Issue
Antimicrobial Effect of Garlic (Allium sativum) and Thyme (Zataria multiflora Boiss) Extracts on Some Food Borne Pathogens and Their Effect on Virulence Gene Expression
Corresponding Author(s) : Azza S El-Demerdash
Cellular and Molecular Biology,
Vol. 64 No. 10: Issue 10
Abstract
The incrementing scope of pathogenic resistance to antibiotics has encouraged the search for antivirulence natural extracts. Therefore, our study designed to demonstrate the antimicrobial activity of an aqueous-garlic and thyme oil extracts against Gram-positive (Staphylococcus aureus) and Gram-negative (Salmonella spp.) bacteria by evaluating the influence of sub-inhibitory concentrations on the expression of the most critical virulence genes of the tested isolates. The antibacterial potential of both herbs was checked by the agar well diffusion method and minimum inhibitory concentration (MIC) assay. Interestingly, all isolates were inhibited by both extracts up to 50% concentration. Also, the MIC values of garlic extract (0.125-1µg/ml) against Salmonella isolates were lower than the values of thyme extract (0.5- 8µg/ml). But in S. aureus isolates, the MIC values of thyme extract (0.25- 2µg/ml) were the lowermost. Conventional PCR investigated that all S. aureus isolates carried the hlg (hemolysin) and icaA (intracellular adhesion) genes, but only six Salmonella isolates (three S. typhimurium and one each of S. kentucky, S. anatum, and S. lagos) had both the sopB (Salmonella outer protein B) and mgtC (membrane protein) genes. Real-time RT-PCR assays were performed to evaluate the extract's effect on the virulence genes. The thyme-oil extract has significantly repressed S. aureus virulence genes expression more than aqueous-garlic extract, which later one has effectively more than thyme-oil extract in downregulating the Salmonella virulence genes. In conclusion, garlic and thyme extracts can be used not only as a flavor, but also as potential antimicrobial agents against Gram-positive and negative bacteria.
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- Alwan A. Global Status Report on Noncommunicable Diseases 2010. Geneva: World Health Organization; 2011.
- Forsythe SJ. Microbiologia da segurança alimentar, trad. Maria Carolina Mardi Guimarí£es e Cris Leonhardt Porto Alegre Artmed. 2002.
- Upadhyay, A., Mooyottu, S., Yin, H., Nair, M.S., Bhattaram, V. and Venkitanarayanan, K. Inhibiting microbial toxins using plant-derived compounds and plant extracts. Medicines. 2015;2(3):186-211.
- Food US, Administration D, others. FDA Task Force on Antimicrobial Resistance: Key Recommendations and Report. 2000.
- Levy SB. Antibiotics, animals and the resistance gene pool. Antibiot Parad how misuse Antibiot destroys their curative powers, 2nd ed Perseus Publ Serv Cambridge, MA. 2002:149-180.
- Farnsworth NR, Loub WD. Information gathering and databases that are pertinent to the development of plant-derived drugs. In: The Potentials for Extracting Protein, Medicines, and Other Useful Chemicals. Workshop Proceedings, OTA-BP-F-23. US Congress, Office of Technology Assessment, Washington, DC. ; 1983:178-195.
- Janovska D, Kubikova K, Kokoska L. Screening for antimicrobial activity of some medicinal plants species of traditional Chinese medicine. Czech J Food Sci. 2003;21(3):107-110.
- Grover A, Bhandari BS, Rai N. Antimicrobial activity of medicinal plants-Azadirachta indica A. Juss, Allium cepa L. and Aloe vera L. Int J Pharm Tech Res. 2011;3:1059-1065.
- Roller S. Natural Antimicrobials for the Minimal Processing of Foods. Elsevier; 2003.
- Whitemore BB, Naidu AS. Thiosulfinates. Nat food Antimicrob Syst. 2000:265-380.
- Kumar A, Sharma VD. Inhibitory effect of garlic (Allium sativum Linn.) on enterotoxigenic Escherichia coli. Indian J Med Res. 1982;76:66-70.
