International Journal of Environmental Health Research

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Efficacy of sodium dodecyl sulphate and natural

extracts against E. coli biofilm

Rok Fink, Stefan Kulaš & Martina Oder

To cite this article: Rok Fink, Stefan Kulaš & Martina Oder (2018): Efficacy of sodium dodecyl
sulphate and natural extracts against E. coli biofilm, International Journal of Environmental Health
Research, DOI: 10.1080/09603123.2018.1470230

To link to this article: https://doi.org/10.1080/09603123.2018.1470230

Published online: 02 May 2018.

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International Journal of Environmental Health Research, 2018
https://doi.org/10.1080/09603123.2018.1470230

Efficacy of sodium dodecyl sulphate and natural extracts against

E. coli biofilm
Rok Finka, Stefan Kulašb and Martina Odera
a
Faculty of Health Sciences, University of Ljubljana, Ljubljana, Slovenia; bFaculty of Pharmacy, University of Sarajevo,
Sarajevo, Bosnia and Herzegovina

ABSTRACT ARTICLE HISTORY

The aim of this study was to determine and compare the efficacy of a Received 15 March 2018
standard cleaning agent, sodium dodecyl sulphate, and natural extracts from Accepted 24 April 2018
pomegranate peel grape skin and bay laurel leaf against E. coli biofilm. The
KEYWORDS
biofilm was exposed for 10 minutes to three different concentrations of each E. coli biofilm; sodium
tested compound. The results show that bay laurel leaf extract is the most dodecyl sulphate;
efficient with 43% biofilm biomass reduction, followed by pomegranate pomegranate peel extract;
peel extract (35%); sodium dodecyl sulphate and grape skin extract each grape skin extract and bay
have 30% efficacy. Our study demonstrated that natural extracts from laurel leaf extract
selected plants have the same or even better efficacy against E. coli biofilm
removal from surfaces than the tested classical cleaning agent do. All this
indicates that natural plant extracts, which are acceptable from the health
and environment points of view, can be potential substitutes for classical
cleaning agents.

Introduction
Bacteria can occupy a wide variety of surfaces in industry and household environments (Simões et al.
2010; Azeredo et al. 2017). Under favourable conditions of nutrients, temperature, water and gasses,
bacteria on surfaces can grow into complex structures of biofilms, which are complex communities of
bacteria that are irreversibly attached to a surface and enveloped with a polysaccharide matrix (Fink
2015). It is well known that bacteria, as planktonic cells, in biofilms are much more resistant to sur-
factants and antimicrobial substances (Bridier et al. 2014; Giuliano and Rybak 2015; Williamson et al.
2017). Such biological formations are difficult to eradicate due to several adaption strategies (Myszka
and Czaczyk 2011). Therefore, biofilms represent a major risk to health, quality and cost issues related
to several industrial processes (Bohinc et al. 2015; Fink et al. 2017).
Cleaning and maintenance of hygiene at the appropriate level require the use of various cleaning
products that remove bacteria and other contaminants from surfaces. Cleaning products are mix-
tures of substances including surfactants, bases, acids, fragrances, additives and antimicrobial agents
(Cappitelli et al. 2014; Fink 2015). A typical representative of classical cleaning agent is sodium dodecyl
sulphate, which is generally used in domestic cleaning, personal hygiene, cosmetic and pharmaceutical,
as well as industrial and commercial cleaning and product formulations. The antibacterial mechanism

CONTACT  Martina Oder  martina.oder@zf.uni-lj.si

© 2018 Informa UK Limited, trading as Taylor & Francis Group
2   R. FINK ET AL.

