Abstract

We investigate the mode of action and classification of antibiotic agents (ceftazidime, patulin, and epigallocatechin gallate; EGCG) on Pseudomonas aeruginosa (P. aeruginosa) biofilm using Raman spectroscopy with multivariate analysis, including support vector machine (SVM) and principal component analysis (PCA). This method allows for quantitative, label-free, non-invasive and rapid monitoring of biochemical changes in complex biofilm matrices with high sensitivity and specificity. In this study, the biofilms were grown and treated with various agents in the microfluidic device, and then transferred onto gold-coated substrates for Raman measurement. Here, we show changes in biochemical properties, and this technology can be used to distinguish between changes induced in P. aeruginosa biofilms using three antibiotic agents. The Raman band intensities associated with DNA and proteins were decreased, compared to control biofilms, when the biofilms were treated with antibiotics. Unlike with exposure to ceftazidime and patulin, the Raman spectrum of biofilms exposed to EGCG showed a shift in the spectral position of the CH deformation stretch band from 1313 cm−1 to 1333 cm−1, and there was no difference in the band intensity at 1530 cm−1 (C = C stretching, carotenoids). The PCA-SVM analysis results show that antibiotic-treated biofilms can be detected with high sensitivity of 93.33%, a specificity of 100% and an accuracy of 98.33%. This method also discriminated the three antibiotic agents based on the cellular biochemical and structural changes induced by antibiotics with high sensitivity and specificity of 100%. This study suggests that Raman spectroscopy with PCA-SVM is potentially useful for the rapid identification and classification of clinically-relevant antibiotics of bacteria biofilm. Furthermore, this method could be a powerful approach for the development and screening of new antibiotics.

© 2014 Optical Society of America

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    [Crossref] [PubMed]

2014 (4)

R. Wakamatsu, S. Takenaka, T. Ohsumi, Y. Terao, H. Ohshima, and T. Okiji, “Penetration kinetics of four mouthrinses into Streptococcus mutans biofilms analyzed by direct time-lapse visualization,” Clin. Oral Investig. 18(2), 625–634 (2014).
[Crossref] [PubMed]

N. Mangwani, S. K. Shukla, T. S. Rao, and S. Das, “Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation,” Colloids Surf. B Biointerfaces 114, 301–309 (2014).
[Crossref] [PubMed]

B. Virdis, D. Millo, B. C. Donose, and D. J. Batstone, “Real-time measurements of the redox states of c-type cytochromes in electroactive biofilms: a confocal resonance Raman Microscopy study,” PLoS ONE 9(2), e89918 (2014).
[Crossref] [PubMed]

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

2013 (3)

Y. T. Zheng, M. Toyofuku, N. Nomura, and S. Shigeto, “Correlation of Carotenoid Accumulation with Aggregation and Biofilm Development in Rhodococcus sp. SD-74,” Anal. Chem. 85(15), 7295–7301 (2013).
[Crossref] [PubMed]

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
[Crossref] [PubMed]

G. B. Jung, Y. J. Lee, G. H. Lee, and H. K. Park, “A simple and rapid detection of tissue adhesive-induced biochemical changes in cells and DNA using Raman spectroscopy,” Biomed. Opt. Express 4(11), 2673–2682 (2013).
[Crossref] [PubMed]

2012 (7)

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
[Crossref] [PubMed]

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

X. Lu, D. R. Samuelson, B. A. Rasco, and M. E. Konkel, “Antimicrobial effect of diallyl sulphide on Campylobacter jejuni biofilms,” J. Antimicrob. Chemother. 67(8), 1915–1926 (2012).
[Crossref] [PubMed]

D. McDougald, S. A. Rice, N. Barraud, P. D. Steinberg, and S. Kjelleberg, “Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal,” Nat. Rev. Microbiol. 10(1), 39–50 (2012).
[PubMed]

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Y. Chao and T. Zhang, “Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm,” Anal. Bioanal. Chem. 404(5), 1465–1475 (2012).
[Crossref] [PubMed]

2011 (4)

S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
[Crossref] [PubMed]

Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

M. Mecozzi, M. Pietroletti, and A. Tornambè, “Molecular and structural characteristics in toxic algae cultures of Ostreopsis ovata and Ostreopsis spp. evidenced by FTIR and FTNIR spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 78(5), 1572–1580 (2011).
[Crossref] [PubMed]

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

2010 (4)

N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
[Crossref] [PubMed]

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

S. Choi and Z. Jiang, “Cardiac sound murmurs classification with autoregressive spectral analysis and multi-support vector machine technique,” Comput. Biol. Med. 40(1), 8–20 (2010).
[Crossref] [PubMed]

T. J. Moritz, D. S. Taylor, C. R. Polage, D. M. Krol, S. M. Lane, and J. W. Chan, “Effect of cefazolin treatment on the nonresonant Raman signatures of the metabolic state of individual Escherichia coli cells,” Anal. Chem. 82(7), 2703–2710 (2010).
[Crossref] [PubMed]

2009 (4)

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy,” Anal. Bioanal. Chem. 393(1), 197–206 (2009).
[Crossref] [PubMed]

T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, and U. Obst, “Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks,” Chemosphere 77(2), 249–257 (2009).
[Crossref] [PubMed]

S. W. Nam, S. T. Kim, K. M. Lee, S. H. Kim, S. Kou, J. Lim, H. Hwang, M. K. Joo, B. Jeong, S. H. Yoo, and S. Park, “N-methyl-D-aspartate receptor-mediated chemotaxis and Ca2+ signaling in Tetrahymena pyriformis,” Protist 160(2), 331–342 (2009).
[Crossref] [PubMed]

V. Janakiraman, D. Englert, A. Jayaraman, and H. Baskaran, “Modeling Growth and Quorum Sensing in Biofilms Grown in Microfluidic Chambers,” Ann. Biomed. Eng. 37(6), 1206–1216 (2009).
[Crossref] [PubMed]

