RESEARCH LETTER
High-intensity narrow-spectrum light inactivation and wavelength
sensitivity of Staphylococcus aureus
Michelle Maclean, Scott J. MacGregor, John G. Anderson & Gerry Woolsey
The Robertson Trust Laboratory for Electronic Sterilisation Technologies, Department of Electronic and Electrical Engineering, University of Strathclyde,
Glasgow, Scotland
Correspondence: Michelle Maclean, The
Robertson Trust Laboratory for Electronic
Sterilisation Technologies, Department of
Electronic and Electrical Engineering,
University of Strathclyde, Royal College
Building, 204 George Street, Glasgow,
Scotland, G1 1XW, UK. Tel.: 144 0 141 548
2891; fax: 144 0 141 552 5398; e-mail:
[email protected]
Received 19 December 2007; accepted
15 May 2008.
First published online 16 June 2008.
DOI:10.1111/j.1574-6968.2008.01233.x
Editor: Mark Enright
Abstract
This study was conducted to investigate the bactericidal effects of visible light on
methicillin-sensitive and methicillin-resistant Staphylococcus aureus (MRSA), and
subsequently identify the wavelength sensitivity of S. aureus, in order to establish
the wavelengths inducing maximum inactivation. Staphylococcus aureus, including
MRSA strains, were shown to be inactivated by exposure to high-intensity visible
light, and, more specifically, through a series of studies using a xenon broadband
white-light source in conjunction with a selection of optical filters, it was found
that inactivation of S. aureus occurs upon exposure to blue light of wavelengths
between 400 and 420 nm, with maximum inactivation occurring at 405 5 nm.
This visible-light inactivation was achieved without the addition of exogenous
photosensitisers. The significant safety benefit of these blue-light wavelengths over
UV light, in addition to their ability to inactivate medically important microorganisms such as MRSA, emphasises the potential of exploiting these non-UV
wavelengths for disinfection applications.
Keywords
photodynamic inactivation; visible light;
Staphylococcus aureus ; wavelength sensitivity.
Introduction
The increasing problem of microbial antibiotic resistance
has generated interest in alternative methods of inactivating
problematic organisms such as methicillin-resistant Staphylococcus aureus (MRSA). One area of interest involves the
use of light-based treatment technologies. Much research
has been carried out involving the photodynamic inactivation (PDI) of S. aureus and MRSA using light, particularly
light of visible wavelengths, and exogenous photosensitisers
such as phenothiazinium dyes, including toluidine blue O
(Wilson & Yianni, 1995; Wainwright et al., 1998), methylene
blue (Wainwright et al., 1998; Zeina et al., 2001), and
porphyrin derivatives such as hematoporphyrin (Bertoloni
et al., 2000). The induction of intracellular porphyrin
production through pretreatment with d-aminolaevulinic
acid followed by light exposure has also provided a successful method for staphylococcal PDI (Nitzan & Kauffman,
1999; Nitzan et al., 2004).
The observation that visible light alone has bactericidal
properties has been previously documented for bacteria,
FEMS Microbiol Lett 285 (2008) 227–232
most notably, the acne-associated bacterium Propionibacterium acnes. Research into P. acnes has found that irradiation
of this organism with blue light leads to photosensitisation
of intracellular porphyrins, stimulation of which leads to the
production of reactive species, predominantly singlet delta
oxygen (1O2), and consequently, cell death (Papageorgiou
et al., 2000; Ashkenazi et al., 2003; Hamblin & Hasan, 2004).
Other bacteria that have been found to be susceptible to
inactivation solely through visible-light exposure include
Helicobacter pylori and some oral black-pigmented bacteria
(Feuerstein et al., 2004; Ganz et al., 2005; Soukos et al.,
2005).
Previous work on the use of pulsed UV-rich light (MacGregor et al., 1998; Anderson et al., 2000; Wang et al., 2005)
has now been expanded to investigate the bactericidal
properties of high-intensity, narrow-band visible-light
wavelengths against S. aureus and other bacterial pathogens
(Anderson et al., 2005; Maclean, 2006). This, and the more
recent work by Guffey & Wilborn (2006a, b), which documented the inactivation of S. aureus using super luminous
diodes, demonstrate that S. aureus can be inactivated
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c
228
M. Maclean et al.
optically using visible light without the use of exogenous
photosensitisers or d-ALA-induced porphyrins.
