1887

Chapter 13 : Antimicrobial Tolerance in Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Antimicrobial Tolerance in Biofilms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap13-1.gif /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap13-2.gif

Abstract:

Tolerance to antimicrobial agents is a common feature of microbial biofilm formation ( ). Table 1 presents a few examples of biofilm tolerance to biocides and antiseptics, and Table 2 summarizes some examples of antibiotic tolerance in biofilms. Neither of these listings is comprehensive, but these two data sets can be analyzed to gain insight into the factors that influence biofilm tolerance. The examples have been selected to illustrate the wide variety of microbial species, growth environments, and antimicrobial chemistries for which biofilm reduced susceptibility has been reported. The short list in Table 1 encompasses studies designed to mimic biofilms in dental plaque, hot tubs, paper mills, drinking water, household drains, urinary catheters, food processing plants, cooling water systems, and hospitals. These examples employ a range of individual and mixed species biofilms and diverse biocidal chemistries including halogens, phenolics, quaternary ammonium compounds, aldehydes, a plant essential oil, and peroxides. The studies captured in Table 2 cover 19 antibiotics and 9 organisms that include aerobic bacteria, strict anaerobes, and a fungus.

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Tolerance factors versus antimicrobial agent molecular weight for the data on (A) biocides and antiseptics from Table 1 and (B) antibiotics from Table 2 . doi:10.1128/microbiolspec.MB-0010-2014.f1

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Tolerance factors grouped and compared by substratum material. doi:10.1128/microbiolspec.MB-0010-2014.f2

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Tolerance factor versus biofilm cell density for the data in Table 1 . The line is the least squares regressed fit. doi:10.1128/microbiolspec.MB-0010-2014.f3

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Efficacy of chlorine treatment against biofilms as a function of the untreated control biofilm areal cell density. The y-axis is the reported log reduction divided by the product of dose concentration and duration ( ). The line is the least squares regressed fit. Sources: references . doi:10.1128/microbiolspec.MB-0010-2014.f4

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Antibiotic efficacy against biofilms as a function of the untreated control biofilm areal cell density. Dashed lines connect data points from the same investigation. The antibiotics used include tobramycin, ciprofloxacin, and gentamicin. Sources: references . doi:10.1128/microbiolspec.MB-0010-2014.f5

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Antimicrobial efficacy as a function of biofilm age. Dashed lines connect data points from the same investigation. Sources: references . doi:10.1128/microbiolspec.MB-0010-2014.f6

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7
Figure 7

(A) Maturation of biofilm and (B) change in gentamicin susceptibility with age. The dashed line in panel A connects the mean values at each time point. The solid line in panel B is the least squares regressed fit. Source: reference . doi:10.1128/microbiolspec.MB-0010-2014.f7

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 8
Figure 8

Tolerance factors for biocides and antibiotics for four bacterial phyla and a fungus. doi:10.1128/microbiolspec.MB-0010-2014.f8

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 9
Figure 9

Medium effects on biofilm susceptibility to antibiotics. The different bar fills denote various media: LB (gray); LB + glucose (triangles); TSA, aerobic (white); TSA, anaerobic (hatched); noble agar, aerobic (black); noble agar, anaerobic (honeycomb). Sources: reference for and unpublished data of Borriello and Stewart for . doi:10.1128/microbiolspec.MB-0010-2014.f9

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 10
Figure 10

Experimentally measured antimicrobial penetration times in biofilms versus molecular weight of the antimicrobial. The penetration time was determined as the time to attain, at the base or center of the biofilm, 50% of the equilibrium concentration of the antimicrobial agent either through a direct measurement of the antimicrobial agent (solid circles) or by loss of membrane integrity detected with a fluorescent probe (open circles). Penetration times greater than 12 min are circled. Sources: references . doi:10.1128/microbiolspec.MB-0010-2014.f10

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 11
Figure 11

Experimentally measured antimicrobial penetration times in biofilms versus dose concentration. The line is the least squares regressed fit. Symbols indicate data for chlorine (cross, 55), chlorine (gray, 54), tobramycin (white, 62), peracetic acid (black, 53). doi:10.1128/microbiolspec.MB-0010-2014.f11