2008 (6)

B. R. Boles and P. K. Singh, “Endogenous oxidative stress produces diversity and adaptability in biofilm communities,” Proc. Natl. Acad. Sci. U.S.A. 105(34), 12503–12508 (2008).
[Crossref] [PubMed]

J. Lim, K. M. Lee, S. H. Kim, S. W. Nam, Y. J. Oh, H. S. Yun, W. Jo, S. Oh, S. H. Kim, and S. Park, “Nanoscale Characterization of Escherichia coli Biofilm Formed under Laminar Flow Using Atomic Force Microscopy (AFM) and Scanning Electron Microscopy (SEM),” Bull. Korean Chem. Soc. 29(11), 2114–2118 (2008).
[Crossref]

J. J. Ojeda, M. E. Romero-Gonzalez, H. M. Pouran, and S. A. Banwart, “In situ monitoring of the biofilm formation of Pseudomonas putida on hematite using flow-cell ATR-FTIR spectroscopy to investigate the formation of inner-sphere bonds between the bacteria and the mineral,” Mineral. Mag. 72(1), 101–106 (2008).
[Crossref]

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

H. Chu, Y. Huang, and Y. Zhao, “Silver Nanorod Arrays as a Surface-Enhanced Raman Scattering Substrate for Foodborne Pathogenic Bacteria Detection,” Appl. Spectrosc. 62(8), 922–931 (2008).
[Crossref] [PubMed]

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “In situ surface-enhanced Raman scattering analysis of biofilm,” Anal. Chem. 80(22), 8538–8544 (2008).
[Crossref] [PubMed]

2007 (2)

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

2006 (2)

C. A. Owen, J. Selvakumaran, I. Notingher, G. Gell, L. L. Hench, and M. M. Stevens, “In vitro toxicology evaluation of pharmaceuticals using Raman micro-spectroscopy,” J. Cell. Biochem. 99(1), 178–186 (2006).

M. Y. Chen, D. J. Lee, Z. Yang, X. F. Peng, and J. Y. Lai, “Fluorecent staining for study of extracellular polymeric substances in membrane biofouling layers,” Environ. Sci. Technol. 40(21), 6642–6646 (2006).
[Crossref] [PubMed]

2005 (2)

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

H. Schulz, M. Baranska, and R. Baranski, “Potential of NIR-FT-Raman spectroscopy in natural carotenoid analysis,” Biopolymers 77(4), 212–221 (2005).
[Crossref] [PubMed]

2004 (2)

P. Bhosale, “Environmental and cultural stimulants in the production of carotenoids from microorganisms,” Appl. Microbiol. Biotechnol. 63(4), 351–361 (2004).
[Crossref] [PubMed]

Y. Yoda, Z. Q. Hu, W. H. Zhao, and T. Shimamura, “Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate,” J. Infect. Chemother. 10(1), 55–58 (2004).
[Crossref] [PubMed]

2003 (2)

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
[Crossref] [PubMed]

I. Notingher, S. Verrier, S. Haque, J. M. Polak, and L. L. Hench, “Spectroscopic study of human lung epithelial cells (A549) in culture: living cells versus dead cells,” Biopolymers 72(4), 230–240 (2003).
[Crossref] [PubMed]

2002 (1)

K. Maquelin, C. Kirschner, L. P. Choo-Smith, N. van den Braak, H. P. Endtz, D. Naumann, and G. J. Puppels, “Identification of medically relevant microorganisms by vibrational spectroscopy,” J. Microbiol. Methods 51(3), 255–271 (2002).
[Crossref] [PubMed]

2001 (2)

T. R. De Kievit, R. Gillis, S. Marx, C. Brown, and B. H. Iglewski, “Quorum-sensing genes in pseudomonas aeruginosa biofilms: their role and expression patterns,” Appl. Environ. Microbiol. 67(4), 1865–1873 (2001).
[Crossref] [PubMed]

P. S. Stewart and J. W. Costerton, “Antibiotic resistance of bacteria in biofilms,” Lancet 358(9276), 135–138 (2001).
[Crossref] [PubMed]

2000 (3)

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

K. C. Schuster, E. Urlaub, and J. R. Gapes, “Single-cell analysis of bacteria by Raman microscopy: spectral information on the chemical composition of cells and on the heterogeneity in a culture,” J. Microbiol. Methods 42(1), 29–38 (2000).
[Crossref] [PubMed]

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

1996 (1)

J. R. Govan and V. Deretic, “Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia,” Microbiol. Rev. 60(3), 539–574 (1996).
[PubMed]

Al-Ahmad, A.

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
[Crossref] [PubMed]

Alekseeva, N. V.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Alhede, M.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

Andersen, J. B.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Andreevskaya, S. G.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Azeredo, J.

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

Banwart, S. A.

J. J. Ojeda, M. E. Romero-Gonzalez, H. M. Pouran, and S. A. Banwart, “In situ monitoring of the biofilm formation of Pseudomonas putida on hematite using flow-cell ATR-FTIR spectroscopy to investigate the formation of inner-sphere bonds between the bacteria and the mineral,” Mineral. Mag. 72(1), 101–106 (2008).
[Crossref]

Baranska, M.

H. Schulz, M. Baranska, and R. Baranski, “Potential of NIR-FT-Raman spectroscopy in natural carotenoid analysis,” Biopolymers 77(4), 212–221 (2005).
[Crossref] [PubMed]

Baranski, R.

H. Schulz, M. Baranska, and R. Baranski, “Potential of NIR-FT-Raman spectroscopy in natural carotenoid analysis,” Biopolymers 77(4), 212–221 (2005).
[Crossref] [PubMed]

Barraud, N.

D. McDougald, S. A. Rice, N. Barraud, P. D. Steinberg, and S. Kjelleberg, “Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal,” Nat. Rev. Microbiol. 10(1), 39–50 (2012).
[PubMed]

Baskaran, H.