of action is the ability of sodium dodecyl sulphate to dissolve the bacterial cell membrane and cause
structural alterations in the cell contents, and eventually cause cell lysis (Singer and Tjeerdema 1993;
Chen et al. 2015). However, some research reported that sodium dodecyl sulphate causes oxidative
stress in maritime organisms (Messina et al. 2014), reproduction effects on soil invertebrates (Gavina
et al. 2016), and even causes sensitive reactions to human skin (Richters et al. 2016).
Household cleaning products are drained to the environment, where cleaning product substances
can cause bioaccumulation and even bacterial resistance. The growing global population and improving
economies in many countries increase the consumption of cleaning products and thereby the pressure
on the environment; it is well recognized that there is an urgent need to reduce the impact per produced
unit of cleaning product to sustain human needs without compromising the basis of natural resources
(Elorriaga et al. 2013). In the previous decade, research has focused on the natural cleaning agents
that are produced from plants, are more biodegradable, efficient and have low potential of bacterial
cross-resistance (Kurinčič et al. 2016; Borges et al. 2017; Pandya et al. 2017). Several plant-derived
extracts or active compounds can prevent antibacterial activity due to the disruption of membrane
potential, inner membrane permeabilization, blebbing and the leakage of cellular contents (Saritha
et al. 2015; Tajima et al. 2016; Amin and Edris 2017; Bacon et al. 2017; Borges et al. 2017; Kwak et
al. 2017), but surprisingly little is known about their effects on complex structures such as biofilms.
Pomegranate peel (Punica granatum) is inedible part of the pomegranate fruit that is a rich source of
tannins, flavonoids, and other phenolic compounds (Li et al. 2006; Devatkal et al. 2013; Wafa et al.
2017). Grape skin (Vitis vinifera) is a great source of phenolic compounds, especially polyphenols.
The polyphenols in grape skin can penetrate the bacterial cell membrane and react with proteins
or cytoplasm (Yadav et al. 2015; Xu et al. 2017). The most abundant component found in bay laurel
(Laurus nobilis) essential oil is 1,8-cineole, also called eucalyptol (Marques et al. 2016), which has a
strong effect on the release of cell constituents both from Gram negative and positive bacteria (Zengin
and Baysal 2014).
Therefore, the aim of this research was to determine the efficacy of a classical cleaning agent (sodium
dodecyl sulphate) and natural extracts from pomegranate peel, grape skin and bay laurel leaf against
E. coli biofilm.

Methods
To assess the potential of the substitution of classical cleaning agent with natural plant extracts, E.
coli biofilm was cultivated for 48 h at 37 °C. After that, the biofilm biomass was exposed to different
concentrations of sodium dodecyl sulphate, pomegranate peel, grape skin, and laurel leaf extract for
10 min. Next, the total biofilm biomass was stained with a crystal violet assay, and the optical density
was measured at 620 nm (Figure 1). Such approach allows evaluating the potential of compounds
against biofilm that is more realistic in practice than solely antimicrobial activity on a count plate
(Azeredo et al. 2017).

Bacterial strains
In our research, standard strains of E. coli ATCC 35218, obtained from the Czech Collection of Micro-
organisms, Brno, Czech Republic were used; they were isolated from the intestinal tract of a dog. E.
coli are Gram-negative rods occurring in pairs or as single cells; they are facultative anaerobic bacteria
and a normal inhabitant of the human and animal intestinal tracts (Bohinc et al. 2014). The bacteria
can excrete toxins, polysaccharides and, most importantly for this research, they can form biofilms.
E. coli is generally used in studies as a model organism and indicator of faecal contamination and is
therefore included in probabilistic hygiene assessment (Oder et al. 2017).
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL HEALTH RESEARCH   3

Control (E. coli Sodium dodecyl Pomegranate peel Grape skin extract Laurel leaf extract
biofilm) – no rinsing sulphate extract (0.001%, 0.01%, (0.001%, 0.01%,
(48h, 37 °C) (0.001%, 0.01%, (0.001%, 0.01%, 0.1%, 10 min) 0.1%, 10 min)
0.1%, 10 min) 0.1%, 10 min)

E. coli biofilm (48h, 37 °C)

Crystal violet assay (OD 620 nm)

Figure 1. Experimental design of the efficacy assessment of sodium dodecyl sulphate and natural extract against E. coli biofilm.

Surface
Flat bottom, sterile, 18-well, polyethylene terephthalate microtiter plates were used directly for the
cultivation of the biofilms.

Cleaning agent and natural extracts

The efficacy of sodium dodecyl sulphate biofilm detachment was tested as it is anionic surfactant used
in many cleaning and hygiene products. Sodium dodecyl sulphate was obtained from Sigma-Aldrich,
United States of America.
Natural extracts of pomegranate peel, grape skin and bay laurel leaf were tested for efficacy against
E. coli biofilm. All the plants for extracts were harvested in Rijeka (Croatia). The pomegranate and
grape were at the optimum stage of ripening. After harvesting all the plants were dried at 40 °C up to
constant weight and then powdered in a grinder. All extracts were macerated for five days with 50%
ethanol. After that, the samples were filtered and poured in a round-bottomed flask and brought to
dryness in a rotary evaporator at 40 °C and 178 mbar and, finally, water extract was obtained using
distillate water (Porrini et al. 2011).

Monitoring of the biofilm levels

Biofilm formation under static conditions was quantified with a crystal violet assay. The assay was
done in 24-well plates, and the method used was well described by (Bohinc et al. 2014). Overnight
cultures were diluted in a 1:300 ratio, with a fresh medium, following which 1 mL of the newly inoc-
ulated medium was dispensed into 24-well sterile microtiter dishes. After that, the dishes were incu-
bated for 48 h at 37° C. After the incubation period, the medium was removed via an aspirator, and
cleaning agents were added. The formed biofilms were exposed to 0.1, 0.01 and 0.001% solutions of
4   R. FINK ET AL.

