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FOOD

MICROBIOLOGY

Food Microbiology 25 (2008) 471478

Potential of a nisin-containing bacterial cellulose film to inhibit

Listeria monocytogenes on processed meats

V.T. Nguyena, M.J. Gidleyb, G.A. Dykesc,

aSchool of Land and Food Sciences, University of Queensland, St. Lucia, Qld., AustraliabCentre for Nutrition and Food Sciences, University of Queensland, St. Lucia, Qld., Australia

cFood Science Australia, Brisbane, Qld., Australia

Received 27 September 2007; received in revised form 15 January 2008; accepted 16 January 2008

Available online 29 January 2008

Abstract

A bacterially produced cellulose film containing nisin was developed and used in a proof-of-concept study to control Listeria

monocytogenes and total aerobic bacteria on the surface of vacuum-packaged frankfurters. Bacterial cellulose pellicles were produced by

Gluconacetobacter xylinus K3 in Corn Steep Liquor-Mannitol Medium and were subsequently purified before nisin was incorporated

into them. Investigations into the effect of nisin concentrations and contact times on incorporation of nisin into cellulose films showed

that the lowest nisin concentration and shortest time needed for production of an effective antimicrobial cellulose film were 625 IU ml1

and 6 h, respectively. The active cellulose films produced under these conditions did not, however, significantly reduce L. monocytogenes

populations on frankfurters (P40.05) during refrigerated storage for 14 days as compared to the controls. Films produced using a higher

concentration of nisin (2500 IU ml1) with the same exposure time (6 h) resulted in a significant (Po0.05) decrease in L. monocytogenes

counts on frankfurters of$2logCFUg1 after 14 days of storage as compared to the control. Both the above-mentioned films showed a

similar effectiveness in reducing total aerobic bacterial populations as measured by total aerobic plate counts on frankfurters. For both

films, total aerobic bacterial levels were significantly (P40.05) reduced by $3.3logCFUg1 after 14 days of storage as compared to

control samples. Bacterial cellulose films were demonstrated in this study to have potential applicability as antimicrobial packaging filmsor inserts for processed meat products.

r 2008 Elsevier Ltd. All rights reserved.

Keywords: Antimicrobial packaging; Bacterial cellulose; Nisin; Listeria monocytogenes

1. Introduction

Listeria monocytogenes causes foodborne listeriosis, a

disease that occurs largely in pregnant woman and the

elderly leading to illness, miscarriages and death. Listeria

contamination has also been responsible for the recall ofmillions of kilograms of food product and substantial

economic loss to industry worldwide. The ability of

L. monocytogenes to grow at low temperature makes it

difficult to control this microorganism in food products by

refrigeration alone (Franklin et al., 2004).

One method used to control L. monocytogenes in food is

through the use of antimicrobial compounds such as nisin,

which is a polypeptide produced by some strains of the

lactic acid bacterium Lactococcus lactis subsp. lactis (Lou

and Yousef, 1999). This compound has been approved for

use as a food preservative by the Joint FAO/WHO Expert

Committee on Food Additives and granted Generally

Recognized As Safe (GRAS) status for use in cheeseproducts in the USA (Hurst, 1983). Direct addition of nisin

to food surfaces may lead to some loss of its activity,

because it migrates towards the center of the food which

can result in an associated dilution and depletion of its

effect (Quintavalla and Vicini, 2002; Han, 2003). In

addition, antimicrobial agents such as nisin may be

inactivated by some components of the food they are

present in (Rose et al., 1999).

Active packaging, which may be defined as packaging

which performs some role other than that of a barrier to

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www.elsevier.com/locate/fm

0740-0020/$ - see front matterr 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.fm.2008.01.004

Corresponding author. Tel.: +61 7 32142037, fax: +61 7 32142050.

E-mail address: gary.dykes@csiro.au (G.A. Dykes).

http://www.elsevier.com/locate/fmhttp://localhost/var/www/apps/conversion/current/tmp/scratch696/dx.doi.org/10.1016/j.fm.2008.01.004mailto:gary.dykes@csiro.aumailto:gary.dykes@csiro.auhttp://localhost/var/www/apps/conversion/current/tmp/scratch696/dx.doi.org/10.1016/j.fm.2008.01.004http://www.elsevier.com/locate/fm