V. Janakiraman, D. Englert, A. Jayaraman, and H. Baskaran, “Modeling Growth and Quorum Sensing in Biofilms Grown in Microfluidic Chambers,” Ann. Biomed. Eng. 37(6), 1206–1216 (2009).
[Crossref] [PubMed]

Batstone, D. J.

B. Virdis, D. Millo, B. C. Donose, and D. J. Batstone, “Real-time measurements of the redox states of c-type cytochromes in electroactive biofilms: a confocal resonance Raman Microscopy study,” PLoS ONE 9(2), e89918 (2014).
[Crossref] [PubMed]

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Baumann, K.

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

Bhosale, P.

P. Bhosale, “Environmental and cultural stimulants in the production of carotenoids from microorganisms,” Appl. Microbiol. Biotechnol. 63(4), 351–361 (2004).
[Crossref] [PubMed]

Bjarnsholt, T.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Bocklitz, T.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

Boles, B. R.

B. R. Boles and P. K. Singh, “Endogenous oxidative stress produces diversity and adaptability in biofilm communities,” Proc. Natl. Acad. Sci. U.S.A. 105(34), 12503–12508 (2008).
[Crossref] [PubMed]

Brown, C.

T. R. De Kievit, R. Gillis, S. Marx, C. Brown, and B. H. Iglewski, “Quorum-sensing genes in pseudomonas aeruginosa biofilms: their role and expression patterns,” Appl. Environ. Microbiol. 67(4), 1865–1873 (2001).
[Crossref] [PubMed]

Buijtels, P. C. A. M.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

Chan, J. W.

T. J. Moritz, D. S. Taylor, C. R. Polage, D. M. Krol, S. M. Lane, and J. W. Chan, “Effect of cefazolin treatment on the nonresonant Raman signatures of the metabolic state of individual Escherichia coli cells,” Anal. Chem. 82(7), 2703–2710 (2010).
[Crossref] [PubMed]

Chao, Y.

Y. Chao and T. Zhang, “Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm,” Anal. Bioanal. Chem. 404(5), 1465–1475 (2012).
[Crossref] [PubMed]

Chen, M. Y.

M. Y. Chen, D. J. Lee, Z. Yang, X. F. Peng, and J. Y. Lai, “Fluorecent staining for study of extracellular polymeric substances in membrane biofouling layers,” Environ. Sci. Technol. 40(21), 6642–6646 (2006).
[Crossref] [PubMed]

Chen, X.

S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
[Crossref] [PubMed]

Cho, Y. H.

S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
[Crossref] [PubMed]

Choi, S.

S. Choi and Z. Jiang, “Cardiac sound murmurs classification with autoregressive spectral analysis and multi-support vector machine technique,” Comput. Biol. Med. 40(1), 8–20 (2010).
[Crossref] [PubMed]

Choo-Smith, L. P.

K. Maquelin, C. Kirschner, L. P. Choo-Smith, N. van den Braak, H. P. Endtz, D. Naumann, and G. J. Puppels, “Identification of medically relevant microorganisms by vibrational spectroscopy,” J. Microbiol. Methods 51(3), 255–271 (2002).
[Crossref] [PubMed]

Christensen, K. B.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Christensen, L. D.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

Chu, H.

Claycomb, J. L.

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
[Crossref] [PubMed]

Conway, S. P.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Costerton, J. W.

P. S. Stewart and J. W. Costerton, “Antibiotic resistance of bacteria in biofilms,” Lancet 358(9276), 135–138 (2001).
[Crossref] [PubMed]

Cui, Y.

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

Das, S.

N. Mangwani, S. K. Shukla, T. S. Rao, and S. Das, “Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation,” Colloids Surf. B Biointerfaces 114, 301–309 (2014).
[Crossref] [PubMed]

De Kievit, T. R.

T. R. De Kievit, R. Gillis, S. Marx, C. Brown, and B. H. Iglewski, “Quorum-sensing genes in pseudomonas aeruginosa biofilms: their role and expression patterns,” Appl. Environ. Microbiol. 67(4), 1865–1873 (2001).
[Crossref] [PubMed]

Deckert, V.

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

Deretic, V.

J. R. Govan and V. Deretic, “Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia,” Microbiol. Rev. 60(3), 539–574 (1996).
[PubMed]

Didenko, L. V.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Donose, B. C.

B. Virdis, D. Millo, B. C. Donose, and D. J. Batstone, “Real-time measurements of the redox states of c-type cytochromes in electroactive biofilms: a confocal resonance Raman Microscopy study,” PLoS ONE 9(2), e89918 (2014).
[Crossref] [PubMed]

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Döring, G.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Du, X. J.

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
[Crossref] [PubMed]

Eberl, L.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Endtz, H. P.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

K. Maquelin, C. Kirschner, L. P. Choo-Smith, N. van den Braak, H. P. Endtz, D. Naumann, and G. J. Puppels, “Identification of medically relevant microorganisms by vibrational spectroscopy,” J. Microbiol. Methods 51(3), 255–271 (2002).
[Crossref] [PubMed]

Englert, D.

V. Janakiraman, D. Englert, A. Jayaraman, and H. Baskaran, “Modeling Growth and Quorum Sensing in Biofilms Grown in Microfluidic Chambers,” Ann. Biomed. Eng. 37(6), 1206–1216 (2009).
[Crossref] [PubMed]

Faubel, W.

T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, and U. Obst, “Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks,” Chemosphere 77(2), 249–257 (2009).
[Crossref] [PubMed]

Friedrich, F.

T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, and U. Obst, “Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks,” Chemosphere 77(2), 249–257 (2009).
[Crossref] [PubMed]

Gapes, J. R.