The present study was carried out to investigate and fully
characterise the bactericidal effect of visible light on
S. aureus. Firstly, the bactericidal effect of high-intensity
visible light (400 nm and longer) on S. aureus and MRSA
was investigated. Subsequently, to identify the region of the
visible spectrum that induces staphylococcal inactivation,
the visible wavelength sensitivity of S. aureus was investigated through a series of optical filter studies. The results
demonstrate that blue light between 400 and 420 nm, but
optimally 405 nm ( 5 nm), has bactericidal effects against
S. aureus.
Materials and methods
Microorganisms
The bacteria used in this study were as follows: S. aureus
NCTC 4135, Escherichia coli NCTC 9001 (National Collection of Type Cultures, Collindale, UK), MRSA LMG 15975
(The Belgian Co-ordinated Collections of Micro-organisms,
Gent, Belgium) and MRSA 16a (a clinical wound isolate
obtained from the Royal Infirmary, Glasgow). Test strains
were inoculated into 100 mL of nutrient broth (Oxoid, UK)
and cultivated at 37 1C under rotary conditions (at
125 r.p.m.). After an 18-h incubation period, the broth was
centrifuged at 3939 g for 10 min and the resultant pellet
resuspended in 100 mL phosphate-buffered saline (PBS)
(Oxoid, UK). This suspension was then diluted in PBS to
give a population density of c. 2.0 105 CFU mL 1 for
experimental use.
Visible light source
A xenon broadband white-light source (Hamamatsu Photonics UK Ltd), together with a 400 nm longwave pass (L-P)
filter, was used for the visible-light exposure of bacterial
Intensity (Arbitrary units)
4000
No Filter
3000
400nm L-P Filter in place
2000
1000
0
250
300
350
400
450
500
550
Wavelength (nm)
Fig. 1. Emission spectrum of xenon lamp from 200 to 500 nm. Also
shown is the emission spectrum when passed through a 400 nm longwave pass filter.
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c
suspensions and the relevant emission spectra are shown in
Fig. 1. The use of this filter allowed transmission of
wavelengths longer than 400 nm (i.e. visible light) and thus
eliminated UV-light inactivation.
High-intensity exposure experiments
The experimental set-up was as follows: a 2 mL volume of
bacterial suspension, with a population density of
2.0 105 CFU mL 1, was transferred to one well of a 12-well
multidish (Nunc, Denmark), which also contained a
7 mm 2 mm magnetic follower. The 400 nm L-P filter was
placed on top of the well. The dish was then positioned
directly under the light source on a magnetic stirrer. This, in
conjunction with the magnetic follower, permitted continuous mechanical agitation of the sample during light
exposure. For the experiments detailed, all parameters were
maintained constant: the sample volume used in each
experiment was 2 mL and the irradiance of the xenon lamp
through the 400 nm L-P filter was 350–400 mW cm 2 (measured using a radiant power meter and detector; L.O.T.
-Oriel Ltd, UK). A separate sample well containing 2 mL
bacterial suspension was used for each exposure time, and
after each exposure, samples were plated onto nutrient agar
(NA) (Oxoid, UK) (see ‘Bacterial Plating and Enumeration’)
and incubated at 37 1C for 24 h. Control samples were also
set-up; these were subjected to identical conditions but were
not exposed to high-intensity visible light, but left in normal
laboratory lighting conditions.
Filter study for identification of inactivation
wavelengths
The experimental set-up for the filter studies on S. aureus
NCTC 4135 was identical to that described above for the
high-intensity exposure experiments, with the 400 nm L-P
filter being substituted with, firstly, a selection of commercially available L-P and shortwave pass (S-P) filters (L.O.T.
-Oriel Ltd), which would identify the causative wavelength
range, and secondly, a selection of narrow bandpass (B-P)
filters ranging from 400 to 500 nm (L.O.T.-Oriel Ltd; Ealing
Catalog. Inc.), which would identify the causative bandwidth to within 10 nm.
For comparison of the germicidal efficiencies for each
narrow bandwidth, the output intensity of the lamp was
amended for each B-P filter so that the same irradiance
(3.27 mW cm 2) was transmitted onto each bacterial sample
for each filter. This 3.27 mW cm 2 irradiance was transmitted through each of the filters and illuminated each
bacterial sample for an equal time period of 2 h. From these
values, the absolute dose, also termed energy density, in
Joules per square centimetre [irradiance (W cm 2) time
(s)] for each 10 nm bandwidth being applied to the S. aureus
FEMS Microbiol Lett 285 (2008) 227–232
229
Light inactivation wavelength sensitivity of S. aureus
2
(3.27 mW cm
2
Bacterial plating and enumeration
In order to obtain accurate viable cell counts, several
standard plating methods were used in this study. The spiral
and spread plate methods, using 50 and 100 mL sample
volumes, respectively, were prepared on NA using a WASP
2 spiral plater (Don Whitley Scientific Ltd, UK). For samples
with anticipated low CFU counts, pour plates, using a 1-mL
sample volume, were prepared manually using molten NA.