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 12
Figure 12

Comparison of antimicrobial susceptibility of exponential phase planktonic (solid symbols) or stationary phase planktonic (open symbols) to biofilm cells. The solid line is the line of equality. Points below the line indicate that biofilm cells were less susceptible than planktonic cells. Points above the line indicate that planktonic cells were less susceptible than biofilm cells. Sources: references . doi:10.1128/microbiolspec.MB-0010-2014.f12

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 13
Figure 13

Conceptual diagram of distinct cell states important for antimicrobial sensitivity. The dead cell state can presumably be accessed from any of the other states. doi:10.1128/microbiolspec.MB-0010-2014.f13

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817466.chap13
1. Stewart PS,, McFeters GA,, Huang CT, . 2000. Biofilm control by antimicrobial agents, p 373405. In Bryers JD (ed), Biofilms, 2nd ed. John Wiley & Sons, New York.
2. Mah TF,, O’Toole GA . 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9 : 3439.[PubMed] [CrossRef]
3. Stewart PS,, Costerton JW . 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358 : 135138.[PubMed] [CrossRef]
4. Lewis K . 2001. Riddle of biofilm resistance. Antimicrob Agents Chemother 45 : 9991007.[PubMed] [CrossRef]
5. Davies D . 2003. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Dis 2 : 114122.[PubMed] [CrossRef]
6. Stewart PS,, Mukherjee PK,, Ghannoum MA, . 2004. Biofilm antimicrobial resistance, p 250268. In Ghannoum M,, O’Toole GA (ed), Microbial Biofilms, 1st ed. ASM Press, Washington, DC. [CrossRef]
7. Bridier A,, Briandet R,, Thomas V,, Dubois-Brissonnet F . 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27 : 10171032.[PubMed] [CrossRef]
8. Ronner AB,, Wong AC . 1993. Biofilm development and sanitizer inactivation of Listeria monocytogenes and Salmonella typhimurium on stainless steel and Buna-n rubber. J Food Prot 56 : 750758.
9. Chen CI,, Griebe T,, Srinivasan R,, Stewart PS . 1993. Effects of various metal substrata on accumulation of Pseudomonas aeruginosa biofilms and efficacy of monochloramine as a biocide. Biofouling 7 : 421251.
10. Anwar H,, Strap JL,, Costerton JW . 1992. Establishment of aging biofilms: possible mechanism of bacterial resistance to antimicrobial therapy. Antimicrob Agents Chemother 36 : 13471351.[PubMed] [CrossRef]
11. Wolcott RD,, Rumbaugh KP,, James G,, Schultz G,, Phillips P,, Yang Q,, Watters C,, Stewart PS,, Dowd SE . 2010. Biofilm maturity studies indicate sharp debridement opens a time-dependent therapeutic window. J Wound Care 19 : 320328.[PubMed] [CrossRef]
12. Stewart PS . 1996. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother 40 : 25172522.[PubMed]
13. Stewart PS,, Raquepas JB . 1995. Implications of reaction-diffusion theory for the disinfection of microbial biofilms by reactive antimicrobial agents. Chem Eng Sci 50 : 30993104.[CrossRef]
14. Ramsey BW,, Pepe MS,, Quan JM,, Otto KL,, Montgomery AB,, Williams-Warren J,, Vasiljev-K M,, Borowitz D,, Bowman CM,, Marshall BC,, Marshall S,, Smith AL . 1999. Intermittent administration of inhaled tobramycin in patients with cystic fibrosis. New Engl J Med 340 : 2330.[PubMed] [CrossRef]
15. Corbin A,, Pitts B,, Parker A,, Stewart PS . 2011. Antimicrobial penetration and efficacy in an in vitro oral biofilm model. Antimicrob Agents Chemother 55 : 33383344.[PubMed] [CrossRef]
16. Tuomanen E,, Cozens R,, Tosch W,, Zak O,, Tomasz A . 1986. The rate of killing of Escherichia coli by [beta]-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 132 : 12971304.[PubMed]