K. C. Schuster, E. Urlaub, and J. R. Gapes, “Single-cell analysis of bacteria by Raman microscopy: spectral information on the chemical composition of cells and on the heterogeneity in a culture,” J. Microbiol. Methods 42(1), 29–38 (2000).
[Crossref] [PubMed]

Gell, G.

C. A. Owen, J. Selvakumaran, I. Notingher, G. Gell, L. L. Hench, and M. M. Stevens, “In vitro toxicology evaluation of pharmaceuticals using Raman micro-spectroscopy,” J. Cell. Biochem. 99(1), 178–186 (2006).

Gillis, R.

T. R. De Kievit, R. Gillis, S. Marx, C. Brown, and B. H. Iglewski, “Quorum-sensing genes in pseudomonas aeruginosa biofilms: their role and expression patterns,” Appl. Environ. Microbiol. 67(4), 1865–1873 (2001).
[Crossref] [PubMed]

Givskov, M.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Govan, J. R.

J. R. Govan and V. Deretic, “Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia,” Microbiol. Rev. 60(3), 539–574 (1996).
[PubMed]

Greenberg, E. P.

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

Grow, A. E.

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
[Crossref] [PubMed]

Haisch, C.

N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
[Crossref] [PubMed]

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy,” Anal. Bioanal. Chem. 393(1), 197–206 (2009).
[Crossref] [PubMed]

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “In situ surface-enhanced Raman scattering analysis of biofilm,” Anal. Chem. 80(22), 8538–8544 (2008).
[Crossref] [PubMed]

Hannig, C.

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
[Crossref] [PubMed]

Hannig, M.

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
[Crossref] [PubMed]

Haque, S.

I. Notingher, S. Verrier, S. Haque, J. M. Polak, and L. L. Hench, “Spectroscopic study of human lung epithelial cells (A549) in culture: living cells versus dead cells,” Biopolymers 72(4), 230–240 (2003).
[Crossref] [PubMed]

Harnisch, F.

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Heijerman, H. G.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Heissler, S.

T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, and U. Obst, “Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks,” Chemosphere 77(2), 249–257 (2009).
[Crossref] [PubMed]

Hench, L. L.

C. A. Owen, J. Selvakumaran, I. Notingher, G. Gell, L. L. Hench, and M. M. Stevens, “In vitro toxicology evaluation of pharmaceuticals using Raman micro-spectroscopy,” J. Cell. Biochem. 99(1), 178–186 (2006).

I. Notingher, S. Verrier, S. Haque, J. M. Polak, and L. L. Hench, “Spectroscopic study of human lung epithelial cells (A549) in culture: living cells versus dead cells,” Biopolymers 72(4), 230–240 (2003).
[Crossref] [PubMed]

Hentzer, M.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Hodson, M. E.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Hoiby, N.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Høiby, N.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

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S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
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S. W. Nam, S. T. Kim, K. M. Lee, S. H. Kim, S. Kou, J. Lim, H. Hwang, M. K. Joo, B. Jeong, S. H. Yoo, and S. Park, “N-methyl-D-aspartate receptor-mediated chemotaxis and Ca2+ signaling in Tetrahymena pyriformis,” Protist 160(2), 331–342 (2009).
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N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
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[Crossref] [PubMed]

J. Lim, K. M. Lee, S. H. Kim, S. W. Nam, Y. J. Oh, H. S. Yun, W. Jo, S. Oh, S. H. Kim, and S. Park, “Nanoscale Characterization of Escherichia coli Biofilm Formed under Laminar Flow Using Atomic Force Microscopy (AFM) and Scanning Electron Microscopy (SEM),” Bull. Korean Chem. Soc. 29(11), 2114–2118 (2008).
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Pak, H. K.

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

Park, H. K.

Park, S.

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
[Crossref] [PubMed]

S. W. Nam, S. T. Kim, K. M. Lee, S. H. Kim, S. Kou, J. Lim, H. Hwang, M. K. Joo, B. Jeong, S. H. Yoo, and S. Park, “N-methyl-D-aspartate receptor-mediated chemotaxis and Ca2+ signaling in Tetrahymena pyriformis,” Protist 160(2), 331–342 (2009).
[Crossref] [PubMed]

J. Lim, K. M. Lee, S. H. Kim, S. W. Nam, Y. J. Oh, H. S. Yun, W. Jo, S. Oh, S. H. Kim, and S. Park, “Nanoscale Characterization of Escherichia coli Biofilm Formed under Laminar Flow Using Atomic Force Microscopy (AFM) and Scanning Electron Microscopy (SEM),” Bull. Korean Chem. Soc. 29(11), 2114–2118 (2008).
[Crossref]

Park, W.

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

Parsek, M. R.

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

Peng, X. F.

M. Y. Chen, D. J. Lee, Z. Yang, X. F. Peng, and J. Y. Lai, “Fluorecent staining for study of extracellular polymeric substances in membrane biofouling layers,” Environ. Sci. Technol. 40(21), 6642–6646 (2006).
[Crossref] [PubMed]

Pereira, M. O.

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

Petit, P. L. C.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

Phipps, R. K.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Pietrogiacomi, D.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

Pietroletti, M.

M. Mecozzi, M. Pietroletti, and A. Tornambè, “Molecular and structural characteristics in toxic algae cultures of Ostreopsis ovata and Ostreopsis spp. evidenced by FTIR and FTNIR spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 78(5), 1572–1580 (2011).
[Crossref] [PubMed]

Polage, C. R.

T. J. Moritz, D. S. Taylor, C. R. Polage, D. M. Krol, S. M. Lane, and J. W. Chan, “Effect of cefazolin treatment on the nonresonant Raman signatures of the metabolic state of individual Escherichia coli cells,” Anal. Chem. 82(7), 2703–2710 (2010).
[Crossref] [PubMed]

Polak, J. M.

I. Notingher, S. Verrier, S. Haque, J. M. Polak, and L. L. Hench, “Spectroscopic study of human lung epithelial cells (A549) in culture: living cells versus dead cells,” Biopolymers 72(4), 230–240 (2003).
[Crossref] [PubMed]

Popp, J.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

Pouran, H. M.