Spiral plates were enumerated using the supplied counting
grid and tables. Spread and pour plates were counted
manually with the aid of a colony counter (Stuart Scientific,
UK). The resultant counts from each of these methods were
then converted into viable CFU counts mL 1 of sample.
6
Bacterial count
(Mean log10 CFU mL–1)
suspensions was calculated as 23.5 J cm
for 2 h).
5
4
3
2
1
0
0
10
20
30
40
50
60
70
Exposure time (min)
Fig. 2. Comparison of the effect of high-intensity visible light of
wavelengths 4 400 nm on suspensions of Staphylococcus aureus NCTC
4135 and Escherichia coli NCTC 9001. Data points for 15 min and above
for S. aureus, and 45 min and above for E. coli, are significantly different
from the respective controls.
Statistical analysis
Results
6
Bacterial count
(Mean log10 CFU mL–1)
With regard to the replication and recording of experimental results, in the high-intensity exposure experiments each
data point on the graphs represents the results from two
independent experiments, with a minimum of triplicate
samples being taken for each experiment. These results are
documented as mean values with SDs being included.
Significant differences in the light-treatment results were
calculated at the 95% confidence interval using ANOVA (one
way) with MINITAB software Release 15. Data on the germicidal efficiency of different wavelengths, as discussed later,
were obtained from replicated CFU count data and calculated as mean log10 reduction per unit dose.
5
4
3
2
1
0
0
10
20
30
40
50
60
70
Exposure time (min)
Fig. 3. Inactivation of MRSA strains in liquid suspension upon exposure
to high-intensity visible light of wavelengths 4 400 nm. Data points for
15 min and above for MRSA LMG 15975, and 25 min and above for
MRSA 16a, are significantly different from the respective controls.
High-intensity exposure experiments
FEMS Microbiol Lett 285 (2008) 227–232
Bacterial count
(Mean log10 CFU mL–1)
6
Figure 2 shows the results for the exposure of S. aureus
suspensions to high-intensity light of wavelengths
4 400 nm. It can be seen that the light had a significant
bactericidal effect on S. aureus, with a 5-log10 reduction
being achieved after a dose of 630 J cm 1 (350 mW
cm 2 30 min). The exposed E. coli suspensions demonstrated negligible inactivation over a 30-min exposure time,
although exposures of 45 and 60 min did demonstrate
significant differences compared with the associated control
samples, indicating that a more prolonged exposure may
induce further inactivation of the exposed E. coli population. In Fig. 3, it can be seen that when the MRSA strains
were light-exposed, inactivation results that were similar to
those obtained with S. aureus NCTC 4135 were observed
(Fig. 2). The population densities of all control samples
stayed constant throughout this series of experiments (Figs 3
and 4). Temperature was also monitored throughout the
5
4
3
2
<500 nm
>400 nm
>500 nm
Control
1
0
0
10
20
30
40
50
Exposure time (min)
Fig. 4. Effect of different wavelength ranges on the inactivation rate of
Staphylococcus aureus NCTC 4135 suspensions. Suspensions were
exposed to high-intensity light of the following wavelength ranges: (’)
500 nm and below; (m) 400 nm and above; () 500 nm and above. Data
points for 10 min and above for o 500 nm exposure, and 15 min and
above for 4 400 nm, are significantly different from the respective
controls.
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230
M. Maclean et al.
Table 1. Log10 reduction and germicidal efficiency (Z) values for the inactivation of Staphylococcus aureus NCTC 4135 following exposure to 10 nm
bandwidths of light from 400 to 420 nm, each for a dose of 23.5 J cm 2
Bandwidth (nm)
Initial Population, N0
(Log10CFU mL 1)
Final Population, N
(Log10CFU mL 1)
Log10 (N/N0)
Reduction
Zw (Log10(N/N0)/J cm 2)
400 5 nm
405 5 nm
410 5 nm
415 5 nm
420 5 nm
430 5 nm
5.36 ( 0.02)
5.29 ( 0.01)
5.31 ( 0.03)
5.20 ( 0.03)
5.26 ( 0.01)
5.35 ( 0.03)
3.83 ( 0.01)
2.89 ( 0.07)
4.16 ( 0.18)
4.65 ( 0.07)
4.99 ( 0.01)
5.25 ( 0.05)
1.5
2.4
1.1
0.5
0.3
0.1
0.064
0.102
0.047
0.021
0.013
0.004
Significant bacterial log reductions, calculated at a 95% confidence interval. (Data for 430 nm exposure shown for comparative purposes; data for
10
440–500 nm not shown).
w
Z, germicidal efficiency
light-exposure experiments and was found to not rise above
37 1C, eliminating any thermal inactivation effects.
