170

Journal of Food Protection, Vol. 71, No. 1, 2008, Pages 170–175

Copyright 䊚, International Association for Food Protection

Research Note

Effect of Surface Roughness and Stainless Steel Finish on

Listeria monocytogenes Attachment and Biofilm Formation
ANDRES RODRIGUEZ,1 WESLEY R. AUTIO,2 AND LYNNE A. MCLANDSBOROUGH1*

1Department of Food Science, University of Massachusetts, 100 Holdsworth Way, Chenoweth Laboratory, Amherst, Massachusetts 01003; and
2Department of Plant, Soil, and Insect, 201 Natural Resources Road, Bowditch Hall, Amherst, Massachusetts 01003, USA

MS 07-182: Received 30 March 2007/Accepted 14 August 2007

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ABSTRACT
The purpose of this study was to evaluate the effect of surface roughness (Ra) and finish of mechanically polished
stainless steel (Ra ⫽ 0.26 ⫾ 0.05, 0.49 ⫾ 0.10, and 0.69 ⫾ 0.05 ␮m) and electropolished stainless steel (Ra ⫽ 0.16 ⫾ 0.06,
0.40 ⫾ 0.003, and 0.67 ⫾ 0.02 ␮m) on Listeria adhesion and biofilm formation. A four-strain cocktail of Listeria monocy-
togenes was used. Each strain (0.1%) was added to 200 ml of tryptic soy broth (TSB), and coupons were inserted to the
mixture for 5 min. For biofilm formation, coupons with adhesive cells were incubated in 1:20 diluted TSB at 32⬚C for 48 h.
The experiment was performed by a randomized block design. Our results show that the level of Listeria present after 48 h
of incubation (mean ⫽ 7 log CFU/cm2) was significantly higher than after 5 min (mean ⫽ 6.0 log CFU/cm2) (P ⬍ 0.01). No
differences in initial adhesion were seen in mechanically finished (mean ⫽ 6.7 log CFU/cm2) when compared with electro-
polished stainless steel (mean ⫽ 6.7 log CFU/cm2) (P ⬎ 0.05). Listeria initial adhesion (values ranged from 5.9 to 6.1 log
CFU/cm2) or biofilm formation (values ranged from 6.9 to 7.2 log CFU/cm2) was not significantly correlated with Ra values
(P ⬎ 0.05). Image analysis with an atomic force microscope showed that bacteria did not colonize the complete surface after
48 h but were individual cells or grouped in microcolonies that ranged from 5 to 10 ␮m in diameter and one to three cell
layers in thickness. Exopolymeric substances were observed to be associated with the colonies. According to our results,
electropolishing stainless steel does not pose a significant advantage for food sanitation over mechanically finished stainless
steel.