- Jezowa L, Rafinski T, Wrocinski T. Investigations on the antibiotic activity of Allium sativum. L Herba Pol. 1966;12:3-13.
- Witte W. Medical consequences of antibiotic use in agriculture. Science (80- ). 1998;279(5353):996-997.
- Ankri S, Mirelman D. Antimicrobial properties of allicin from garlic. Microbes Infect. 1999;1(2):125-129.
- Ghasemi S, Javadi NHS, Esmaeili S, Khosravi-Darani K. Minimum inhibitory concentration of Zataria multiflora Boiss. essential oil on Salmonella Enteritidis, Listeria monocytogenes, Escherichia coli 0157: H7 and Staphylococcus aureus. Asian J Chem. 2012;24(12):5943.
- Ushimaru PI, Silva MTN da, Stasi D, Claudio L, Barbosa L, Fernandes Junior A. Antibacterial activity of medicinal plant extracts. Brazilian J Microbiol. 2007;38(4):717-719. doi:10.1590/S1517-83822007000400024.
- Upadhyay A, Upadhyaya I, Kollanoor-Johny A, Venkitanarayanan K. Combating pathogenic microorganisms using plant-derived antimicrobials: a minireview of the mechanistic basis. Biomed Res Int. 2014;2014.
- Foley SL, Zhao S, Walker RD. Foodborne Pathogens. Foodborne Pathog Dis. 2007;4(3):253-276. doi:10.1089/fpd.2007.0085.
- Onyeagba RA, Ugbogu OC, Okeke CU, Iroakasi O. Studies on the antimicrobial effects of garlic (Allium sativum Linn), ginger (Zingiber officinale Roscoe) and lime (Citrus aurantifolia Linn). African J Biotechnol. 2004;3(10):552-554.
- Betoni JEC, Mantovani RP, Barbosa LN, Di Stasi LC, Fernandes Junior A. Synergism between plant extract and antimicrobial drugs used on Staphylococcus aureus diseases. Mem Inst Oswaldo Cruz. 2006;101(4):387-390.
- Wayne PA. National committee for clinical laboratory standards. Perform Stand Antimicrob disc susceptibility Test. 2002;12.
- Durairaj S, Srinivasan S, Lakshmanaperumalsamy P. In vitro Antibacterial Activity and Stability of Garlic Extract at Different pH and Temperature. Electr J Biol. 2009;5(1):5-10.
- CLSI (Clinical and Laboratory Standards Institute). M100-S23 Performance Standards for Antimicrobial.; 2013.
- Khosravi A, Malekan MA. Determination of Alcoholic and aqueous extract of Lavender Astvkas on Staphylococcus aureus and other Gram-negative bacteria. The J Qazvin Univ Med Sci. 2004;29:3-9.
- Ciftci A, Findik A, Onuk EE, Savasan S. Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis. Brazilian J Microbiol. 2009;40(2):254-261.
- Kumar JD, Negi YK, Gaur A, Khanna D. Detection of virulence genes in Staphylococcus aureus isolated from paper currency. Int J Infect Dis. 2009;13(6):e450--e455.
- Huehn S, La Ragione RM, Anjum M, et al. Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathog Dis. 2010;7(5):523-535.
- Yuan JS, Reed A, Chen F, Stewart CN. Statistical analysis of real-time PCR data. BMC Bioinformatics. 2006;7(1):85.
- Mason WJ, Blevins JS, Beenken K, Wibowo N, Ojha N, Smeltzer MS. Multiplex PCR protocol for the diagnosis of staphylococcal infection. J Clin Microbiol. 2001;39(9):3332-3338.
- Yang X, Brisbin J, Yu H, et al. Selected lactic acid-producing bacterial isolates with the capacity to reduce Salmonella translocation and virulence gene expression in chickens. PLoS One. 2014;9(4):e93022.
- Osman KM, Marouf SH, Zolnikov TR, AlAtfeehy N. Isolation and characterization of Salmonella enterica in day-old ducklings in Egypt. Pathog Glob Health. 2014;108(1):37-48.