Figure 2. Optical density of E. coli biofilm on surface before and after exposure to different concentrations of sodium dodecyl sulphate,
pomegranate peel, grape skin, and bay laurel leaf extract.

a cleaning agent and extracts. The control was an E. coli biofilm without rinsing. All the experiments
were performed with six parallels and three repetitions. To simulate a realistic exposure time in the
cleaning procedure, the formed biofilms were exposed for 10 min at room temperature, after which
the solutions were removed (Fink et al. 2017). Bacteria left on the surface were stained with 1 mL of
a crystal violet suspension for 5 min. The excess dye was rinsed away two times with 2 mL of the PBS
(0.026 g KH2PO4, 0.047 g K2HPO4 in 1 L). The dye from the cells was remobilized with 1 ml of 96%
ethanol, and 200 μL of this solution was transferred to a 94-well microtiter plate. The optical density
of the solution was measured at a wavelength of 620 nm by the Infinite 200® PRO microplate reader
from Tecan, Austria. Alongside the crystal violet method, a light microscopy Olympus CX40 and CCD
CMOS camera was used to visualize the effects of the tested compounds at the highest concentrations
on E. coli biofilm.
Statistical analysis was run on R software version 3.1.3 (Bell Laboratories, New Jersey, U.S.) It
included ANOVA analysis of optical densities regarding the concentration of each tested compound.
The significance level was set at p < 0.05.

Results
The results of E. coli biofilm biomass removal from the surface show that sodium dodecyl sulphate
removes significant amounts of biofilm. The results also show that low concentrations remove biomass
from the surface (Figure 2(a)). Similar to that, pomegranate peel extract removes biofilm biomass
(Figure 2(b)). Results regarding the grape skin extract show that increasing the concentration of extract
results in increased biofilm removal from surfaces (Figure 2(c)). This potential is even more evident
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL HEALTH RESEARCH   5

Table 1. Results of ANOVA comparison for cleaning agent and natural extracts regarding concentration and optical density.

Compound Concentration (%) Mean OD (620 nm) p-value

Sodium dodecyl sulphate No rinsing 0.1680 ± 0.002 <0.0001
0.001 0.1156 ± 0.010
0.01 0.1222 ± 0.016
0.1 0.1167 ± 0.006
Pomegranate peel extract No rinsing 0.1680 ± 0.003 <0.0001
0.001 0.1013 ± 0.012
0.01 0.1094 ± 0.021
0.1 0.1084 ± 0.004
Grape skin extract No rinsing 0.1680 ± 0.025 <0.0001
0.001 0.1287 ± 0.019
0.01 0.1127 ± 0.017
0.1 0.1171 ± 0.015
Laurel leaf extract No rinsing 0.1680 ± 0.029 <0.0001
0.001 0.1147 ± 0.027
0.01 0.1054 ± 0.022
0.1 0.0965 ± 0.015

Control (E. coli Sodium dodecyl Pomegranate peel Grape skin extract Laurel leaf extract
biofilm) – no rinsing sulphate extract (0.1%, 10 min) (0.1%, 10 min)
(0.1%, 10 min) (0.1%, 10 min)

30% efficacy 35% efficacy 30% efficacy 43% efficacy

Figure 3. Optical microscope image of E. coli biofilm before and after exposure to 0.1% concentration of sodium dodecyl sulphate,
pomegranate peel, grape skin and bay laurel leaf extract.

in the case of bay laurel leaf extract, for which significant biofilm biomass removal can be observed
at a concentration of 0.1% (Figure 2(c)).
The results of statistical analysis show (Table 1) for all tested compounds that mean optical density is
dose-depended. By increasing the concentration, optical density is decreased. (p < 0.05). This indicates
that part of the biofilm is removed from the surface. The results also show that bay laurel leaf extract
removes the most biofilm biomass (OD = 0.0965), followed by pomegranate peel extract (OD = 0.108),
sodium dodecyl sulphate (OD = 0.116), and grape skin extract (OD = 0.117).
Results of microscope imaging show the effects of sodium dodecyl sulphate and natural extracts
on E. coli biofilm in comparison to the control (Figure 3). The figure demonstrates that bay laurel leaf
and pomegranate peel extract removes large parts of biofilm, and singular cells are left on that surface.
In contrast, when the biofilm is treated with sodium dodecyl sulphate and grape skin extract, large
particles of biomass remain on the surface.
6   R. FINK ET AL.

