Food and Nutrition Sciences, 2013, 4, 299-304
http://dx.doi.org/10.4236/fns.2013.43040 Published Online March 2013 (http://www.scirp.org/journal/fns)
Quantitative Adhesion of Staphylococcus aureus on
Stainless Steel Coated with Milk
Fatima Hamadi1,2, Hassan Latrache2*, Fatima Asserne2, Soumya Elabed3,4, Ha f i da Zahir2,
Ibnsouda Koraichi Saad3,4, Hafida Hanine2, Jamaa Bengourram5
1Laboratory of Biotechnology and Vaorization of Natural Resources, Department of Biology, Faculty of Science, University Ibn
Zohr, Agadir, Marocco; 2Laboratory of Valorization and Safety of Food Products, Faculty of Sciences and Technics, University Sul-
tan Moulay Slimane, Beni Mellal, Morocco; 3Laboratoy of Microbial Biotechnology, Faculty of Science and Technics, University
Sidi Mohamed Ben Abdellah, Fés-Sáis, Marocco; 4Regional University Center of Interface, University Sidi Mohamed Ben Abdellah,
Fés, Marocco; 5Laboratory of industrial Engineering, Food and Environment, Faculty of Sciences and Technics, University Sultan
Moulay Slimane, Beni Mellal, Marocco.
Received September 14th, 2011; revised December 9th, 2011; accepted December 16th, 2011
ABSTRACT
The surface energy characteristics of uncoated (clean) and coated stainless steel with UHT milk at various contact time
(5 min, 30 min, 1 hours, 3 hours, 6 hours, 24 hours) were determined using contact angle measurement. Whatever the
contact time, the clean stainless steel coupons became more hydrophobic and more electron acceptor when they are
coated by milk. Inversely, the electron donor character seems to decreasing in this condition. The calculated surface
energy component of coated stainless steel was found to vary with contact time. Its hydrophobicity and its electron ac-
ceptor were minimal after 3 hours of contact, but its electron donor was minimal after 1 hours of contact. Adhesion ex-
periments of Staphylococcus aureus were carried out on uncoated and coated stainless steels at various contact times.
For all contact times, the adhesion results show that milk reduce S. aureus adhesion, and the level of this reduction de-
pend on contact time. This reduction was lower and higher after 1 hour, 5 min and 30 min of contact respectively.
Keywords: Surface Energy Characteristics; S. aureus; Adhesion; Milk; Stainless Steel
1. Introduction
The formation of biofilm creates major problems in the
food industry since it may represent an important source
of contamination for materials or foodstuffs coming into
contact with them, so leading to food spoilage or trans-
mission of diseases. Biofilms are of interest in the dairy
industry, as bacteria within biofilms are more difficult to
eliminate than plank tonic cells, and bacteria detached
from biofilms can contaminate milk and milk products
[1]. This biotransfer may affect hygiene and the com-
mercial value of the product. To control these problems,
it has been recognized that a greater understanding of the
interactions between microorganisms and food—process-
ing surface is required [2-4].
The adhesion of bacteria to surface is the first and es-
sential stage in the formation of biofilm. This adhesion
depends on both physicochemical properties of cell sur-
face and solid surface, and also on characteristics of the
surrounding medium.
Stainless steel is the most frequently used material for
food processing equipment because of its high impor-
tance related to food safety reasons. There are many cir-
cumstances in dairies where substratum surface is either
continuously or periodically in contact with liquids that
contain microorganisms. These conditions could affect
the substratum surface properties and consequently the
adhesion process.
Staphylococcus aureus is a gram positive bacterium,
which is an important food-borne pathogen [5-7]. In food
industry this organism could be able to attach and to
form biofilms on the food-processing surface [5,7,8]. S.
aureus was studied here because little information [5-7]
is available of its adhesion behaviour in dairy industry in
comparison with other organisms such as Listeria mono-
cytognes and bacillus [4,9-12].
The aim of this study was therefore to investigate the
surface properties of stainless steel at various times of
contact with milk. The adhesion of S. aureus to stainless
steel was also examined and discussed in terms of phys-
icochemical properties of cell surface and substratum
surface.
*Corresponding author.