- Gunasegaran T, Rathinam X, Kasi M, Sathasivam K, Sreenivasan S, Subramaniam S. Isolation and identification of Salmonella from curry samples and its sensitivity to commercial antibiotics and aqueous extracts of Camelia sinensis (L.) and Trachyspermum ammi (L.). Asian Pac J Trop Biomed. 2011;1(4):266-269.
- Khalifa SM, Abdel-Rhman HSH, Abd-El-Galil KH, Habib E, Barwa R. Occurrence and characterization of Staphylococcus aureus in meat and meat products marketed in Mansoura, Egypt. Egypt J Med Microbiol. 2014;23(3).
- Ammar, A. M.Attia, A. M., El-Aziz, N.K., Abd Hamid, M.I, Abd El, El-Demerdash AS. Class 1 integron and associated gene cassettes mediating multiple-drug resistance in some foodborne pathogens. Int Food Res J. 2016;23(1):332-339.
- Jakee JEI, Ata NS, El-Moez SIA, Kandiel MM, Radwan NM. Assessment of the prevalence of Salmonellae in food. Int J Curr Microbiol Appl Sci. 2014;3(3):30-42. http://www.ijcmas.com/vol-3-3/J.EI Jakee, et al.pdf.
- Salamci E, Kordali S, Kotan R, Cakir A, Kaya Y. Chemical compositions, antimicrobial and herbicidal effects of essential oils isolated from Turkish Tanacetum aucheranum and Tanacetum chiliophyllum var. chiliophyllum. Biochem Syst Ecol. 2007;35(9):569-581.
- Valero M, Frances E. Synergistic bactericidal effect of carvacrol, cinnamaldehyde or thymol and refrigeration to inhibit Bacillus cereus in carrot broth. Food Microbiol. 2006;23(1):68-73.
- Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem. 2003;10(10):813-829.
- Smith-Palmer A, Stewart J, Fyfe L. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol. 2001;18(4):463-470.
- Walsh SE, Maillard J-Y, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG. Activity and mechanisms of action of selected biocidal agents on Gram-positive and-negative bacteria. J Appl Microbiol. 2003;94(2):240-247.
- Cavalitto CJ, Bailey JH. The antibacterial principles of (Allium sativum L.): Isolation, physical properties and antibacterial action. J Am Chem Soc. 1994;66:195-200.
- Cutler RR, Wilson P. Antibacterial activity of a new, stable, aqueous extract of allicin against methicillin-resistant Staphylococcus aureus. Br J Biomed Sci. 2004;61(2):71-74.
- Li G, Ma X, Deng L, et al. Fresh garlic extract enhances the antimicrobial activities of antibiotics on resistant strains in vitro. Jundishapur J Microbiol. 2015;8(5):1-6. doi:10.5812/jjm.14814.
- Belguith H, Kthiri F, Ammar A Ben, Jaafoura H, Hamida J Ben, Landoulsi A. Morphological and Biochemical Changes of Salmonella Hadar Exposed to Aqueous Garlic Extract. Int J Morphol. 2009;27(3).
- Tiwari BK, Valdramidis VP, O´Donnell CP, Muthukumarappan K, Bourke P, Cullen PJ. Application of natural antimicrobials for food preservation. J Agric Food Chem. 2009;57(14):5987-6000.
- Goodarzi . H. Teimourzadeh. Med Microbiol. 2006.
- Majerczyk CD, Sadykov MR, Luong TT, Lee C, Somerville GA, Sonenshein AL. Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol. 2008;190(7):2257-2265.
- Melchior MB, Vaarkamp H, Fink-Gremmels J. Biofilms: a role in recurrent mastitis infections? Vet J. 2006;171(3):398-407.
- Günzel D, Kucharski LM, Kehres DG, Romero MF, Maguire ME. The MgtC virulence factor of Salmonella enterica serovar Typhimurium activates Na+, K+-ATPase. J Bacteriol. 2006;188(15):5586-5594.
- Bugarel M, Granier SA, Weill F-X, Fach P, Brisabois A. A multiplex real-time PCR assay targeting virulence and resistance genes in Salmonella enterica serotype Typhimurium. BMC Microbiol. 2011;11(1):151.