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the outside environment, is of increasing interest to food

producers (Vermeiren et al., 1999). In the case of foods,

active packaging generally either acts to increase or

indicate the shelf life or safety of products (de Kruijf

et al., 2002). Oxygen and ethylene scavengers, moisture

removers and taint removers are all used in active

packaging systems for food (Vermeiren et al., 1999; deKruijf et al., 2002). It has been widely suggested that

antimicrobial agents could also be incorporated into food

packaging films to create an active packaging system which

will maintain their activity during food storage. Controlled

release of such agents from packaging films could inhibit

the growth of target microorganisms over time and thus

extend the shelf life of packaged products (Quintavalla and

Vicini, 2002). Among available packaging materials,

cellulose-based products have attracted increasing interest

due to their edibility, biodegradability and potential as a

good carrier of a wide range of antimicrobial agents (Cagri

et al., 2004). Studies describing the incorporation of nisin

into non-bacterial cellulose-based packaging films to create

antimicrobial materials have been reported. The films

developed in these studies have been used to inhibit

L. monocytogenes on the surface of frankfurters (Luchans-

ky and Call, 2004) and reduce Listeria innocua and

Staphylococcus aureus on cheese and processed ham

(Scannell et al., 2000). In all these cases, cellulose was

obtained as a commercially available product of plant

origin and formed into films or inserts in the laboratory.

Cellulose may also be produced by bacteria as well as

by plants and other organisms. Bacterial cellulose can be

produced in relatively large amounts by microbial fermen-

tation of various substrates by Gluconacetobacter xylinusstrains. In static culture, bacterial cellulose is synthesized

in the form of pellicle on the top of the growth media

which may act as ready-made films or inserts for

application in foods. Bacterial cellulose membranes have

unique characteristics compared to other sources of

cellulose, such as high purity, high crystallinity, high

tensile strength and high water holding capacity, and

therefore show good potential for a variety of applications

(Iguchi et al., 2000). Bacterial cellulose has been used

commercially to produce, for example, acoustic transducer

diaphragms and artificial skin (Jonas and Farah, 1998).

The use of bacterial cellulose has, however, not been

reported with respect to the development of active

packaging for food applications.

Currently, the cost of the production of bacterial

cellulose means it is only practical for high-value products;

however, the potential exists to grow bacterial cellulose

films on waste streams in-house in food processing

facilities. Such a system might make its use far more

cost-effective. Furthermore, the unique absorption proper-

ties and the purity of bacterial cellulose may make it either

particularly useful for foods or desirable because of its

esthetics for use in high-value food products. We therefore

undertook a proof-of-concept study to develop and apply

bacterial cellulose films containing nisin to control

L. monocytogenes and other bacteria on the surface of

frankfurters as models for higher value meat products.

2. Materials and methods

2.1. Bacterial strains and culture media

L. monocytogenes Scott A serotype 4b (Department of

Health and Human Services, Food and Drug Administra-

tion, Cincinnati, USA) and G. xylinus K3 (School of Land

and Food Sciences, University of Queensland, Brisbane,

Australia) were used in this study. They were maintained at

80 1C on Protect Bacterial Preservers (Technical Service

Consultants, Heywood, UK). L. monocytogenes Scott A

serotype 4b was resuscitated by incubation on Tryptone

Soya Agar (TSA; Oxoid, Basingstoke, UK) at 30 1C for

24 h, while G. xylinus K3 was resuscitated by incubation on

Yeast Extract Peptone Mannitol Agar (YPM; 25 g l1

mannitol, 5 g l1

yeast extract, 3 g l1

peptone and 15 g l1

agar) at 301C for 48 h. Working cultures of L. mono-

cytogenes and G. xylinus were prepared by subculturing

onto TSA and YPM, respectively. The medium used

for cellulose production was Corn Steep Liquor (CSL)-

Mannitol Medium (20 g l1 mannitol, 40g l1 CSL,

2.7gl1 Na2HPO4, 1.15gl1 citric acid H2O). Prior to

sterilization at 121 1C, the pH value of the medium was

adjusted to 5.0.

2.2. Nisin solution preparation

Nisin powder (2.5% pure nisin in denaturized milksolids) was purchased from Sigma-Aldrich (Gillingham,

Dorset, UK). A nisin solution of 50,000IU ml1 was

prepared by dissolving 0.5 g of nisin in 10 ml of 0.01 M

HCl. The suspension was then centrifuged at 3000 g for

15min in a sterile 15-ml centrifuge tube to remove

insoluble whey proteins. The supernatant was filtered and

stored as a stock solution at 4 1C (Komitopoulou et al.,

1999). This solution was diluted with 0.01 M HCl to obtain

a nisin solution of 10,000 IU ml1, which was used as a

working solution in this study unless otherwise stated.