Identification of inactivation wavelength range
As a first step to identify the wavelength range within the
visible spectrum inducing staphylococcal inactivation, different visible-wavelength ranges were selected using S-P and
L-P filters using similar irradiances. Figure 4 shows the
effects of the different wavelength ranges on the rate of
inactivation of S. aureus NCTC 4135 cells in PBS suspensions. Exposure to wavelengths of 500 nm and below
induced the most rapid inactivation rate, and this was likely
the result of the inclusion of UV wavelengths, which are well
known to have a strong germicidal effect. Wavelengths
longer than 400 nm also caused total inactivation. When
longer wavelengths of 500 nm and above were investigated,
no inactivation was observed. This confirmed that the
visible wavelengths inducing staphylococcal inactivation
were in the wavelength region of 400–500 nm.
Identification of the inactivation bandwidth
In order to identify the narrow bandwidth of visible light
between 400 and 500 nm inducing staphylococcal inactivation, B-P filters were used. The S. aureus suspensions
exposed to each narrow 10 nm bandwidth between 400 and
500 nm received an absolute dose of 23.5 J cm 2, and significant log10 reductions were achieved through exposure to
400–420 nm bandwidths, as shown in Table 1. Here it can be
seen that the maximum log10 reduction of S. aureus cells
resulted from exposure to 405 5 nm wavelength light.
Exposure to bandwidths of 430–500 nm did not cause
significant inactivation of the bacteria.
The inactivation capability at each wavelength can be
quantified as the germicidal efficiency, defined as the log10
reduction of a bacterial population by inactivation per unit
dose in Joule per square centimetre (Wang et al., 2005).
Thus, germicidal efficiency, Z = log10(N/N0) J cm 2.
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Numerical data for the germicidal efficiencies achieved
through light exposure to 10 nm bandwidths of light
from 400 to 430 nm (with centre wavelength increments of
5 nm) are listed in Table 1. The results show that the
germicidal efficiency peak of 0.102 log10 J cm 2 was
at 405 nm, but the 400 nm light also demonstrated
good germicidal activity for S. aureus, with a value of
0.064 log10 J cm 2. Bandwidths between 430 and 500 nm
demonstrated no significant germicidal efficiency against
S. aureus suspensions.
Discussion
Investigations using a high-intensity xenon lamp, in conjunction with a selection of commercially available L-P, S-P
and B-P filters, have demonstrated the sensitivity of
S. aureus to visible light, and also identified the bactericidal
wavelengths inducing maximum visible-light inactivation to
within a 10 nm bandwidth. The results have highlighted that
inactivation is evident using 400–420-nm-wavelength blue
light, with the most effective bactericidal activity at
405 5 nm. Wavelengths of longer than 430 nm were found
to induce no effect on the viability of S. aureus cells. The
occurrence of the peak at 405 nm suggests that an inactivation process is at its optimum within the S. aureus cells at
this specific wavelength.
The identification of this narrow band of inactivation
wavelengths highlights that the vast majority of the illuminating wavelengths emitted by the broadband xenon lamp
( 4 400 nm) were superfluous to the inactivation process.
Therefore, in Figs 2 and 3, although c. 630 J cm 2 was
required for a 5-log10 reduction of S. aureus and MRSA
strains, this was the total irradiance, only a small fraction of
which was responsible for the inactivation. Although this
value is useful for comparison with other studies that have
used broadband light sources, the experiments using the
narrowband filters provide more meaningful values of
absolute dose: 23.5 J cm 2 of 405 nm light resulting in a
2.4 log10 reduction of S. aureus.