- Bernardo K, Pakulat N, Fleer S, et al. Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrob Agents Chemother. 2004;48(2):546-555.
- Sun H, Xu Y, Sitkiewicz I, et al. Inhibitor of streptokinase gene expression improves survival after group A streptococcus infection in mice. Proc Natl Acad Sci. 2012;109(9):3469-3474.
- Kollanoor-Johny A, Mattson T, Baskaran SA, et al. Reduction of Salmonella enterica serovar Enteritidis colonization in 20-day-old broiler chickens by the plant-derived compounds trans-cinnamaldehyde and eugenol. Appl Environ Microbiol. 2012;78(8):2981-2987.
- Wojnicz D, Kucharska AZ, Sokól-LÈ©towska A, Kicia M, Tichaczek-Goska D. Medicinal plants extracts affect virulence factors expression and biofilm formation by the uropathogenic Escherichia coli. Urol Res. 2012;40(6):683-697. doi:10.1007/s00240-012-0499-6.
- Sakuragi Y, Kolter R. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol. 2007;189(14):5383-5386.
References
Alwan A. Global Status Report on Noncommunicable Diseases 2010. Geneva: World Health Organization; 2011.
Forsythe SJ. Microbiologia da segurança alimentar, trad. Maria Carolina Mardi Guimarí£es e Cris Leonhardt Porto Alegre Artmed. 2002.
Upadhyay, A., Mooyottu, S., Yin, H., Nair, M.S., Bhattaram, V. and Venkitanarayanan, K. Inhibiting microbial toxins using plant-derived compounds and plant extracts. Medicines. 2015;2(3):186-211.
Food US, Administration D, others. FDA Task Force on Antimicrobial Resistance: Key Recommendations and Report. 2000.
Levy SB. Antibiotics, animals and the resistance gene pool. Antibiot Parad how misuse Antibiot destroys their curative powers, 2nd ed Perseus Publ Serv Cambridge, MA. 2002:149-180.
Farnsworth NR, Loub WD. Information gathering and databases that are pertinent to the development of plant-derived drugs. In: The Potentials for Extracting Protein, Medicines, and Other Useful Chemicals. Workshop Proceedings, OTA-BP-F-23. US Congress, Office of Technology Assessment, Washington, DC. ; 1983:178-195.
Janovska D, Kubikova K, Kokoska L. Screening for antimicrobial activity of some medicinal plants species of traditional Chinese medicine. Czech J Food Sci. 2003;21(3):107-110.
Grover A, Bhandari BS, Rai N. Antimicrobial activity of medicinal plants-Azadirachta indica A. Juss, Allium cepa L. and Aloe vera L. Int J Pharm Tech Res. 2011;3:1059-1065.
Roller S. Natural Antimicrobials for the Minimal Processing of Foods. Elsevier; 2003.
Whitemore BB, Naidu AS. Thiosulfinates. Nat food Antimicrob Syst. 2000:265-380.
Kumar A, Sharma VD. Inhibitory effect of garlic (Allium sativum Linn.) on enterotoxigenic Escherichia coli. Indian J Med Res. 1982;76:66-70.
Jezowa L, Rafinski T, Wrocinski T. Investigations on the antibiotic activity of Allium sativum. L Herba Pol. 1966;12:3-13.
Witte W. Medical consequences of antibiotic use in agriculture. Science (80- ). 1998;279(5353):996-997.
Ankri S, Mirelman D. Antimicrobial properties of allicin from garlic. Microbes Infect. 1999;1(2):125-129.
Ghasemi S, Javadi NHS, Esmaeili S, Khosravi-Darani K. Minimum inhibitory concentration of Zataria multiflora Boiss. essential oil on Salmonella Enteritidis, Listeria monocytogenes, Escherichia coli 0157: H7 and Staphylococcus aureus. Asian J Chem. 2012;24(12):5943.
Ushimaru PI, Silva MTN da, Stasi D, Claudio L, Barbosa L, Fernandes Junior A. Antibacterial activity of medicinal plant extracts. Brazilian J Microbiol. 2007;38(4):717-719. doi:10.1590/S1517-83822007000400024.