Quantitative Adhesion of Staphylococcus aureus on Stainless Steel Coated with Milk 300
2. Materials and Methods
2.1. Bacterial Strains, Growth Conditions and
Preparation of Microbial Suspension
The bacterial strain used in this study was Staphylococ-
cus aureus ATCC 25923. The strain was cultured in Lu-
ria Burtani broth at 37˚C for 24 h after culture, the cells
were harvested by centrifugation for 15 min at 8400 xg
and were washed twice with and resuspended in KNO3
solution with ionic strength 0.1 M. The physicochemical
properties of this strain were measured by contact angle
measurements. The results are presented in Table 1 [13].
2.2. Cleaning of Stainless Steel Coupons
The solid support selected for this study was stainless
steel 304. Before being coated with milk, the steel was
cut into 1cmx1cm coupons and cleaned by soaking for 15
min in ethanol solution. The coupons were then rinsed
with distilled water and autoclaved at 120˚C for 15 min.
2.3. Treatment of Stainless Steel Coupons with
UHT-Milk
The cleaned stainless steel coupons were placed into a
Petri dish and 10 ml of ultrahigh-temperature (UHT)-
treated milk was added. The steel was allowed to contact
milk for 5 min, 30 min, 1 h, 3 h, 6 h and 24 h at 4˚C. Af-
ter each contact time, the coupons of steel were rinsed
three times with distilled water.
2.4. Contact Angle Measurements
Contact angle measurements were performed using a
goniometer (GBX instruments, France) by the sessile
drop method. One drop of a liquid was deposited onto a
dry stainless steel uncoated and coated by milk at differ-
ent contact times. Three to six contact angle measure-
ments were made on substratum surface for all probe
liquids including water, formamide and diiodomethane.
The Lifshitz-Van der Waals (γLW), electron donor (γ−) and
electron acceptor (γ+) components of the surface tension
of bacteria and for stainless steel were estimated from the
approach proposed by Van Oss et al. (1988) [14]. In this
approach the contact angles (θ) can be expressed as:
cos1 222
LW LW
SLSL SL
LL
The Lewis acid-base surface tension component is de-
fined by:
2
AB
SSS




The surface hydrophobicity was evaluated through
contact angle measurements and by the approach of Van
Oss [14,15]. In this approach, the degree of hydrophobic-
ity of a given material (i) is expressed as the free energy
of interaction between two entities of that material when
immersed in water (w): ΔGiwi. If the interaction between
the two entities is stronger than the interaction of each
entity with water, the material is considered hydrophobic
(ΔGiwi < 0); conversely, for a hydrophilic material, ΔGiwi
> 0. ΔGiwi is calculated through the surface tension com-
ponents of the interacting entities, according to the fol-
lowing formula:


2
22
2
iwi
LW LW
iwi w
iiww wiiw
G

   
   


 






2.5. Adhesion Experiments
Ten millimetres of bacterial suspension containing 108
CFU.ml−1 was incubated in a Petri dish containing stainless
steel coupons treated by milk for 3 h at 4˚C. After 3 h of
incubation, the coupons were then rinsed three times with
distilled water to remove the nonadhering bacteria. The
stainless steel coupons were immersed in a test tube con-
taining physiological water (Nacl: 9 g/l). Bacterial cells
were detached from the inert support by using a sonica-
tion bath (ultrasonic) for 5 min. CFUs were counted by
using the serial dilution technique of the bacterial sus-
pension obtained after sonication. Counts were deter-
mined on Luria Burtani agar after incubation for 24 h at
37˚C. Each experiment was performed in duplicate.
3. Results and Discussion
3.1. Surface Free Energy Characteristics of
Stainless Steel Uncoated and Coated
with Milk at Various Contact Times
Contact angles were measured on stainless steel surface
before and after coating with milk using the three test
liquids: water, formamide and diidomethane (Table 2).
L



 
 


Table 1. Contact angle values, surface energy and their components of S. aureus [13].
Contact angle Surface free energy components (mj/m2)
Water Formamide Diidomethane γLW γ− γ+ γAB γt ΔGiwi
26.45 (1) 30.4 (1) 59.45 (2) 28.85 (0) 51.3 (0.99)2.4 (0) 21.9 (3) 50.75 (2.4) 28.57
Standard deviation is given in parentheses.