J. J. Ojeda, M. E. Romero-Gonzalez, H. M. Pouran, and S. A. Banwart, “In situ monitoring of the biofilm formation of Pseudomonas putida on hematite using flow-cell ATR-FTIR spectroscopy to investigate the formation of inner-sphere bonds between the bacteria and the mineral,” Mineral. Mag. 72(1), 101–106 (2008).
[Crossref]

Puppels, G. J.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

K. Maquelin, C. Kirschner, L. P. Choo-Smith, N. van den Braak, H. P. Endtz, D. Naumann, and G. J. Puppels, “Identification of medically relevant microorganisms by vibrational spectroscopy,” J. Microbiol. Methods 51(3), 255–271 (2002).
[Crossref] [PubMed]

Qvortrup, K.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

Rabaey, K.

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Rao, T. S.

N. Mangwani, S. K. Shukla, T. S. Rao, and S. Das, “Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation,” Colloids Surf. B Biointerfaces 114, 301–309 (2014).
[Crossref] [PubMed]

Rasco, B. A.

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
[Crossref] [PubMed]

X. Lu, D. R. Samuelson, B. A. Rasco, and M. E. Konkel, “Antimicrobial effect of diallyl sulphide on Campylobacter jejuni biofilms,” J. Antimicrob. Chemother. 67(8), 1915–1926 (2012).
[Crossref] [PubMed]

Rasmussen, T. B.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Reinicke, M.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

Rice, S. A.

D. McDougald, S. A. Rice, N. Barraud, P. D. Steinberg, and S. Kjelleberg, “Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal,” Nat. Rev. Microbiol. 10(1), 39–50 (2012).
[PubMed]

Rizzo, L.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

Romanov, Y. M.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Romero-Gonzalez, M. E.

J. J. Ojeda, M. E. Romero-Gonzalez, H. M. Pouran, and S. A. Banwart, “In situ monitoring of the biofilm formation of Pseudomonas putida on hematite using flow-cell ATR-FTIR spectroscopy to investigate the formation of inner-sphere bonds between the bacteria and the mineral,” Mineral. Mag. 72(1), 101–106 (2008).
[Crossref]

Rösch, P.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

Sacco, O.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

Samuelson, D. R.

X. Lu, D. R. Samuelson, B. A. Rasco, and M. E. Konkel, “Antimicrobial effect of diallyl sulphide on Campylobacter jejuni biofilms,” J. Antimicrob. Chemother. 67(8), 1915–1926 (2012).
[Crossref] [PubMed]

Sannino, D.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

Scarpa, A.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

Schaefer, A. L.

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

Schmid, U.

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

Schmitt, M.

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
[Crossref] [PubMed]

Schulz, H.

H. Schulz, M. Baranska, and R. Baranski, “Potential of NIR-FT-Raman spectroscopy in natural carotenoid analysis,” Biopolymers 77(4), 212–221 (2005).
[Crossref] [PubMed]

Schumacher, W.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

Schuster, K. C.

K. C. Schuster, E. Urlaub, and J. R. Gapes, “Single-cell analysis of bacteria by Raman microscopy: spectral information on the chemical composition of cells and on the heterogeneity in a culture,” J. Microbiol. Methods 42(1), 29–38 (2000).
[Crossref] [PubMed]

Schwartz, T.

T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, and U. Obst, “Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks,” Chemosphere 77(2), 249–257 (2009).
[Crossref] [PubMed]

Selvakumaran, J.

C. A. Owen, J. Selvakumaran, I. Notingher, G. Gell, L. L. Hench, and M. M. Stevens, “In vitro toxicology evaluation of pharmaceuticals using Raman micro-spectroscopy,” J. Cell. Biochem. 99(1), 178–186 (2006).

Shigeto, S.

Y. T. Zheng, M. Toyofuku, N. Nomura, and S. Shigeto, “Correlation of Carotenoid Accumulation with Aggregation and Biofilm Development in Rhodococcus sp. SD-74,” Anal. Chem. 85(15), 7295–7301 (2013).
[Crossref] [PubMed]

Shimamura, T.

Y. Yoda, Z. Q. Hu, W. H. Zhao, and T. Shimamura, “Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate,” J. Infect. Chemother. 10(1), 55–58 (2004).
[Crossref] [PubMed]

Shukla, S. K.

N. Mangwani, S. K. Shukla, T. S. Rao, and S. Das, “Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation,” Colloids Surf. B Biointerfaces 114, 301–309 (2014).
[Crossref] [PubMed]

Sillankorva, S.

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

Simões, M.

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

Singh, P. K.

B. R. Boles and P. K. Singh, “Endogenous oxidative stress produces diversity and adaptability in biofilm communities,” Proc. Natl. Acad. Sci. U.S.A. 105(34), 12503–12508 (2008).
[Crossref] [PubMed]

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

Skindersoe, M. E.

T. B. Rasmussen, M. E. Skindersoe, T. Bjarnsholt, R. K. Phipps, K. B. Christensen, P. O. Jensen, J. B. Andersen, B. Koch, T. O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov, “Identity and effects of quorum-sensing inhibitors produced by Penicillium species,” Microbiology 151(5), 1325–1340 (2005).
[Crossref] [PubMed]

Smirnov, T. A.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Smyth, A.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Steinberg, P. D.

D. McDougald, S. A. Rice, N. Barraud, P. D. Steinberg, and S. Kjelleberg, “Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal,” Nat. Rev. Microbiol. 10(1), 39–50 (2012).
[PubMed]

Stepanova, T. V.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Stevens, M. M.

C. A. Owen, J. Selvakumaran, I. Notingher, G. Gell, L. L. Hench, and M. M. Stevens, “In vitro toxicology evaluation of pharmaceuticals using Raman micro-spectroscopy,” J. Cell. Biochem. 99(1), 178–186 (2006).