Upadhyay A, Upadhyaya I, Kollanoor-Johny A, Venkitanarayanan K. Combating pathogenic microorganisms using plant-derived antimicrobials: a minireview of the mechanistic basis. Biomed Res Int. 2014;2014.
Foley SL, Zhao S, Walker RD. Foodborne Pathogens. Foodborne Pathog Dis. 2007;4(3):253-276. doi:10.1089/fpd.2007.0085.
Onyeagba RA, Ugbogu OC, Okeke CU, Iroakasi O. Studies on the antimicrobial effects of garlic (Allium sativum Linn), ginger (Zingiber officinale Roscoe) and lime (Citrus aurantifolia Linn). African J Biotechnol. 2004;3(10):552-554.
Betoni JEC, Mantovani RP, Barbosa LN, Di Stasi LC, Fernandes Junior A. Synergism between plant extract and antimicrobial drugs used on Staphylococcus aureus diseases. Mem Inst Oswaldo Cruz. 2006;101(4):387-390.
Wayne PA. National committee for clinical laboratory standards. Perform Stand Antimicrob disc susceptibility Test. 2002;12.
Durairaj S, Srinivasan S, Lakshmanaperumalsamy P. In vitro Antibacterial Activity and Stability of Garlic Extract at Different pH and Temperature. Electr J Biol. 2009;5(1):5-10.
CLSI (Clinical and Laboratory Standards Institute). M100-S23 Performance Standards for Antimicrobial.; 2013.
Khosravi A, Malekan MA. Determination of Alcoholic and aqueous extract of Lavender Astvkas on Staphylococcus aureus and other Gram-negative bacteria. The J Qazvin Univ Med Sci. 2004;29:3-9.
Ciftci A, Findik A, Onuk EE, Savasan S. Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis. Brazilian J Microbiol. 2009;40(2):254-261.
Kumar JD, Negi YK, Gaur A, Khanna D. Detection of virulence genes in Staphylococcus aureus isolated from paper currency. Int J Infect Dis. 2009;13(6):e450--e455.
Huehn S, La Ragione RM, Anjum M, et al. Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathog Dis. 2010;7(5):523-535.
Yuan JS, Reed A, Chen F, Stewart CN. Statistical analysis of real-time PCR data. BMC Bioinformatics. 2006;7(1):85.
Mason WJ, Blevins JS, Beenken K, Wibowo N, Ojha N, Smeltzer MS. Multiplex PCR protocol for the diagnosis of staphylococcal infection. J Clin Microbiol. 2001;39(9):3332-3338.
Yang X, Brisbin J, Yu H, et al. Selected lactic acid-producing bacterial isolates with the capacity to reduce Salmonella translocation and virulence gene expression in chickens. PLoS One. 2014;9(4):e93022.
Osman KM, Marouf SH, Zolnikov TR, AlAtfeehy N. Isolation and characterization of Salmonella enterica in day-old ducklings in Egypt. Pathog Glob Health. 2014;108(1):37-48.
Gunasegaran T, Rathinam X, Kasi M, Sathasivam K, Sreenivasan S, Subramaniam S. Isolation and identification of Salmonella from curry samples and its sensitivity to commercial antibiotics and aqueous extracts of Camelia sinensis (L.) and Trachyspermum ammi (L.). Asian Pac J Trop Biomed. 2011;1(4):266-269.
Khalifa SM, Abdel-Rhman HSH, Abd-El-Galil KH, Habib E, Barwa R. Occurrence and characterization of Staphylococcus aureus in meat and meat products marketed in Mansoura, Egypt. Egypt J Med Microbiol. 2014;23(3).
Ammar, A. M.Attia, A. M., El-Aziz, N.K., Abd Hamid, M.I, Abd El, El-Demerdash AS. Class 1 integron and associated gene cassettes mediating multiple-drug resistance in some foodborne pathogens. Int Food Res J. 2016;23(1):332-339.
Jakee JEI, Ata NS, El-Moez SIA, Kandiel MM, Radwan NM. Assessment of the prevalence of Salmonellae in food. Int J Curr Microbiol Appl Sci. 2014;3(3):30-42. http://www.ijcmas.com/vol-3-3/J.EI Jakee, et al.pdf.