17. Taber HW,, Mueller JP,, Miller PF,, Arrow AS . 1987. Bacterial uptake of aminoglycoside antibiotics. Microbiol Rev 51 : 439457.[PubMed]
18. Lewis K . 2007. Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5 : 4856.[PubMed] [CrossRef]
19. Lewis K . 2010. Persister cells. Annu Rev Microbiol 64 : 357372.[PubMed] [CrossRef]
20. Elkins JG,, Hassett DJ,, Stewart PS,, Schweizer HP,, McDermott TR . 1999. Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide: protective role of catalase. Appl Environ Microbiol 65 : 45944600.[PubMed]
21. Bagge N,, Schuster M,, Hentzer M,, Ciofu O,, Givskov M,, Greenberg EP,, Høiby N . 2004. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Antimicrob Agents Chemother 48 : 11751187.[PubMed] [CrossRef]
22. Pamp SJ,, Gjermansen M,, Johansen HK,, Tolker-Nielsen T . 2008. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 68 : 223240.[PubMed] [CrossRef]
23. Stewart PS,, Franklin MJ . 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol 6 : 199210.[PubMed] [CrossRef]
24. Nguyen D,, Joshi-Datar A,, Lepine F,, Bauerle E,, Olakanmi O,, Beer K,, McKay G,, Siehnel R,, Schafhauser J,, Wang Y,, Britigan BE,, Singh PK . 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334 : 982986.[PubMed] [CrossRef]
25. Bernier SP,, Lebeaux D,, DeFrancesco AS,, Valomon A,, Soubigou G,, Coppée JY,, Ghigo JM,, Beloin C . 2013. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet 9 : e1003144. doi:10.1371/journal.pgen.1003144. [PubMed] [CrossRef]
26. Liao J,, Schurr MJ,, Sauer K . 2013. The MerR-like regulator BrlR confers biofilm tolerance by activating multidrug-efflux pumps in Pseudomonas aeruginosa biofilms. J Bacteriol 195 : 33523363.[PubMed] [CrossRef]
27. Zhang L,, Mah TF . 2008. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190 : 44474452.[PubMed] [CrossRef]
28. Bjarnsholt T,, Jensen ,, Burmølle M,, Hentzer M,, Haagensen JA,, Hougen HP,, Calum H,, Madsen KG,, Moser C,, Molin S,, Høiby N,, Givskov M . 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151 : 373383.[PubMed] [CrossRef]
29. Harrison JJ,, Wade WD,, Akierman S,, Vacchi-Suzzi C,, Stremick CA,, Turner RJ,, Ceri H . 2009. The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing as a biofilm. Antimicrob Agents Chemother 53 : 22532258.[PubMed] [CrossRef]
30. Van Acker H,, Sass A,, Dhondt I,, Nelis HJ,, Coenye T . 2014. Involvement of toxin-antitoxin modules in Burkholderia cenocepacia biofilm persistence. Pathog Dis. [Epub ahead of print.] doi:10.1111/2049-632X.12177. [PubMed] [CrossRef]
31. Mah TF,, Pitts B,, Pellock B,, Walker GC,, Stewart PS,, O’Toole GA . 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426 : 306310.[PubMed] [CrossRef]
32. Colvin KM,, Gordon VD,, Murakami K,, Borlee BR,, Wozniak DJ,, Wong GC,, Parsek MR . 2011. The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa . PLoS Pathog 7 : e10012164. doi:10.1371/journal.ppat.1001264. [CrossRef]
33. Billings N,, Millan MR,, Caldara M,, Rusconi R,, Tarasova Y,, Stocker R,, Ribbeck K . 2013. The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog 9 : e1003526. doi:10.1371/journal.ppat.1003526. [CrossRef]
34. Lynch SV,, Dixon L,, Benoit MR,, Brodie EL,, Keyhan M,, Hu P,, Ackerley DF,, Andersen GL,, Matin A . 2007. Role of the rapA gene in controlling antibiotic resistance of Escherichia coli biofilms. Antimicrob Agents Chemother 51 : 36503658.[PubMed] [CrossRef]
35. Zhang L,, Hinz AJ,, Nadeau JP,, Mah TF . 2011. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J Bacteriol 193 : 55105513.[PubMed] [CrossRef]