Listeria monocytogenes continues to be a problem for
human health and food processing plants. In 2002, in the
northeastern region of the United States, a large outbreak
of Listeria caused seven deaths and three miscarriages, and
46 people became sick. L. monocytogenes isolated from a
floor drain suggested that a poultry processing plant was
responsible for the outbreak. As a result, the processor vol-
untarily recalled 27.4 million lb (2,400 metric tons) of fresh
and frozen ready-to-eat turkey and chicken products (1).
Listeria can attach and adhere to processing surfaces (41)
and form biofilms (9, 25, 36, 43). It is believed that L.
monocytogenes can survive in a processing environment in
the form of biofilms (36). Extensive research has been con-
ducted on L. monocytogenes and biofilm formation on food
processing surfaces (19, 26, 27, 35, 43).
The effect of surface roughness (Ra) on bacterial ad-
hesion and retention has been evaluated with controversial
results. The Ra value is defined as ‘‘the arithmetic average
value of all departures from the mean line through the sam-
pling length’’ (38), and thus, a higher Ra value is an indi-
cation of greater surface roughness. Although some authors
have found a relationship between Ra values and bacterial
adhesion (3, 4, 34, 47), the opposite results have also been
* Author for correspondence. Tel: 413-545-1016; Fax: 413-545-1262;
E-mail: lm@foodsci.umass.edu.
published (18, 23, 38). Guobjornsdottir et al. (20) did not
find any differences in listerial adhesion to steel with dif-
ferent Ra values (ranging from 0.1 to 0.8 ␮m) after 15 min.
On the contrary, Arnold et al. (3) found that the adhesion
of a bacterial cocktail from a poultry processing plant after
1.5 h was dependent on the Ra. It has also been suggested
that after electropolishing stainless steel, the surfaces be-
come smoother, and bacterial attachment decreases (3, 4,
46). Most of these studies focus on bacterial adhesion after
short time periods (ranging from 5 to 30 min) and use dif-
ferent bacterial species. To our knowledge, no one has eval-
uated the initial adhesion and biofilm formation of L. mono-
cytogenes with stainless steel and different Ra values.
The atomic force microscope (AFM) was invented in
1986 (8), and since then, it has been used to image bacterial
cells (6, 7, 10, 39, 47). Extensive research has been done
to image stainless steel with different Ra values and finishes
(2, 3, 12, 34, 40, 46). The AFM has several advantages
over these techniques that include in situ visualization of
bacterial biofilms without further preparation of the sample
(37). L. monocytogenes biofilms have been imaged with a
scanning electron microscope (17, 22, 32, 35) and confocal
scanning laser microscopy (13, 28, 30), but no one, to our
knowledge, has imaged an L. monocytogenes biofilm in
stainless steel with an AFM.
The purpose of this study was to evaluate the initial
J. Food Prot., Vol. 71, No. 1
TABLE 1. Surface roughness (Ra) values expected and measured
for the stainless steel used in this experiment
Ra value (␮m)
0.25a 0.50a 0.75a
Mechanically finished
(MF)b 0.26 ⫾ 0.05 0.49 ⫾ 0.10 0.69 ⫾ 0.05
Mechanically finished
and electropolished
(MFE) 0.16 ⫾ 0.06 0.40 ⫾ 0.003 0.67 ⫾ 0.02
a was evaluated in triplicate every day, and the whole experiment
Ra value desired.
b Ra value measured (mean ⫾ standard deviation).
bacterial adhesion and biofilm formation of a four-strain
cocktail of L. monocytogenes with stainless steel using dif-
ferent Ra values. The AFM was used to image Listeria
biofilms on stainless steel.
MATERIALS AND METHODS
Bacterial strains. Stock cultures of four strains of L. mono-
cytogenes (LM10, LM21, LM27, and LM29) were stored at
⫺75⬚C in tryptic soy broth (Difco, Becton Dickinson, Sparks,
Md.) supplemented with (0.6%) yeast extract (TSBYE) with the
addition of glycerol to a final concentration of 12.5% (40). Month-
ly, working cultures were transferred from frozen to tryptic soy
agar with 0.6% yeast extract slants (TSAYE) at 32⬚C for 24 h and
stored at 4⬚C. Prior to every experiment, a loopful of each strain
was transferred from the working culture slant into 10 ml of
TSBYE that was incubated at 32⬚C for 18 h.
Slide preparation. The flat stainless steel coupons (type 304
with a 4b finish) used in this study had a total surface area of 13
cm2 per coupon. Stainless steel slides were mechanically polished
(mechanical finished [MF]; Harrison Electropolishing, Houston
Tex.) to a specified level of Ra (Table 1), and a subset of the
slides were further electropolished after mechanical polishing (me-
chanical finished with electropolishing [MFE]; Harrison Electro-
polishing). Stainless steel slides were washed and cleaned prior to
use as described by Djordjevic et al. (15). To remove the grease,
the slides were soaked in acetone for 10 min and washed with
distilled water. Slides were cleaned with ethanol and rinsed thor-
oughly with distilled water. Slides were boiled in distilled water
for 10 min. As a final step, stainless steel slides were placed in a
50-ml centrifuge tubes and autoclaved for 15 min at 121⬚C. Every
slide was used once.
Attached cell preparation. Each strain was individually
grown in 10 ml of TSBYE for 18 h. To prepare the inoculation
mixture, 0.1% of each strain was added to 200 ml of TSB. A total
of 10 ml of the mixture containing the bacteria was added to 10-
ml sterile test tubes containing stainless steel slides for 5 min.
Bacterial adhesion was performed with slides in a vertical orien-
tation. Stainless steel coupons were removed and rinsed with ster-
ile 0.1% buffered peptone water to remove loosely attached cells.
To determine attached cell numbers, stainless steel coupons were
inserted in 50-ml centrifuge tubes containing 30 ml of 0.1% buff-
ered peptone water and 3 g of glass beads (diameter, 710 to 1,180
microns; Sigma-Aldrich, St. Louis, Mo.), agitated for 1 min, di-
luted, and then plated on TSAYE with a spiral plater (Spiral Bio-
tech, Norwood, Mass.) (40).
Biofilm growth and preparation. After cells were attached
as described above, each coupon was placed in 10 ml of TSB
STAINLESS STEEL SURFACE ROUGHNESS AND FINISH 171
1:20 at 32⬚C for 48 h. Cell numbers were determined after re-
moval and plating as described in the previous section.
Atomic force microscope. A CP-II atomic force instrument
was used (Veeco, Santa Barbara, Calif.). To image the stainless
steel topography, a cantilever with a spring constant of 3 N/m
(Veeco) was used to image in contact mode in air at a speed of
0.7 Hz. Listeria biofilms were imaged with different scan sizes
from 100 by 100 ␮m, 25 by 25 ␮m, and 10 by 10 ␮m.
Experimental design and statistical analysis. The experi-
ment was designed with a randomized block design, each variable
was repeated 13 times. The results were analyzed by an analysis
of variance with SAS statistical software (SAS Institute, Cary,