Quantitative Adhesion of Staphylococcus aureus on Stainless Steel Coated with Milk 301
Table 2. Contact angle values, surface energy and their components of uncoated (control) and coated stainless steel at differ-
ent contact times.
Contact angle Surface free energy components (mj/m2)
Contact time
Water Formamide DiidomethaneγLW γ− γ+ γAB γt ΔGiwi
Control 64 (2) 68 (1.8) 60 (5) 28.1 (2.6)32.5 (2) 0.1 (0) 3.16 (2) 31 (5) 11.5
5 min 127 (5) 104 (1.13) 79 (2) 18 (3) 0.5 (0) 0.7 (0) 0.75 (0.3) 18.8 (4) −73.53
30 min 129 (2) 107 (4) 75 (4) 19.65 (2.1)0.45 (0) 1.15 (0.6)0.85 (1) 20.5 (3) −69.76
1 h 129 (0.7) 112 (0.9) 72 (4) 21.45 (2)0.05 (0) 3.25 (0.4)0.4 (0) 21.9 (1.9) −62.68
3 h 115 (0.45) 72 (0.9) 51 (0.6) 33.3 (0.3)3.9 (0.1) 0.6 (0.1) 3 (0.37) 36.5 (0.6) −42.10
6 h 127 (4) 96 (4) 63 (2) 26.6 (1.1)1.6 (1) 1.11 (0.2)2.3 (1.2) 28.9 (2.4) −67.60
24 h 115 (1.7) 73 (3) 56 (0.7) 31.19 (0.6)3.1 (0.7) 0.7 (0.4) 2.9 (1.1) 34.13 (1.8) −64.46
Standard deviation is given in parentheses.
The contact angle data were then used to calculate the
surface energy components of all samples (Table 2). The
results show that uncoated stainless steel surface was
hydrophilic with ΔGiwi = 11.50 mj/m2. Regardless of
contact time, stainless steel coated with milk alters sig-
nificantly its surface hydrophobicity. The uncoated
stainless steel surface hydrophobycity ranged from hy-
drophilic character (positive value of ΔGiwi) to hydro-
phobic character (negative value of ΔGiwi). It is known
that milk is a complex biological fluid composed by sev-
eral components including proteins, fats and calcium
phosphate. According to Mittelman (1998) [16], the ad-
sorption of milk and its components on substratum sur-
face occurs within 5 s to 10 s.
The effect of proteins hydrophobicity of solid surface
is reported by some works [17,18]. Yang et al. (1991)
[17] have found that the adsorption of β-lactoglobulin
onto substratum surface could render hydrophilic sur-
faces more hydrophobic and hydrophobic surfaces more
hydrophilic. Barnes et al. (1999) [5] reported that the fat
components are likely to interact with hydrophobic sur-
face of stainless steel. Other works [19], have reported
that surface energy characteristics of a solid surface in-
fluence the extent and rate of protein adsorption. In our
work the observed increasing hydrophobicity of coated
stainless steel could be due to the adsorption of proteins
and/or fat components to substratum surface. The order
of deposition of milk components should be related to
initial surface energy characteristic of substratum.
Harnett et al. (2006) [20] have calculated the surface
energy of various materials coating a series of proteins of
collagen, and fibroncetin and they found that these pro-
teins affect significantly the electron donor and the elec-
tron acceptor of some substratum surfaces. To our knowl-
edge, the effect of proteins or other components of milk
on electron donor/electron acceptor properties of sub-
stratum surface were not examined previously. Stainless
steel coated with milk has a very lower electron donor
compared to stainless steel uncoated with very high elec-
tron donor property (Table 2). In opposite, the electron
acceptor of stainless steel was not markedly affected by
the presence of milk (Table 2). The variation of hydro-
phobicity, electron donor and electron acceptor proper-
ties of stainless steel pretreated with milk as a function of
contact time are presented in Figure 1.
The surface hydrophobicity decreases from 5 min to 3
h and increases from 3 h to 24 h (Figure 1(a)). This hy-
drophobicity achieved the minimum at 3 h of contact.
Figures 1(b) and (c) show that contact time affect mark-
edly the electron donor and electron acceptor properties
of coated stainless steel. The electron donor and electron
acceptor properties achieved the maximum at 3 h of con-
tact and 1h of contact respectively.
Kim and Lund (1997) [21] have found that the adsorp-
tion process for β-lactoglobulin on stainless steel was
very rapid in the first 5 min and essentially reached equi-
librium within 10 min. These authors have also reported
that the precipitation of calcium phosphate onto the stain-
less steel surface was very slow compared to monolayer
deposition of β-lactoglobulin. Addesso and Lund (1997)
[19] show that protein adsorption onto a surface depends
on protein concentration. The random observed variation
of physicochemical properties of stainless steel as a func-
tion of contact time should be related to a nature and an
amount of milk components adsorbed onto substratum
surface and its kinetic deposition.
3.2. Adhesion of S. aureus to Stainless Steel
Treated with Milk under Different Contact
Time. Kinetic Evolution of S. aureus
Adhesion on Stainless Steel
Pretreated by Milk
Several works [4,5,11,12,22-24] have studied the effect
of milk or proteins milk on bacterial adhesion. In this
study, we are interested to examine the adhesion kinetic
of S. aureus to stainless steel coated with UHT milk. The
results of S. aureus adhesion on coated and uncoated
stainless steel are presented in Figure 2.
Coated stainless steel with UHT milk was shown to
reduce the attachment of S. aureus whatever contact time.