36. Zhang L,, Chiang WC,, Gao Q,, Givskov M,, Tolker-Nielsen T,, Yang L,, Zhang G . 2012. The catabolite repression control protein Crc plays a role in the development of antimicrobial-tolerant subpopulations in Pseudomonas aeruginosa biofilms. Microbiology 158 : 30143019.[PubMed] [CrossRef]
37. Stewart PS,, Rayner J,, Roe F,, Rees WM . 2001. Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfmates. J Appl Microbiol 91 : 525532.[PubMed] [CrossRef]
38. Luppens SB,, Reij MW,, van der Heijden RW,, Rombouts FM,, Abee T . 2002. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl Environ Microbiol 68 : 41944200.[PubMed] [CrossRef]
39. Buckingham-Meyer K,, Goeres DM,, Hamilton MA . 2007. Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods 70 : 236244.[PubMed] [CrossRef]
40. Byun MW,, Kim JH,, Kim DH,, Kim HJ,, Jo C . 2007. Effects of irradiation and sodium hypochlorite on the micro-organisms attached to a commercial food container. Food Microbiol 24 : 544548.[PubMed] [CrossRef]
41. Griebe T,, Chen CI,, Srinivasan R,, Stewart PS, . 1993. Analysis of biofilm disinfection by monochloramine and free chlorine, p 151161. In Geesey GG,, Lewandowski Z,, Flemming HC (ed), Biofouling and Biocorrosion in Industrial Water Systems. Lewis Publishers, Boca Raton, FL.
42. Norwood DE,, Gilmour A . 2000. The growth and resistance to sodium hypochlorite of Listeria monocytogenes in a steady-state multispecies biofilm. J Appl Microbiol 88 : 512520.[PubMed] [CrossRef]
43. Oie S,, Huang Y,, Kamiya A,, Konishi H,, Nakazawa T . 1996. Efficacy of disinfectants against biofilm cells of methicillin-resistant Staphylococcus aureus . Microbios 85 : 223230.[PubMed]
44. Kim J,, Pitts B,, Stewart PS,, Camper A,, Yoon J . 2008. Comparison of the antimicrobial effects of chlorine, silver ion, and tobramycin on biofilm. Antimicrob Agents Chemother 52 : 14461453.[PubMed] [CrossRef]
45. Anwar H,, van Biesen T,, Dasgupta M,, Costerton JW . 1989. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system. Antimicrob Agents Chemother 33 : 18241826.[PubMed] [CrossRef]
46. Jass J,, Costerton JW,, Lappin-Scott HM . 1995. The effect of electrical currents and tobramycin on Pseudomonas aeruginosa biofilms. J Indust Microbiol 15 : 234242.[PubMed] [CrossRef]
47. Borriello G,, Werner EM,, Roe F,, Kim AM,, Ehrlich GD,, Stewart PS . 2004. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob Agents Chemother 48 : 26592664.[PubMed] [CrossRef]
48. Shapiro JA,, Nguyen VL,, Chamberlain NR . 2011. Evidence for persisters in Staphylococcus epidermidis RP62a planktonic cultures and biofilms. J Med Microbiol 60 : 950960.[PubMed] [CrossRef]
49. Tré-Hardy M,, Macé C,, Manssouri NE,, Vanderbist F,, Traore H,, Devleeschouwer MJ . 2009. Effect of antibiotic co-administration on young and mature biofilms of cystic fibrosis clinical isolates: the importance of the biofilm model. Int J Antimicrob Agents 33 : 4045.[PubMed] [CrossRef]
50. Singla S,, Harjai K,, Chhibber S . 2013. Susceptibility of different phases of biofilm of Klebsiella pneumoniae to three different antibiotics. J Antibiot 66 : 6166.[PubMed] [CrossRef]
51. Corcoran M,, Morris D,, De Lappe N,, O’Connor J,, Lalor P,, Dockery P,, Cormican M . 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Appl Environ Microbiol 80 : 15071514.[PubMed] [CrossRef]
52. Zuroff TR,, Bernstein H,, Lloyd-Randolfi J,, Jimenez-Taracido L,, Stewart PS,, Carlson RP . 2010. Robustness analysis of culturing perturbations on Escherichia coli colony biofilm beta-lactam and aminoglycoside antibiotic tolerance. BMC Microbiol 10 : 185. [PubMed] [CrossRef]