Stewart, P. S.

P. S. Stewart and J. W. Costerton, “Antibiotic resistance of bacteria in biofilms,” Lancet 358(9276), 135–138 (2001).
[Crossref] [PubMed]

Szkola, A.

N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
[Crossref] [PubMed]

Takenaka, S.

R. Wakamatsu, S. Takenaka, T. Ohsumi, Y. Terao, H. Ohshima, and T. Okiji, “Penetration kinetics of four mouthrinses into Streptococcus mutans biofilms analyzed by direct time-lapse visualization,” Clin. Oral Investig. 18(2), 625–634 (2014).
[Crossref] [PubMed]

Tawakoli, P. N.

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
[Crossref] [PubMed]

Taylor, D. S.

T. J. Moritz, D. S. Taylor, C. R. Polage, D. M. Krol, S. M. Lane, and J. W. Chan, “Effect of cefazolin treatment on the nonresonant Raman signatures of the metabolic state of individual Escherichia coli cells,” Anal. Chem. 82(7), 2703–2710 (2010).
[Crossref] [PubMed]

Terao, Y.

R. Wakamatsu, S. Takenaka, T. Ohsumi, Y. Terao, H. Ohshima, and T. Okiji, “Penetration kinetics of four mouthrinses into Streptococcus mutans biofilms analyzed by direct time-lapse visualization,” Clin. Oral Investig. 18(2), 625–634 (2014).
[Crossref] [PubMed]

the Consensus Committee,

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Thompson, P. A.

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
[Crossref] [PubMed]

Tiganova, I. G.

T. A. Smirnov, L. V. Didenko, I. G. Tiganova, S. G. Andreevskaya, N. V. Alekseeva, T. V. Stepanova, and Y. M. Romanov, “Study of the structures of biofilms formed by Salmonella typhimurium bacteria on abiotic surfaces by the methods of light and transmission electron microscopy,” Appl. Biochem. Microbiol. 46(7), 706–711 (2010).
[Crossref]

Tornambè, A.

M. Mecozzi, M. Pietroletti, and A. Tornambè, “Molecular and structural characteristics in toxic algae cultures of Ostreopsis ovata and Ostreopsis spp. evidenced by FTIR and FTNIR spectroscopy,” Spectrochim. Acta A Mol. Biomol. Spectrosc. 78(5), 1572–1580 (2011).
[Crossref] [PubMed]

Touw, D. J.

G. Döring, S. P. Conway, H. G. Heijerman, M. E. Hodson, N. Høiby, A. Smyth, D. J. Touw, and the Consensus Committee, “Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus,” Eur. Respir. J. 16(4), 749–767 (2000).
[Crossref] [PubMed]

Toyofuku, M.

Y. T. Zheng, M. Toyofuku, N. Nomura, and S. Shigeto, “Correlation of Carotenoid Accumulation with Aggregation and Biofilm Development in Rhodococcus sp. SD-74,” Anal. Chem. 85(15), 7295–7301 (2013).
[Crossref] [PubMed]

Urlaub, E.

K. C. Schuster, E. Urlaub, and J. R. Gapes, “Single-cell analysis of bacteria by Raman microscopy: spectral information on the chemical composition of cells and on the heterogeneity in a culture,” J. Microbiol. Methods 42(1), 29–38 (2000).
[Crossref] [PubMed]

Vaiano, V.

L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
[Crossref]

van Belkum, A.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

van den Braak, N.

K. Maquelin, C. Kirschner, L. P. Choo-Smith, N. van den Braak, H. P. Endtz, D. Naumann, and G. J. Puppels, “Identification of medically relevant microorganisms by vibrational spectroscopy,” J. Microbiol. Methods 51(3), 255–271 (2002).
[Crossref] [PubMed]

van Gennip, M.

M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
[Crossref] [PubMed]

van Soolingen, D.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

Verbrugh, H. A.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

Verrier, S.

I. Notingher, S. Verrier, S. Haque, J. M. Polak, and L. L. Hench, “Spectroscopic study of human lung epithelial cells (A549) in culture: living cells versus dead cells,” Biopolymers 72(4), 230–240 (2003).
[Crossref] [PubMed]

Vieira, M. J.

M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
[Crossref] [PubMed]

Virdis, B.

B. Virdis, D. Millo, B. C. Donose, and D. J. Batstone, “Real-time measurements of the redox states of c-type cytochromes in electroactive biofilms: a confocal resonance Raman Microscopy study,” PLoS ONE 9(2), e89918 (2014).
[Crossref] [PubMed]

B. Virdis, F. Harnisch, D. J. Batstone, K. Rabaey, and B. C. Donose, “Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy,” Energy Environ. Sci. 5(5), 7017–7024 (2012).
[Crossref]

Wagner, M.

N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
[Crossref] [PubMed]

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy,” Anal. Bioanal. Chem. 393(1), 197–206 (2009).
[Crossref] [PubMed]

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “In situ surface-enhanced Raman scattering analysis of biofilm,” Anal. Chem. 80(22), 8538–8544 (2008).
[Crossref] [PubMed]

Wakamatsu, R.

R. Wakamatsu, S. Takenaka, T. Ohsumi, Y. Terao, H. Ohshima, and T. Okiji, “Penetration kinetics of four mouthrinses into Streptococcus mutans biofilms analyzed by direct time-lapse visualization,” Clin. Oral Investig. 18(2), 625–634 (2014).
[Crossref] [PubMed]

Walter, A.

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
[Crossref] [PubMed]

Wang, F.

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
[Crossref] [PubMed]

Wang, S.

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
[Crossref] [PubMed]

Wang, Y.

Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

Welsh, M. J.

P. K. Singh, A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg, “Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms,” Nature 407(6805), 762–764 (2000).
[Crossref] [PubMed]

Willemse-Erix, H. F.

