases: a systematic review. Clin Oral Investig, 2013, 17(7): 1627-1634.

[74] Vuotto C, Barbanti F, Mastrantonio P, Donelli G. Lactobacillus brevisCD2 inhibitsPrevotella melaninogenicabiofilm. Oral Diseases, 2013, 20(7): 668-674.

[75] Hallström H, Lindgren S, Yucel-Lindberg T. Effect of probiotic lozenges on inflammatory reactions and oral biofilm during experimental gingivitis. Acta Odontol Scand, 2013, 71(3/4): 828-833.

[76] Azevedo MS, van de Sande FH, Romano AR. Microcosm biofilms originating from children with different caries experience have similar cariogenicity under successive sucrose challenges. Caries Res, 2011, 45(6): 510-517.

[77] O'Toole PW, Cooney JC. Probiotic bacteria influence the composition and function of the intestinal microbiota. Interdiscip Perspect Infect Dis, 2008, 2008: 175285.

[78] Floch MH, Walker WA, Guandalini S. Recommendations for probiotic use–2008. J Clin Gastroenterol, 2008, 42(Suppl 2): S104-S108.

[79] Gionchetti P, Rizzello F, Helwig U. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology, 2003, 124(5): 1202-1209.

[80] Mimura T, Rizzello F, Helwig U. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut, 2004, 53(1): 108-114.

[81] Collado MC, Jalonen L, Meriluoto J. Protection mechanism of probiotic combination against human pathogens: in vitro adhesion to human intestinal mucus. Asia Pac J Clin Nutr, 2006, 15(4): 570-575.

[82] Candela M, Perna F, Carnevali P. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol, 2008, 125(3): 286-292.

[83] Kim Y, Oh S, Kim SH. Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun, 2009, 379(2): 324-329.

[84] Hancock V, Dahl M, Klemm P. Probiotic Escherichia coli strain Nissle 1917 outcompetes intestinal pathogens during biofilm formation. J Med Microbiol, 2010, 59(Pt 4): 392-399.

[85] Ruas-Madiedo P, Gueimonde M, Margolles A. Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J Food Prot, 2006, 69(8): 2011-2015.

[86] Miyazaki Y, Kamiya S, Hanawa T. Effect of probiotic bacterial strains of Lactobacillus, Bifidobacterium, and Enterococcus on enteroaggregative Escherichia coli. J Infect Chemother, 2010, 16(1): 10-18.

[87] Reid Gregor, Habash Marc. Urogenital microflora and urinary tract infections. Medical Importance of the Normal Microflora, 1999 Boston, MA Springer US 423-440.

[88] Grin PM, Kowalewska PM, Alhazzan W. Lactobacillus for preventing recurrent urinary tract infections in women: meta-analysis. Can J Urol, 2013, 20(1): 6607-6614.

[89] Kumar S, Bansal A, Chakrabarti A. Evaluation of efficacy of probiotics in prevention of candida colonization in a PICU-a randomized controlled trial. Crit Care Med, 2013, 41(2): 565-572.

[90] Stapleton AE, Au-Yeung M, Hooton TM. Randomized, placebo-controlled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin Infect Dis, 2011, 52(10): 1212-1217.

[91] MacPhee RA, Hummelen R, Bisanz JE. Probiotic strategies for the treatment and prevention of bacterial vaginosis. Expert Opin Pharmacother, 2010, 11(18): 2985-2995.

[92] Abad CL, Safdar N. The role of lactobacillus probiotics in the treatment or prevention of urogenital infections—a systematic review. J Chemother, 2009, 21(3): 243-252.

[93] Klebanoff SJ, Hillier SL, Eschenbach DA. Control of the microbial flora of the vagina by H₂O₂-generating lactobacilli. J Infect Dis, 1991, 164(1): 94-100.

[94] Falagas M, Betsi GI, Athanasiou S. Probiotics for the treatment of women with bacterial vaginosis. Clin Microbiol Infect, 2007, 13(7): 657-664.

[95] Cribby S, Taylor M, Reid G. Vaginal microbiota and the use of probiotics. Interdiscip Perspect Infect Dis, 2008, 2008: 256490.

[96] Homayouni A, Bastani P, Ziyadi S. Effects of probiotics on the recurrence of bacterial vaginosis: a review. J Low Genit Tract Dis, 2014, 18(1): 79-86.

[97] Ratna Sudha M, Yelikar KA, Deshpande S. Clinical study of Bacillus coagulans Unique IS-2 (ATCC PTA-11748) in the treatment of patients with bacterial vaginosis. Indian J Microbiol, 2012, 52(3): 396-399.

[98] Sudha MR, Maurya AK. Effect of oral supplementation of the probiotic capsule UB-01BV in the treatment of patients with bacterial vaginosis. Benef Microbes, 2012, 3(2): 151-155.

[99] Hantoushzadeh S, Golshahi F, Javadian P. Comparative efficacy of probiotic yoghurt and clindamycin in treatment of bacterial vaginosis in pregnant women: a randomized clinical trial. J Matern Fetal Neonatal Med, 2012, 25(7): 1021-1024.

[100] Hummelen R, Changalucha J, Butamanya NL. Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 to prevent or cure bacterial vaginosis among women with HIV. Int J Gynaecol Obstet, 2010, 111(3): 245-248.