53. Bridier A,, Dubois-Brissonnet F,, Greub G,, Thomas V,, Briandet R . 2011. Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55 : 26482654.[PubMed] [CrossRef]
54. Davison WM,, Pitts B,, Stewart PS . 2010. Spatial and temporal patterns of biocide action against Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 54 : 29202927.[PubMed] [CrossRef]
55. de Beer D,, Srinivasan R,, Stewart PS . 1994. Direct measurement of chlorine penetration into biofilms during disinfection. Appl Environ Microbiol 60 : 43394344.[PubMed]
56. Jang A,, Szabo J,, Hosni AA,, Coughlin M,, Bishop PL . 2006. Measurement of chlorine dioxide penetration in dairy process pipe biofilms during disinfection. Appl Microbiol Biotechnol 72 : 368376.[PubMed] [CrossRef]
57. Lee WH,, Wahman DG,, Bishop PL,, Pressman JG . 2011. Free chlorine and monochloramine application to nitrifying biofilm: comparison of biofilm penetration, activity, and viability. Environ Sci Technol 45 : 14121419.[PubMed] [CrossRef]
58. Liu X,, Roe F,, Jesaitis A,, Lewandowski Z . 1998. Resistance of biofilms to the catalase inhibitor 3-amino-1,2,4-triazole. Biotechnol Bioeng 59 : 156162.[PubMed] [CrossRef]
59. Dabbi-Oubekka S,, Briandet R,, Fontaine-Aupart MP,, Steenkeste K . 2012. Correlative time-resolved fluorescence microscopy to assess antibiotic diffusion-reaction in biofilms. Antimicrob Agents Chemother 56 : 33493358.[PubMed] [CrossRef]
60. Sandt C,, Barbeau J,, Gagnon MA,, LaFleur M . 2007. Role of the ammonium group in the diffusion of quaternary ammonium compounds in Streptococcus mutans biofilms. J Antimicrob Chemother 60 : 12811287.[PubMed] [CrossRef]
61. Stewart PS,, Roe F,, Rayner J,, Elkins JG,, Lewandowski Z,, Ochsner UA,, Hassett DJ . 2000. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 66 : 836838.[PubMed] [CrossRef]
62. Tseng BS,, Zhang W,, Harrison JJ,, Quach TP,, Song JL,, Penterman J,, Singh PK,, Chopp DL,, Packman AI,, Parsek MR . 2013. The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol 15 : 28652878.[PubMed]
63. Vrany JD,, Stewart PS,, Suci PA . 1997. Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa biofilms displaying rapid-transport characteristics. Antimicrob Agents Chemother 41 : 13521358.[PubMed]
64. Anderl JN,, Franklin MJ,, Stewart PS . 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44 : 18181824.[PubMed] [CrossRef]
65. Liao J,, Sauer K . 2012. The MerR-like transcriptional regulator BrlR contributes to Pseudomonas aeruginosa biofilm tolerance. J Bacteriol 194 : 48234836.[PubMed] [CrossRef]
66. Podos SD,, Thanassi JA,, Leggio M,, Pucci MJ . 2012. Bactericidal activity of ACH-702 against nondividing and biofilm staphylococci. Antimicrob Agents Chemother 56 : 38123818.[PubMed] [CrossRef]
67. Spoering AL,, Lewis K . 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183 : 67466751.[PubMed] [CrossRef]
68. Thrower Y,, Pinney RJ,, Wilson M . 1997. Susceptibilities of Actinobacillus actinomycetemcomitans biofilms to oral antiseptics. J Med Microbiol 46 : 425429.[PubMed] [CrossRef]
69. Green PN,, Pirrie RS . 1993. A laboratory apparatus for the generation and biocide efficacy testing of Legionella biofilms. J Appl Bacteriol 74 : 388393.[PubMed] [CrossRef]
70. Wood P,, Jones M,, Bhakoo M,, Gilbert P . 1996. A novel strategy for control of microbial biofilms through generation of biocide at the biofilm-surface interface. Appl Environ Microbiol 62 : 25982602.[PubMed]
71. Walker JT,, Morales M . 1997. Evaluation of chlorine dioxide (ClO2) for the control of biofilms. Wat Sci Technol 35 : 319323.[CrossRef]