FEMS Microbiol Lett 285 (2008) 227–232
231
Light inactivation wavelength sensitivity of S. aureus
The use of these dose values can also be used to explain
why throughout previous studies on the PDI of S. aureus
using exogenous photosensitisers, inactivation in the
absence of photosensitisers or d-ALA-induced porphyrins
has either been dismissed or not been discussed. Bertoloni
et al. (2000) and Zeina et al. (2001) both used broadband
light sources emitting visible light 400–700 nm (as used in
this study; Figs 2 and 3) for illumination of the bacterial
samples but only applied maximum doses of 3.6 and
20.16 J cm 2, respectively, compared with the much greater
630 J cm 2 dose applied in the present study (Figs 2 and 3).
The finding that exposure to high-intensity visible light,
at intensities that resulted in a 5 log10 reduction in S. aureus
and MRSA populations, had a negligible effect of E. coli
reflects results found in previous PDI studies involving
photosensitisers. In one study using pretreatment with
d-ALA, which used a white-light source for illumination (as
in the present study), the inactivation of E. coli required at
least 10-times higher doses to achieve similar activation
levels to that for S. aureus (Nitzan & Kauffman, 1999).
The sigmoidal shape of the inactivation curve for visiblelight inactivation reveals an initial period of low biocidal
activity that may indicate a requirement for a build-up of
energy, reactive molecules or cellular damage, which must
occur before induction of bacterial inactivation is initiated.
It is likely that the mechanism of inactivation is quite
different to that of continuous UV-C exposure, which
induces DNA damage, primarily as a result of UV absorption
by the DNA bases in the wavelength region 240–280 nm
(Blatchley & Peel, 1991), or near-UV light, inactivation by
which has been accredited to sublethal damage of DNA
repair systems (Tyrrell & Peak, 1978). Visible-light inactivation, on the other hand, as established for other bacteria
such as P. acnes, H. pylori and some black-pigmented
bacteria (Ashkenazi et al., 2003; Feuerstein et al., 2004; Ganz
et al., 2005; Soukos et al., 2005), has been accredited to the
photo-stimulation of endogenous intracellular porphyrin
molecules. These studies identified the stimulating wavelengths to be visible light in the wavelength region
400–500 nm, and more specifically 400–420 nm in the cases
of P. acnes and H. pylori (Ashkenazi et al., 2003; Elman et al.,
2003; Ganz et al., 2005). Because of the similarity in
causative wavelengths, it is hypothesised that the inactivation mechanism occurring with the S. aureus and MRSA
strains in the present study is also the result of photostimulation of intracellular porphyrins, which results in the
production of reactive species, predominantly singlet delta
oxygen (1O2), and consequently, cell death.
Papageorgiou et al. (2000) investigated the effect of blue
light on P. acnes and their findings are in general agreement
with those established in this study. They found that the
sensitivity of P. acnes to visible light was at a maximum in
the blue region of 415 nm. Papageorgiou et al. (2000) state
FEMS Microbiol Lett 285 (2008) 227–232
that 415 nm corresponds to the absorption maximum of the
specific porphyrin molecules produced by P. acnes. The
maximum of 405 nm determined in the present study may
indicate that porphyrin molecules that have different absorption maxima are present within S. aureus bacteria or are
produced by them. The recent work of Guffey & Wilborn
(2006a, b), however, reports inactivation of S. aureus at both
405 and 470 nm. In their study, low populations of S. aureus
plated onto agar surfaces were exposed to doses of magnitude similar to those used in the present study. For 405 nm
inactivation, they measured an approximate single log10
reduction in bacterial concentration for a dose of 15 J cm 2
compared with the reduction of 2.4 log10 for a dose of
23 J cm 2 found in this work. At 470 nm, Guffey & Wilborn
(2006b) measured a log10 reduction of around 0.4–0.5 for a
dose of 15 J cm 2; our results, on the other hand, indicate
that no inactivation of S. aureus occurs at 470 nm.
The germicidal efficiency of the 405-nm-wavelength light
is much lower than that for UV wavelengths; however, this
disadvantage may be more than outweighed for some
applications by the greater safety afforded at this wavelength. While it is well established that UV irradiation
provides a method of inactivating pathogenic microorganisms, it is not apposite to expose humans to UV radiation
because of the well-recognised risks of eye damage and skin
cancer. Significantly, this study has shown that these blue
wavelengths within the visible-light spectrum are capable of
inactivating S. aureus, including MRSA, while posing a
negligible threat to human health (ACGIH, 2007).
Acknowledgements
The first author would like to thank The Engineering and
Physical Sciences Research Council (EPSRC) for their support through a Doctoral Training Grant (awarded in 2002/
2003). All authors would like to thank The Robertson Trust
for their funding support.
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