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
[Crossref] [PubMed]

Wood, L. L.

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
[Crossref] [PubMed]

Wu, Z.

Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

Yang, Z.

M. Y. Chen, D. J. Lee, Z. Yang, X. F. Peng, and J. Y. Lai, “Fluorecent staining for study of extracellular polymeric substances in membrane biofouling layers,” Environ. Sci. Technol. 40(21), 6642–6646 (2006).
[Crossref] [PubMed]

Yoda, Y.

Y. Yoda, Z. Q. Hu, W. H. Zhao, and T. Shimamura, “Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate,” J. Infect. Chemother. 10(1), 55–58 (2004).
[Crossref] [PubMed]

Yoo, S. H.

S. W. Nam, S. T. Kim, K. M. Lee, S. H. Kim, S. Kou, J. Lim, H. Hwang, M. K. Joo, B. Jeong, S. H. Yoo, and S. Park, “N-methyl-D-aspartate receptor-mediated chemotaxis and Ca2+ signaling in Tetrahymena pyriformis,” Protist 160(2), 331–342 (2009).
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Yoon, J.

S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
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Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

Yun, H. S.

J. Lim, K. M. Lee, S. H. Kim, S. W. Nam, Y. J. Oh, H. S. Yun, W. Jo, S. Oh, S. H. Kim, and S. Park, “Nanoscale Characterization of Escherichia coli Biofilm Formed under Laminar Flow Using Atomic Force Microscopy (AFM) and Scanning Electron Microscopy (SEM),” Bull. Korean Chem. Soc. 29(11), 2114–2118 (2008).
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Y. Chao and T. Zhang, “Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm,” Anal. Bioanal. Chem. 404(5), 1465–1475 (2012).
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Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

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Y. Yoda, Z. Q. Hu, W. H. Zhao, and T. Shimamura, “Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate,” J. Infect. Chemother. 10(1), 55–58 (2004).
[Crossref] [PubMed]

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Zheng, Y. T.

Y. T. Zheng, M. Toyofuku, N. Nomura, and S. Shigeto, “Correlation of Carotenoid Accumulation with Aggregation and Biofilm Development in Rhodococcus sp. SD-74,” Anal. Chem. 85(15), 7295–7301 (2013).
[Crossref] [PubMed]

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Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

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Anal. Bioanal. Chem. (3)

N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy,” Anal. Bioanal. Chem. 393(1), 197–206 (2009).
[Crossref] [PubMed]

Y. Chao and T. Zhang, “Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm,” Anal. Bioanal. Chem. 404(5), 1465–1475 (2012).
[Crossref] [PubMed]

A. Walter, M. Reinicke, T. Bocklitz, W. Schumacher, P. Rösch, E. Kothe, and J. Popp, “Raman spectroscopic detection of physiology changes in plasmid-bearing Escherichia coli with and without antibiotic treatment,” Anal. Bioanal. Chem. 400(9), 2763–2773 (2011).
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Anal. Chem. (3)

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N. P. Ivleva, M. Wagner, H. Horn, R. Niessner, and C. Haisch, “In situ surface-enhanced Raman scattering analysis of biofilm,” Anal. Chem. 80(22), 8538–8544 (2008).
[Crossref] [PubMed]

Y. T. Zheng, M. Toyofuku, N. Nomura, and S. Shigeto, “Correlation of Carotenoid Accumulation with Aggregation and Biofilm Development in Rhodococcus sp. SD-74,” Anal. Chem. 85(15), 7295–7301 (2013).
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L. Rizzo, D. Sannino, V. Vaiano, O. Sacco, A. Scarpa, and D. Pietrogiacomi, “Effect of solar simulated N-doped TiO2 photocatalysis on the inactivation and antibiotic resistance of an E. coli strain in biologically treated urban wastewater,” Appl. Catal. B 144, 369–378 (2014).
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P. Bhosale, “Environmental and cultural stimulants in the production of carotenoids from microorganisms,” Appl. Microbiol. Biotechnol. 63(4), 351–361 (2004).
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M. Simões, M. O. Pereira, S. Sillankorva, J. Azeredo, and M. J. Vieira, “The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms,” Biofouling 23(4), 249–258 (2007).
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J. Lim, K. M. Lee, S. H. Kim, S. W. Nam, Y. J. Oh, H. S. Yun, W. Jo, S. Oh, S. H. Kim, and S. Park, “Nanoscale Characterization of Escherichia coli Biofilm Formed under Laminar Flow Using Atomic Force Microscopy (AFM) and Scanning Electron Microscopy (SEM),” Bull. Korean Chem. Soc. 29(11), 2114–2118 (2008).
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ChemPhysChem (1)

U. Neugebauer, U. Schmid, K. Baumann, W. Ziebuhr, S. Kozitskaya, V. Deckert, M. Schmitt, and J. Popp, “Towards a detailed understanding of bacterial metabolism-spectroscopic characterization of staphylococcus epidermidis,” ChemPhysChem 8(1), 124–137 (2007).
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Clin. Oral Investig. (2)

P. N. Tawakoli, A. Al-Ahmad, W. Hoth-Hannig, M. Hannig, and C. Hannig, “Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm,” Clin. Oral Investig. 17(3), 841–850 (2013).
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R. Wakamatsu, S. Takenaka, T. Ohsumi, Y. Terao, H. Ohshima, and T. Okiji, “Penetration kinetics of four mouthrinses into Streptococcus mutans biofilms analyzed by direct time-lapse visualization,” Clin. Oral Investig. 18(2), 625–634 (2014).
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N. Mangwani, S. K. Shukla, T. S. Rao, and S. Das, “Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation,” Colloids Surf. B Biointerfaces 114, 301–309 (2014).
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M. Y. Chen, D. J. Lee, Z. Yang, X. F. Peng, and J. Y. Lai, “Fluorecent staining for study of extracellular polymeric substances in membrane biofouling layers,” Environ. Sci. Technol. 40(21), 6642–6646 (2006).
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Food Microbiol. (1)