[101] Hemmerling A, Harrison W, Schroeder A. Phase 2a study assessing colonization efficiency, safety, and acceptability of Lactobacillus crispatus CTV-05 in women with bacterial vaginosis. Sex Transm Dis, 2010, 37(12): 745-750.

[102] Schellenberg JJ, Dumonceaux TJ, Hill JE. Selection, phenotyping and identification of acid and hydrogen peroxide producing bacteria from vaginal samples of Canadian and East African women. PLoS One, 2012, 7(7): e41217.

[103] Parent D, Bossens M, Bayot D. Therapy of bacterial vaginosis using exogenously-applied Lactobacilli acidophili and a low dose of estriol: a placebo-controlled multicentric clinical trial. Arzneimittelforschung, 1996, 46(1): 68-73.

[104] Anukam KC, Osazuwa E, Osemene GI. Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect, 2006, 8(12/13): 2772-2776.

[105] Mastromarino P, Macchia S, Meggiorini L. Effectiveness of Lactobacillus-containing vaginal tablets in the treatment of symptomatic bacterial vaginosis. Clin Microbiol Infect, 2009, 15(1): 67-74.

[106] Anukam K, Osazuwa E, Ahonkhai I. Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus gR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial. Microbes Infect, 2006, 8(6): 1450-1454.

[107] Petricevic L, Witt A. The role of Lactobacillus casei rhamnosus Lcr35 in restoring the normal vaginal flora after antibiotic treatment of bacterial vaginosis. BJOG, 2008, 115(11): 1369-1374.

[108] Larsson PG, Stray-Pedersen B, Ryttig KR. Human lactobacilli as supplementation of clindamycin to patients with bacterial vaginosis reduce the recurrence rate; a 6-month, double-blind, randomized, placebo-controlled study. BMC Womens Health, 2008, 8: 3.

[109] Hillier SL, Krohn MA, Rabe LK. The normal vaginal flora, H₂O₂-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis, 1993, 16(Suppl 4): S273-S281.

[110] Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med, 2005, 353(18): 1899-1911.

[111] Reid G, McGroarty JA, Gil Domingue PA. Coaggregation of urogenital bacteria in vitro and in vivo. Curr Microbiol, 1990, 20: 47-52.

[112] Kaewnopparat S, Dangmanee N, Kaewnopparat N. In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe, 2013, 22: 6-13.

[113] Mastromarino P, Brigidi P, Macchia S. Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets. J Appl Microbiol, 2002, 93(5): 884-893.

[114] Muli F, Struthers JK. Use of a continuous-culture biofilm system to study the antimicrobial susceptibilities of Gardnerella vaginalis and Lactobacillus acidophilus. Antimicrob Agents Chemother, 1998, 42(6): 1428-1432.

[115] Swidsinski A, Mendling W, Loening-Baucke V. Adherent biofilms in bacterial vaginosis. Obstet Gynecol, 2005, 106(5 Pt 1): 1013-1023.

[116] Patterson JL, Girerd PH, Karjane NW. Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Am J Obstet Gynecol, 2007, 197(2): 170.e1-170.e7.

[117] Senok AC, Verstraelen H, Temmerman M et al. Probiotics for the treatment of bacterial vaginosis. Cochrane Database Syst Rev 2009; ( 4): CD006289.

[118] Verstraelen H, Swidsinski A. The biofilm in bacterial vaginosis: implications for epidemiology, diagnosis and treatment. Curr Opin Infect Dis, 2013, 26(1): 86-89.

[119] Saunders S, Bocking A, Challis J. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Colloids Surf B Biointerfaces, 2007, 55(2): 138-142.

[120] McMillan A, Dell M, Zellar MP. Disruption of urogenital biofilms by lactobacilli. Colloids Surf B Biointerfaces, 2011, 86(1): 58-64.

[121] Chapman CM, Gibson GR, Rowland I. Effects of single- and multi-strain probiotics on biofilm formation and in vitro adhesion to bladder cells by urinary tract pathogens. Anaerobe, 2014, 27: 71-76.

[122] Borges S, Barbosa J, Silva J. Evaluation of characteristics of Pediococcus spp. to be used as a vaginal probiotic. J Appl Microbiol, 2013, 115(2): 527-538.

[123] Wong VW, Martindale RG, Longaker MT. From germ theory to germ therapy: skin microbiota, chronic wounds, and probiotics. Plast Reconstr Surg, 2013, 132(5): 854e-886e.

[124] Valdéz JC, Peral MC, Rachid M. Interference of Lactobacillus plantarum with Pseudomonas aeruginosa in vitro and in infected burns: the potential use of probiotics in wound treatment. Clin Microbiol Infect, 2005, 11(6): 472-479.

[125] Walencka E, Rózalska S, Sadowska B. The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol Praha, 2008, 53(1): 61-66.

[126] Sadowska B, Walencka E, Wieckowska-Szakiel M. Bacteria competing with the adhesion and biofilm formation by Staphylococcus aureus. Folia Microbiol Praha, 2010, 55(5): 497-501.

[127] Varma P, Nisha N, Dinesh KR. Anti-infective properties of Lactobacillus fermentum against Staphylococcus aureus and Pseudomonas aeruginosa. J Mol Microbiol Biotechnol, 2011, 20(3): 137-143.

[128] Sikorska H, Smoragiewicz W. Role of probiotics in the prevention and treatment of meticillin-resistant Staphylococcus aureus infections. Int J Antimicrob Agents, 2013, 42(6): 475-481.