N.C.).
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RESULTS
The level of Listeria present in the biofilms after 48 h
of incubation (mean ⫽ 7 log CFU/cm2) was significantly
higher than the attached cells after initial adhesion (mean
⫽ 6.0 log CFU/cm2) (P ⬍ 0.01). Biofilm formation oc-
curred independently of the surface finish (7.0 ⫾ 4.9 log
CFU/cm2 on MF and 7.0 ⫾ 6.0 log CFU/cm2 on MFE) (P
⬎ 0.05). Similarly, initial adhesion was independent of sur-
face finish (6.0 ⫾ 5.9 log CFU/cm2 for MF and 5.9 ⫾ 5.9
log CFU/cm2 for MFE) (P ⬎ 0.05). When these data were
broken down by surface finish and roughness (Fig. 1), the
effect of Ra on Listeria initial adhesion and biofilm for-
mation was not significantly different (P ⬎ 0.05). We did
not find any significant differences in Ra or finish on Lis-
teria initial adhesion (values ranged from 5.9 to 6.1 log
CFU/cm2) (Fig. 1A) or biofilm formation (values ranged
from 6.9 to 7.2 log CFU/cm2) (Fig. 1B) (P ⬎ 0.05).
To visualize stainless steel with different Ra values and
finishes, we used an AFM (Fig. 2). This microscope al-
lowed us to visualize the bacterial biofilms without any
preparation. When stainless steel was mechanically pol-
ished and further electropolished, its surface appeared
smoother than the mechanically finished stainless steel (40).
The AFM was used to image the bacteria on all stain-
less steel finishes used in this study. Listeria seemed to
grow along the stainless steel crevices in mechanically pol-
ished stainless steel (data not shown). This was not seen in
mechanically and further electropolished stainless steel,
though the overall bacterial counts were similar. The AFM
images clearly showed that Listeria did not colonize the
entire stainless surface but grew associated to the stainless
steel surface as individual cells or in the form of biofilms
as small microcolonies ranging from 5 to 10 ␮m in diam-
eter (Fig. 2) with exopolymeric substances (EPS) (Fig. 2C,
arrows). The height (Z-value) of individual cells imaged
with the AFM was 0.12 to 0.18 ␮m, and the height of the
microcolonies ranged from 0.2 to 0.45 ␮m, indicating that
the visualized microcolonies consisted of one to three cell
layers in thickness (Fig. 2C). Under all the surfaces tested,
microcolonies grew similarly (data not shown).
DISCUSSION
The overall purpose of this study was to evaluate the
effect of Ra values of stainless steel with two different fin-
172 RODRIGUEZ ET AL.
FIGURE 1. L. monocytogenes biofilm formation (A) and initial
bacterial adhesion (B) on stainless steel with three different
roughnesses and either MF (black bars) or MFE (gray bars).
ishes (MF versus MFE) on Listeria initial adhesion and
biofilm formation. The results of this study show that Lis-
teria adhesion and biofilm formation were independent of
Ra and finish.
Other researchers have come to various conclusions
about whether or not stainless steel surface finishes can in-
fluence bacterial adhesion; however, because of the great
variability in research protocols, it can be very difficult to
compare results. Bacterial adhesion has been studied after
time periods ranging from 5 min to 2 h and stainless steel
Ra values ranging from 0.1 to 3.3 ␮m (5, 18, 20, 23, 46).
To our knowledge, this study is unique in the use of a 48-h
biofilm growth in addition to adhesive cells on different
J. Food Prot., Vol. 71, No. 1
surfaces. Because we observed that initial adhesion was
independent of Ra and finish, it was not surprising to find
that biofilm formation at 48 h was also independent of Ra
and finish.
The results presented are in agreement with other re-
searchers who have not observed any influence of surface
finish or roughness upon bacterial adhesion. Hilbert et al.
(23) found no differences in Listeria adhesion to steel with
different roughness values (Ra ⫽ 0.01 to 0.9 ␮m) after 5
and 25 min of adhesion time. Similarly, Guobjornsdottir et
al. (20) did not find any differences in stainless steel with
different Ra values (ranging from 0.1 to 0.8 ␮m) and lis-
terial adhesion after 15 min. Verran and Boyd (45) used
two different bacterial species, Staphylococcus aureus and
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Pseudomonas aeruginosa, and studied the adhesion to
stainless steel with two grades (304 and 316) and different
finishes after 60 min, and no differences were seen regard-
ing Ra and bacterial adhesion. The initial adhesion evalu-
ated in our study was done after 5 min. The results of our
research are comparable to these studies.
These results are contradictory with several studies that
showed a relationship between surface finish and bacterial
adhesion (3, 4, 34, 47). Arnold et al. (3) evaluated the effect
of control stainless steel versus electropolished steel at low-
er Ra values than tested in this study. They observed lower
adhesion as the Ra was reduced from 0.14 to less than 0.02
␮m with a cocktail of bacteria from a poultry processing
plant after 1 to 2 h and observed significantly lower levels
of bacteria on electropolished stainless steel than on the
control (3). Similarly, Arnold and Silvers (4) found that
attachment to stainless steel and early biofilm formation of
a mixture of bacteria were decreased on electropolished
stainless steel. Contrary to these results, Sofyan et al. (42)
observed an increase in adhesion of L. monocytogenes after
electropolishing stainless steel.
In this article, we used an AFM to visualize listerial
biofilms. Other microscopy techniques to visualize bacterial
cells, such as confocal scanning laser microscopy, require
bacteria to be stained with fluorescent DNA or molecular
dyes prior to imaging (17, 28, 30, 32, 35). Similarly, scan-
ning electron microscopy sample preparation includes de-
hydration, a conductive surface for imaging, and imaging
under vacuum (24). On the contrary, the major condition
needed to image bacterial cells with an AFM is immobili-
zation on a supportive material (24). This allows us to im-
age biofilms because they grow on surfaces (37). In general,
it is recommended that biological systems be imaged with
an AFM cantilever with a low spring constant (k ⫽ 0.9
N/m) to minimize the damage of soft samples (Veeco).
However, after performing AFM analysis with cantilevers
having various spring constants, we have found that low
spring constant cantilevers catch and skip violently during
the imaging of biofilms. We believe this was because the
cantilever tip became trapped in the bacterial EPS. The
problem was alleviated by the use of cantilevers with higher
spring constants (k ⫽ 3 N/m) (data not shown). The use of
AFM to image Listeria biofilms required minimum sample
preparation and allowed us to visualize bacteria in their
natural, hydrated state. With the AFM, we were able to
J. Food Prot., Vol. 71, No. 1 STAINLESS STEEL SURFACE ROUGHNESS AND FINISH 173