Y. Cui, Y. J. Oh, J. Lim, M. Youn, I. Lee, H. K. Pak, W. Park, W. Jo, and S. Park, “AFM study of the differential inhibitory effects of the green tea polyphenol-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria,” Food Microbiol. 29(1), 80–87 (2012).
[Crossref] [PubMed]

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M. van Gennip, L. D. Christensen, M. Alhede, K. Qvortrup, P. Ø. Jensen, N. Høiby, M. Givskov, and T. Bjarnsholt, “Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo,” Infect. Immun. 80(8), 2601–2607 (2012).
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J. Clin. Microbiol. (1)

P. C. A. M. Buijtels, H. F. Willemse-Erix, P. L. C. Petit, H. P. Endtz, G. J. Puppels, H. A. Verbrugh, A. van Belkum, D. van Soolingen, and K. Maquelin, “Rapid Identification of Mycobacteria by Raman Spectroscopy,” J. Clin. Microbiol. 46(3), 961–965 (2008).
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J. Infect. Chemother. (1)

Y. Yoda, Z. Q. Hu, W. H. Zhao, and T. Shimamura, “Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate,” J. Infect. Chemother. 10(1), 55–58 (2004).
[Crossref] [PubMed]

J. Microbiol. Methods (3)

A. E. Grow, L. L. Wood, J. L. Claycomb, and P. A. Thompson, “New Biochip Technology for Label-Free Detection of Pathogens and Their Toxins,” J. Microbiol. Methods 53(2), 221–233 (2003).
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J. Phys. Chem. B (1)

N. P. Ivleva, M. Wagner, A. Szkola, H. Horn, R. Niessner, and C. Haisch, “Label-free in situ SERS imaging of biofilms,” J. Phys. Chem. B 114(31), 10184–10194 (2010).
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J. J. Ojeda, M. E. Romero-Gonzalez, H. M. Pouran, and S. A. Banwart, “In situ monitoring of the biofilm formation of Pseudomonas putida on hematite using flow-cell ATR-FTIR spectroscopy to investigate the formation of inner-sphere bonds between the bacteria and the mineral,” Mineral. Mag. 72(1), 101–106 (2008).
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S. W. Nam, X. Chen, J. Lim, S. H. Kim, S. T. Kim, Y. H. Cho, J. Yoon, and S. Park, “In vivo Fluorescence Imaging of Bacteriogenic Cyanide in the Lungs of Live Mice Infected with Cystic Fibrosis Pathogens,” PLoS ONE 6(7), e21387 (2011).
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S. W. Nam, S. T. Kim, K. M. Lee, S. H. Kim, S. Kou, J. Lim, H. Hwang, M. K. Joo, B. Jeong, S. H. Yoo, and S. Park, “N-methyl-D-aspartate receptor-mediated chemotaxis and Ca2+ signaling in Tetrahymena pyriformis,” Protist 160(2), 331–342 (2009).
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Res. Microbiol. (1)

X. J. Du, F. Wang, X. Lu, B. A. Rasco, and S. Wang, “Biochemical and genetic characteristics of Cronobacter sakazakii biofilm formation,” Res. Microbiol. 163(6-7), 448–456 (2012).
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Y. Wang, W. Zhang, Z. Wu, X. Zhu, and C. Lu, “Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence,” Vet. Microbiol. 152(1-2), 151–160 (2011).
[Crossref] [PubMed]

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Figures (7)

Fig. 1
Fig. 1

Schematic image of microfluidic device and experimental setup for biofilm formation

Fig. 2
Fig. 2

Representative fluorescent images of P. aeruginosa cells and biofilm and 3D-reconstructed image of the cells and biofilm in the microfluidic device. (A) 3D-reconstructed image of biofilms in the microfluidic device for 1-3 days. (B) Bacteria cells were stained by fluorescein isothiocyanate-labeled goat anti-rabbit antibody (Ab-FITC) and biofilm by tetramethylrhodamine isothiocyanate-labeled concanavalin A (Concanavalin A-RITC). Scale bars represent 20 μm.

Fig. 3
Fig. 3

Averaged Raman spectrum of P. aeruginosa biofilm.

Fig. 4
Fig. 4

Averaged Raman spectra of three antibiotic solutions (ceftazidime, patulin and EGCG).

Fig. 5
Fig. 5

Raman spectra of P. aeruginosa biofilms. (A) Averaged spectra for control and antibiotic-treated biofilms; (B-D) (a) Overlaid spectra of control and antibiotic-treated biofilm, (b) spectral differences of control biofilm and biofilm treated with antibiotic: (B) ceftazidime, (C) patulin, (D) EGCG.

Fig. 6
Fig. 6

Relative intensities of the Raman peaks for control biofilm and biofilm treated with three antibiotic agents. *P < 0.001 (one-way ANOVA) with post hoc comparisons (Table 2).

Fig. 7
Fig. 7

PCA-SVM scores: (a) PC1-PC2 plot of control biofilm and biofilm treated with antibiotic agents, (b) PC3-PC4 plot of control and biofilms treated with ceftazidime, patulin and EGCG. The optimal boundary lines could be used as a marker to monitor and detect the presence of antibiotic agents and to find the distinctive functions of newly-developed antibiotic agents on P. aeruginosa biofilm.

Tables (3)

Tables Icon

Table 1 Peak assignment of the Raman spectra of P. aeruginosa biofilm [19, 3942]

Tables Icon

Table 2 Effect of treatment with antibiotic agents on the variation in P. aeruginosa biofilm components. Each Raman peak indicates a significant difference between two groups after ANOVA (Student-Newman-Keuls test, P < 0.05).

Tables Icon

Table 3 Representative five Raman spectral peaks with high contribution at PC1 to PC4.

Metrics