Salamci E, Kordali S, Kotan R, Cakir A, Kaya Y. Chemical compositions, antimicrobial and herbicidal effects of essential oils isolated from Turkish Tanacetum aucheranum and Tanacetum chiliophyllum var. chiliophyllum. Biochem Syst Ecol. 2007;35(9):569-581.
Valero M, Frances E. Synergistic bactericidal effect of carvacrol, cinnamaldehyde or thymol and refrigeration to inhibit Bacillus cereus in carrot broth. Food Microbiol. 2006;23(1):68-73.
Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem. 2003;10(10):813-829.
Smith-Palmer A, Stewart J, Fyfe L. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol. 2001;18(4):463-470.
Walsh SE, Maillard J-Y, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG. Activity and mechanisms of action of selected biocidal agents on Gram-positive and-negative bacteria. J Appl Microbiol. 2003;94(2):240-247.
Cavalitto CJ, Bailey JH. The antibacterial principles of (Allium sativum L.): Isolation, physical properties and antibacterial action. J Am Chem Soc. 1994;66:195-200.
Cutler RR, Wilson P. Antibacterial activity of a new, stable, aqueous extract of allicin against methicillin-resistant Staphylococcus aureus. Br J Biomed Sci. 2004;61(2):71-74.
Li G, Ma X, Deng L, et al. Fresh garlic extract enhances the antimicrobial activities of antibiotics on resistant strains in vitro. Jundishapur J Microbiol. 2015;8(5):1-6. doi:10.5812/jjm.14814.
Belguith H, Kthiri F, Ammar A Ben, Jaafoura H, Hamida J Ben, Landoulsi A. Morphological and Biochemical Changes of Salmonella Hadar Exposed to Aqueous Garlic Extract. Int J Morphol. 2009;27(3).
Tiwari BK, Valdramidis VP, O´Donnell CP, Muthukumarappan K, Bourke P, Cullen PJ. Application of natural antimicrobials for food preservation. J Agric Food Chem. 2009;57(14):5987-6000.
Goodarzi . H. Teimourzadeh. Med Microbiol. 2006.
Majerczyk CD, Sadykov MR, Luong TT, Lee C, Somerville GA, Sonenshein AL. Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol. 2008;190(7):2257-2265.
Melchior MB, Vaarkamp H, Fink-Gremmels J. Biofilms: a role in recurrent mastitis infections? Vet J. 2006;171(3):398-407.
Günzel D, Kucharski LM, Kehres DG, Romero MF, Maguire ME. The MgtC virulence factor of Salmonella enterica serovar Typhimurium activates Na+, K+-ATPase. J Bacteriol. 2006;188(15):5586-5594.
Bugarel M, Granier SA, Weill F-X, Fach P, Brisabois A. A multiplex real-time PCR assay targeting virulence and resistance genes in Salmonella enterica serotype Typhimurium. BMC Microbiol. 2011;11(1):151.
Bernardo K, Pakulat N, Fleer S, et al. Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrob Agents Chemother. 2004;48(2):546-555.
Sun H, Xu Y, Sitkiewicz I, et al. Inhibitor of streptokinase gene expression improves survival after group A streptococcus infection in mice. Proc Natl Acad Sci. 2012;109(9):3469-3474.
Kollanoor-Johny A, Mattson T, Baskaran SA, et al. Reduction of Salmonella enterica serovar Enteritidis colonization in 20-day-old broiler chickens by the plant-derived compounds trans-cinnamaldehyde and eugenol. Appl Environ Microbiol. 2012;78(8):2981-2987.
Wojnicz D, Kucharska AZ, Sokól-LÈ©towska A, Kicia M, Tichaczek-Goska D. Medicinal plants extracts affect virulence factors expression and biofilm formation by the uropathogenic Escherichia coli. Urol Res. 2012;40(6):683-697. doi:10.1007/s00240-012-0499-6.
Sakuragi Y, Kolter R. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol. 2007;189(14):5383-5386.