72. Goeres DM,, Loetterle LR,, Hamilton MA . 2007. A laboratory hot tub model of disinfectant efficacy evaluation. J Microbiol Meth 68 : 184192.[PubMed] [CrossRef]
73. Tabak M,, Scher K,, Hartog E,, Römling U,, Matthews KR,, Chikindas ML,, Yaron S . 2007. Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol Lett 267 : 200206.[PubMed] [CrossRef]
74. Stickler D,, Hewett P . 1991. Activity of antiseptics against biofilms of mixed bacterial species growing on silicone surfaces. Eur J Clin Microbiol Infect Dis 10 : 416421.[PubMed] [CrossRef]
75. Neyret C,, Herry JM,, Meylheuc T,, Dubois-Brissonnet F . 2014. Plant-derived compounds as natural antimicrobials to control paper mill biofilms. J Ind Microbiol Biotechnol 41 : 8796.[PubMed] [CrossRef]
76. Blanc V,, Isabal S,, Sánchez MC,, Llama-Palacios A,, Herrera D,, Sanz M,, León R . 2013. Characterization and application of a flow system for in vitro multispecies oral biofilm formation. J Periodont Res [Epub ahead of print.] doi:10.1111/jre.12110. [PubMed] [CrossRef]
77. Tafin UF,, Corvec S,, Betrisey B,, Zimmerli W,, Trampuz A . 2012. Role of rifampin against Propionibacterium acnes biofilm in vitro and in an experimental foreign-body infection model. Antimicrob Agents Chemother 56 : 18851891.[PubMed] [CrossRef]
78. Soriano F,, Huelves L,, Naves P,, Rodriguez-Cerrato V,, del Prado G,, Ruiz V,, Ponte C . 2009. In vitro activity of ciprofloxacin, moxifloxacin, vancomycin, and erythromycin against planktonic and biofilm forms of Corynebacterium urealyticum . J Antimicrob Chemother 63 : 353356.[PubMed] [CrossRef]
79. Khan W,, Bernier SP,, Kuchma SL,, Hammond JH,, Hasan F,, O’Toole GA . 2010. Aminoglycoside resistance of Pseudomonas aeruginosa biofilms modulated by extracellular polysaccharide. Int Microbiol 13 : 207212.[PubMed]
80. Folsom JP,, Richards L,, Pitts B,, Roe F,, Ehrlich GD,, Parker A,, Mazurie A,, Stewart PS . 2010. Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10 : 294. [PubMed] [CrossRef]
81. Zheng Z,, Stewart PS . 2004. Growth limitation of Staphylococcus epidermidis in biofilms contributes to rifampin tolerance. Biofilms 1 : 3135.[CrossRef]
82. Walters MC,, Roe F,, Bugnicourt A,, Franklin MJ,, Stewart PS . 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47 : 317323.[PubMed] [CrossRef]
83. Okuda K,, Zendo T,, Sugimoto S,, Iwase T,, Tajima A,, Yamada S,, Sonomoto K,, Mizunoe Y . 2013. Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother 57 : 55725579.[PubMed] [CrossRef]
84. Larsen T . 2014. Susceptibility of Porphyromonas gingivalis in biofilms to amoxicillin, doxycycline and metronidazole. Oral Microbiol Immunol 17 : 267271.[CrossRef]
85. Frank KL,, Reichert EJ,, Piper KE,, Patel R . 2007. In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrob Agents Chemother 51 : 888895.[PubMed] [CrossRef]
86. Al-Dhaheri RS,, Douglas LJ . 2008. Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob Agents Chemother 52 : 18841887.[PubMed] [CrossRef]
87. Hawser SP,, Douglas LJ . 1995. Resistance of Candida albicans biofilms to antifungal agents in vitro . Antimicrob Agents Chemother 39 : 21282131.[PubMed] [CrossRef]

Tables

Generic image for table
TABLE 1

Selected examples of tolerance of bacteria in biofilms to biocides and antiseptics

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014
Generic image for table
TABLE 2

Selected examples of tolerance of bacteria or fungi in biofilms to antibiotics

Citation: Stewart P. 2015. Antimicrobial Tolerance in Biofilms, p 269-285. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0010-2014

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error