© 2010 Nature America, Inc. All rights reserved.
PROTOCOL
1460 | VOL.5 NO.8 | 2010 | NATURE PROTOCOLS
INTRODUCTION
Clinicians who deal with device-related and other chronic bacterial
infections increasingly face a new category of infectious diseases
that differs radically from acute epidemic bacterial infections. These
diseases are much less aggressive than acute infections, they often
persist for months or years, and they progress through periods of
latency that alternate with periods of acute exacerbation. Moreover,
although traditional antibiotic therapy provides some relief during
such exacerbations, antibiotics fail to resolve the infections
1
.
Chronic bacterial infections with Pseudomonas aeruginosa have
an important role in pulmonary infection in cystic fibrosis (CF)
2
.
The majority of people with CF acquire P. aeruginosa, and in these
people, chronic lung infection, repeated exacerbations and progres-
sive deterioration in lung function remain major causes of morbidity
and mortality. In the chronically infected CF lung, P. aeruginosa
adopts a biofilm mode of growth with the formation of structured
microbial communities that grow within microcolonies embedded
in an extracellular matrix. It has been shown that with the forma-
tion of bacterial biofilms, it becomes extremely difficult to eradicate
the infection
3
. Biofilm bacteria are much more resistant to antibi-
otic treatment, as well as to the host immune response, and we are
only beginning to understand the reasons for this biofilm recalci-
trance
4–7
. The formation of bacterial biofilms profoundly influences
the biological activities of the constituting bacteria in a way that is
not easily predicted on the basis of our current knowledge
8,9
.
Despite evidence that P. aeruginosa grows within microcolonies in
the airways of people with CF, conventional clinical susceptibility test-
ing involves the culture of planktonically grown bacteria that have been
recovered from the respiratory tract. Consequently, antibiotic therapy
is directed by these susceptibility test results to treat symptomatic indi-
viduals affected by CF with chronic infections. However, it seems rea-
sonable that the antibiotic susceptibilities of planktonic populations, as
determined by minimal inhibitory concentration (MIC) methodolo-
gies, do not necessarily reflect the actual resistance profile in vivo
10
.
One may argue that the strategies of susceptibility testing
should account for differences in growth behavior within biofilms,
in which the bacteria grow slowly and are densely packed in a
microaerophilic environment
11,12
. Previous studies comparing the
antibiotic resistance profile of biofilm- versus planktonic-grown
P. aeruginosa have revealed that there is obviously not a single agent
or combination of agents that dominates the biofilm susceptibility
profile of CF isolates
5,13
, and others have shown that people treated
with biofilm-effective therapy had improved clinical outcomes
14
. This
implies a need for individualized biofilm susceptibility testing in the
clinical setting. Nevertheless, even if antimicrobial biofilm resistance
is strain specific, it is indispensable to clearly show in clinical trials
that biofilm susceptibility testing results in sufficiently different treat-
ment regimes and that these treatment regimes benefit people with
CF
15
. However, the major problem faced in evaluating the benefit of
alternative antibiotic treatment has been the lack of a suitable assay
that could provide clinicians with an antibiotic resistance profile of
biofilm-grown bacteria. The use of a standardized and reliable high-
throughput system to monitor biofilm growth in the presence of
various antibiotics would overcome this hindrance.
In 1999, a 96-well-plate–based assay to monitor biofilm formation
and perform subsequent quantitative microbiology was established
in Ceri’s laboratory, and since then it has been widely used to test
antimicrobial resistance profiles of biofilm-grown clinical isolates
in several bacterial pathogens
16–21
. However, this test system is very
material- and time-consuming and is hardly applicable to antimi-
crobial resistance testing in routine diagnostics. Other alternative
methods to quantify microbial biofilms have been tested for vari-
ous organisms. One of these alternative methods for the testing of
drug effects on biofilm cells is the colorimetric determination of
metabolic activity after drug exposure
22–28
, which requires less post-
processing of samples and correlates with cell viability (as opposed,
for example, to crystal violet staining of the bacterial biofilm mass)
29
.
A 96-well-plate–based optical method for the
quantitative and qualitative evaluation of
Pseudomonas aeruginosa biofilm formation and its
application to susceptibility testing
Mathias Müsken
1,4
, Stefano Di Fiore
2
, Ute Römling
3
& Susanne Häussler
1,4
1
Chronic Pseudomonas Infection Research Group, Helmholtz Center for Infection Research, Braunschweig, Germany.
2
Fraunhofer Institute for Molecular Biology and
Applied Ecology, Aachen, Germany.
3
Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.
4
Pathophysiology of Bacterial
Biofilms, Twincore, Center for Experimental and Clinical Infection Research, a joint venture of the Helmholtz Center for Infection Research and the Medical School
Hannover, Hannover, Germany. Correspondence should be addressed to S.H. (susanne.haeussler@helmholtz-hzi.de).
Published online 29 July 2010; doi:10.1038/nprot.2010.110
A major reason for bacterial persistence during chronic infections is the survival of bacteria within biofilm structures, which protect
cells from environmental stresses, host immune responses and antimicrobial therapy. Thus, there is concern that laboratory methods
developed to measure the antibiotic susceptibility of planktonic bacteria may not be relevant to chronic biofilm infections, and it
has been suggested that alternative methods should test antibiotic susceptibility within a biofilm. In this paper, we describe a fast
and reliable protocol for using 96-well microtiter plates for the formation of Pseudomonas aeruginosa biofilms; the method is easily
adaptable for antimicrobial susceptibility testing. This method is based on bacterial viability staining in combination with automated
confocal laser scanning microscopy. The procedure simplifies qualitative and quantitative evaluation of biofilms and has proven to be
effective for standardized determination of antibiotic efficiency on P. aeruginosa biofilms. The protocol can be performed within ~60 h.