The minimum inhibitory concentration (MIC) of nisin

was determined by the method of Turner et al. (2004).

Briefly, an overnight culture of L. monocytogenes in

Tryptone Soya Broth (TSB; Oxoid) was adjusted to an

optical density of 1 at 600 nm using a spectrophotometer

(Varian Techtron Pty. Ltd., Mulgrave, Australia). A 1-ml

aliquot of this culture was aseptically distributed into 1.5-

ml sterile tubes (Eppendorf, Sarstedt, Germany). Each tube

was supplemented with 100 ml of a serial two-fold dilution

of nisin solution and the optical density was measured at

600 nm. All the mixtures were incubated in 30 1C for 24 h

and the OD600 of each culture was measured again. The

MIC of nisin against L. monocytogenes Scott A was

calculated as the concentration in lowest dilution yielding

no change in OD600.

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and 251C for TPC, and the number of bacteria was

expressed as CFU ml1.

2.8. Statistical analysis

All quantitative data, unless otherwise stated, are

presented as the means of triplicates with error representedby standard deviation. Significant differences between

bacterial numbers of controls and treated samples were

determined by the ANOVA procedure using Minitab

(Minitab 14; Minitab Inc., Minneapolis, USA) at the 5%

level.

3. Results

3.1. Incorporation of nisin into cellulose films

The antibacterial activity of the crude cellulose films

containing nisin produced in this study against L.

monocytogenes on TSA plates can be seen in Fig. 1a. It is

apparent that the bacterial cellulose itself has no anti-

microbial activity as no zone of inhibition is observed for

the control samples (Fig. 1b).

The degree of inhibition ofL. monocytogenes Scott A by

dilutions of nisin was used to determine the MIC as

312IUml1, which was the lowest dilution resulting in the

complete inhibition of L. monocytogenes.

Cellulose films were exposed to nisin solutions ranging

from 10,000 to 156.3 IU ml1 in a two-fold dilution series

for 12 h. The highest nisin concentration was that based on

the maximum allowable amount of nisin (10 mg g1) in

cheese in the USA. The lowest nisin concentration of156.3 IU ml1 was based on the MIC identified from the

previous experiment. The diffusion assay showed that there

was no inhibition zone around cellulose films containing

nisin from solutions of concentration lower than

625IUml1, indicating that this concentration is the lowest

needed to create active cellulose films. It was also apparent

that a greater concentration of nisin used resulted in an

increase in antimicrobial activity of cellulose films, as

indicated by the area of the associated inhibition zone

(Fig. 2).

In order to investigate the effect of contact time with

nisin solutions on antimicrobial activity of active cellulose

films, a solution of 625 IU ml1 was used with cellulose

films for different periods of time. The results showed that

there was no inhibition zone around cellulose films exposed

to nisin for less than 6 h, while an incorporation time of

more than 6 h resulted in no significant (P40.05) change inthe diameter of the zone (Fig. 3). It was therefore apparent

that 6 h was the shortest period of exposure needed for the

production of active bacterial cellulose films.

In this study, we also found that there was no change in

the concentration of nisin in the solution during exposure

to cellulose. The volume of the nisin solutions, on the other

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Zone of clearing No clearing

Fig. 1. Antimicrobial activity of cellulose films against Listeria monocytogenes Scott A on TSA plates. (a) Cellulose film exposed to a nisin solution of

10,000 IU ml1. (b) Control film prepared without the presence of nisin.

20

21

22

23

24

25

26

27

156.3 312.5 625 1250 2500 5000 10000

Nisin concentration (IU ml-1)

Diameterofzoneofinhibition(mm)

Fig. 2. Antimicrobial activity of active cellulose films exposed to seven

nisin concentrations for 12 h against Listeria monocytogenes Scott A on

TSA plates. Activity of films is expressed as diameter of the inhibition

zone including cellulose films (+22mm). Error bar represents the

standard deviation for triplicate experiments.

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hand, decreased after exposure to cellulose films which

were also observed to expand. The volume of nisin solutionabsorbed by cellulose continued to increase during

exposure for up to 8 h but remained constant after this

time period until the experiment was terminated (Fig. 4).