Discussion
Biofilm-associated bacteria are especially problematic since they can more easily withstand host
defences, antimicrobials and other stresses in comparison to planktonic cells. Biofilm-related infec-
tions are becoming a major public health issue, and the uncritical use of antimicrobials and cleaning
agents forces science to explore biofilm control strategies with lower risk to health and environment
(Tambe et al. 2001; Kurinčič et al. 2016; Borges et al. 2017). An alternative strategy is the use of nat-
ural cleaning agents, preferably derived from plants, being generally recognized as safe, not affecting
food and feed consumption nor provoking resistance, while being sufficiently effective to assure good
hygiene practice. Several plant-derived extracts can prevent the attachment of pathogens (Lebert et
al. 2007; Simões et al. 2010; Abid et al. 2014; Karygianni et al. 2016); however, from a practical point
of view, assessment should be based on testing biofilms as a worst-case scenario.
Therefore, the aim of this study was to analyse the potential of natural extracts from pomegranate
peel, grape skin and bay laurel leaf extracts to replace a classical cleaning agent, e.g. sodium dodecyl
sulphate. The results show that increasing concentrations of the classical cleaning agent and natural
extract result in statistically significant (p < 0.05) decreases of biofilm biomass. Moreover, a detailed
assessment indicates that 0.1% bay laurel leaf extract is the most efficient (43%), followed by 0.1%
pomegranate peel extract (35%), while 0.1% sodium dodecyl sulphate and 0.1% grape skin extract
show similar efficacy (30%) relative to no rinsing.
Abid et al. (2014) studied the antibacterial activity of cumin, harmal and pomegranate extract
and found that pomegranate extract has the highest impact on bacteria growth for most bacteria
isolates. In another study, Al-Obaidi et al. (2017) analysed the effectiveness of pomegranate extracts
as mouthwash and found a high percentage of antibacterial activity on a bacteria genus isolated from
patients mouths. Similar to that Al-Terehi et al. (2015) studied the potential of pomegranate peel extract
and found antimicrobial activity against several bacterial and fungi strains. Our research shows that
pomegranate peel extract has some potential for biofilm biomass removal from surfaces, since up to
35% of E. coli biofilm biomass could be removed. One reason can be that the pomegranate peel con-
tains tannins such as punicalin, ponicalagnin and granatin B, but also alkaloids such as pelletierine,
pseudo-pelletierine and methyl pelletierine Al-Terehi et al. (2015).
Some of the research found grape skin extract to have potential against many microorganisms. For
instance, a study of the antibacterial effects of polyphenols from grape skin extract showed a large
inhibition zone on bacteria and fungi, and an especially great effect was found against E. coli (Ghouila
et al. 2017). Levy et al. (2017) analysed grape seed extract and found antibacterial activity against S.
typhimurium, L. monocitogenes and E. coli. In a study by Klančnik et al. (2017), the authors tested
the anti-adhesion potential of grape skin extract and found significant potential for the reduction of
bacterial cell adhesion. We found that grape skin extract is effective in E. coli biofilm biomass removal
from surfaces. However, it is the least effective among the tested extracts; a 0.1% solution can remove
up to 30% of biomass, which is comparable to sodium dodecyl sulphate.
The results of this study show that bay laurel extract can remove up to 0.072 OD (43%) E. coli
biomass biofilm relative to the control. The potential of bay laurel extracts from the antimicrobial
viewpoint have been reviewed in some studies (García-Díez et al. 2016; Marques et al. 2016). For
example, Alejo-Armijo et al. (2017) demonstrated that procyanidins in bay laurel extract have anti-
bacterial activity, but also disrupt biofilm growth and cause cell detachment. In another study, essential
oils from bay laurel leaf show strong antibacterial activity against several bacterial cells, among also E.
coli (Dadalioǧlu and Evrendilek 2004). In one study Merghni et al. (2016) analysed the antibacterial
and anti-biofilm potentials of bay laurel leaf extract and revealed that essential oils have an excellent
antibiofilm activity with eradication between 80 and 95%. Chmit et al. (2014) studied bay laurel leaf
extract on S. epidermidis biofilm and found biomass reduction up to 35% with regard to the biomass
amount before treatment.
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL HEALTH RESEARCH   7

Conclusions
Biofilms are a major public health issue, as more and more bacteria are becoming resistant to antimi-
crobials and because the consumption of compounds for bacteria control is increasing exponentially.
One possibility is to substitute classical cleaning and antimicrobial agents with natural extracts that
have low cross-resistance potential and are generally recognized as safe. The results of this study show
the great potential some plant extracts, e.g. bay laurel leaf extract that removes about 43% of total
E. coli biofilm biomass at 0.1% solution. In comparison, a 0.1% solution of sodium dodecyl sulphate
removes a mere 30% of total biofilm biomass. In the foreseeable future, biofilm control strategies will
face challenges in effectively eradicating biofilm formations from surfaces, while simultaneously pro-
viding approaches with low impacts on human health, the environment and cross-resistance potential.

Acknowledgement
The authors would like to express their gratitude to Prof Ibrahim Mujić for providing the natural extracts.

Disclosure statement
No potential conflict of interest was reported by the authors.

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