Quantitative Adhesion of Staphylococcus aureus on Stainless Steel Coated with Milk 302
(a)
(b)
(c)
Figure 1. Variation of physicochemical properties of stai nl e ss
steel coated with milk as a function of contact time. (a) Hy-
drophobicity; (b) Electron donor property; (c) Electron
acceptor property.
The role of milk or components of milk in inhibiting
bacterial adhesion was reported previously by several
works. Barnes et al. (1999) [5] have reported that the
pretreatment of stainless steel with skim milk was found
to reduce S. aureus adhesion. According to Hood and
Figure 2. Number of S. aureus cells adhered to uncoated
(control) and coated stainless steel at different contact times.
Zottola (1997) [4], the attachment of Listeria monocyto-
genes and Salmonella typhimurium to stainless steel was
inhibited by preconditioning with whole and chocolate
milk and was enhanced when using diluted milk.
To our knowledge, the surface physicochemical prop-
erties have not been considered in interpreting the effect
of milk on bacterial adhesion results despite the clear
change in substratum surface physicochemical properties
after contact with milk or milk components.
The adhesion results obtained here were discussed and
interpreted in terms of hydrophobicity and electron do-
nor/electron acceptor properties of both surfaces (cell
surface, stainless steel surface). The electrostatic interac-
tions were neglected since our experience was performed
in a solution with high ionic strength [25,26]. Since S.
aureus is hydrophilic (Table 1) and uncoated stainless
steel surface is also hydrophilic (Table 2), the S. aureus
adhesion on this substratum was increased. In the other
hand, the adhesion of hydrophilic S. aureus was reduced
on hydrophobic stainless steel coated with milk. These
results are in accord with the hypothesis that the hydro-
phobic cells tend to attach to a hydrophobic substrate and
the hydrophilic cells tend to attach to a hydrophilic sub-
strate. On the other hand, the difference in level adhesion
between stainless uncoated and coated stainless steel
could be related to the contribution of acid-base interac-
tions; these interactions seem to be lower in the case of
uncoated stainless steel since its electron donor was very
low in comparison with the electron donor of coated
stainless steel.
From Figure 2, we also observe that the level of S.
aureus adhesion changes as a function of contact time.
The S. aureus adhesion was much reduced at 30 min
comparatively for other times of contact. This variation is
not completely explained by physicochemical interac-
tions. However, others interactions between cell surface
and milk or milk components adsorbed on surface could
be contribute in bacterial adhesion at different contact
times. The difference in nature of proteins adsorbed for
each contact time and the faster conformational rear-

Quantitative Adhesion of Staphylococcus aureus on Stainless Steel Coated with Milk 303
rangement undergone by one protein at surface relative
to that of other proteins could be the origin of the varia-
tion observed in adhesion results. Barnes et al. (1999) [5]
have found that the pre-treatment of stainless steel with
the individual milk proteins α-, β- and
 casein and
α-lactalbumin at equal concentration reduce attachment
of S. aureus and this reduction was marked with β casein.
McEldowney and Fletcher (1987) [27] observed that hy-
drated layers of polymers and proteins that form on inert
surfaces can either facilitate or reduce bacterial adhesion.
Al Makhlafi et al. (1994) [22] examined the effect of
competitive adsorption of bovine serum albumin (BSA)
and β-lactoglobulin on Listeria monocytogenes adhesion
to silica, and they found that the film formed by the ad-
sorption of β-lactoglobulin followed by BSA encouraged
adhesion more than the film formed by the adsorption of
BSA followed by β-lactoglobulin.
4. Conclusion
The results obtained here show that the physicochemical
properties including hydrophobicity and electron donor-
electron acceptor properties of stainless steel surface were
markedly affected by treatment by milk. The adhesion
results show that whatever the contact time, the pre-
treatment of substratum by milk reduce the adhesion
level. This reduction is random with the contact time.
This research suggests that it is very important to take
into account the contact time between the substratum and
milk in the cleaning and sanitizing process.
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