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FIGURE 2. Atomic force images (three dimensional) of a stainless steel coupon with a measured surface roughness of 0.64 ␮m
mechanically finished and further electropolished. (A) Measured at 100 by 100 ␮m. Bacterial biofilm microcolonies ranging from 5 to
10 ␮m can be seen. (B) An image (25 by 25 ␮m) in more detail of a Listeria microcolony (boxed in A). (C) An image (10 by 10 ␮m)
of a microcolony composed of Listeria cells (boxed in A and B) and exopolymeric substances (arrows).

image how listerial biofilms grow on stainless steel whose
morphology was observed to be independent of the Ra.
Listeria has been shown to produce EPS during biofilm
formation (11, 13, 21, 22). EPS is an integral part of the
biofilm definition of Donlan and Costerton (16): ‘‘A biofilm
is a sessile microbial community characterized by cells that
are irreversibly attached to a substratum, interface or to
each other, embedded in a matrix of EPS that they have
produced.’’ EPS composition can vary and be composed of
carbohydrates and proteins and, to a lesser extent, other
substances such as lipids or DNA (14, 31). With the AFM,
we were able to image Listeria biofilms in which cells were
associated with possible EPS (Fig. 2C); however, this meth-
od cannot be used to define composition. Biofilm EPS is
thought to contribute to antimicrobial agent resistance and
desiccation survival and to enhance nutrient capture (14,
29, 33, 44).
According to our study, Listeria biofilms are formed
on stainless steel independently on the surface finish (Ra).
Sanitation techniques need to be addressed to avoid initial
adhesion and bacterial retention; once a biofilm is formed,
it is harder to remove (14, 33), and bacterial transfer and
cross-contamination of food products increase (40).
ACKNOWLEDGMENT
This research was funded by U.S. Department of Agriculture Na-
tional Research Initiative Competitive Grant 2003-35201-13549.
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