3.2. Inhibition of bacteria on frankfurters by active bacterial

cellulose films

Active bacterial cellulose films for frankfurter packaging

were prepared with exposure to 625 IU ml1 nisin for 6 h. It

was observed that there was no increase in the

L. monocytogenes population in control samples over the

storage period of 14 days (Fig. 5). Frankfurters packaged

with cellulose films containing nisin showed a slight

decrease of $1logCFUg1 of L. monocytogenes after

day 8, but were not significantly different from control

sample counts at the end of the storage period. In order to

enhance antimicrobial activity, active bacterial cellulose

films exposed to a nisin solution at a higher concentration

(2500 IU ml1) for 6 h were prepared. It was found that the

number of L. monocytogenes decreased sharply by

$2logCFUg1 after 2 days of storage in samples covered

by these films and then remained constant until the end of

experiment.

A TPC was also determined to assess the potential

implication of active bacterial cellulose films in extending

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20

21

22

23

24

0 2 4 6 8 10 12

Time (h)

Diameterofzoneofinhibition(m

m)

Fig. 3. Antimicrobial activity of active cellulose films exposed to

625 IUml1 nisin for seven time periods against Listeria monocytogenes

Scott A on TSA plates. Activity of films is expressed as diameter of the

inhibition zone including cellulose films (+22 mm). Error bar represents

the standard deviation for triplicate experiments.

0.00

0.10

0.20

0.30

0.40

0.50

0.60

0 2 4 6 8 10 12

Time (h)

Absorbedvolumeofnisin(ml)

Fig. 4. Volume of nisin solutions absorbed by bacterial cellulose films

exposed for seven time periods. Error bar represents the standard

deviation for triplicate experiments.

0

1

2

3

4

5

6

7

8

9

10

0 2 4 6 8 10 12 14

Time (days)

L.monocytogenesCount(log10CFU

g-1)

Fig. 5. Numbers of Listeria monocytogenes Scott A on frankfurters

packed with active cellulose films exposed to nisin solutions at 625 IU ml1

(m) and 2500 IUml1 (K), or with no exposure to nisin (n) and with no

cellulose film (J) during storage over 14 days at 4 1C. Error bar represents

the standard deviation for triplicate experiments.

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the shelf life of processed meats. The initial TPC was

$6.3 log CFU g1 and increased continuously during 14

days of storage in control samples to $9.7 log CFU g1

(Fig. 6). The rate of increase in TPC was more rapid for the

control with cellulose film not containing nisin than for the

control without cellulose film, although final numbers after

14 days were approximately the same for both controls. By

contrast, frankfurters packaged with cellulose films ex-

posed to nisin solutions containing 625 and 2500 IU ml1

nisin showed an immediate and significant (Po0.05)

reduction in TPC of $0.8 and $1.5 log CFU g1, respec-

tively, which lasted until day 6 of the storage trial.

Although there was a gradual increase of TPC after day

6, the final counts on frankfurters with both levels of nisin

were significantly (Po0.05) lower by $3.4 log CFU g1 as

compared to that of controls.

4. Discussion

Previous studies have shown that nisin may be efficiently

incorporated into cellulose-based packaging films and used

for controlling pathogens in food products (Ming et al.,

1997; Scannell et al., 2000; Franklin et al., 2004; Luchansky

and Call, 2004). Our study is the first, however, to

demonstrate that self-assembled cellulose films of bacterial

origin may also be developed and used in this capacity.

We initially established that cellulose films absorbed

nisin solutions and expanded during the incorporation

process and that the cellulose acted largely as a sponge.

The sudden step change in zone of inhibition after 6 h

contact time with nisin solution (Fig. 3) may be linked

to the results of the volume of nisin absorbed (Fig. 4).

It can be seen that expansion of the cellulose and asso-

ciated absorption of nisin solution was a relatively

slow process which reached its maximum after 68 h. Itseems that this volume of nisin solution was required to

produce an antimicrobial effect. Nisin did not physically

bind to the cellulose, as the nisin concentration did not

change after exposure to films. In a previous study,

Scannell et al. (2000) reported that nisin bound well onto

cellulose-based inserts. The purity and compositions of the

inserts in this study were not reported and binding could

have been due to absorption of nisin to other components

in the inserts. Bacterial cellulose is known to have a higher

purity than cellulose from other sources (Iguchi et al.,

2000) and the cellulose films used in our study were

established to be free of other polymers by NMR spectro-

scopy (data not shown).

Prior to investigating the effect of active bacterial

cellulose film against bacteria on food products, we

established the effect of nisin concentration and contact

time on incorporation of nisin into bacterial cellulose. This

work was done with an aim of determining the optimum

conditions for the production of active cellulose films. In

order to reduce the number of experiments, the MIC of

nisin against L. monocytogenes Scott A on TSA was

determined. Although the MIC of nisin against Listeria

spp. is well established, this value was found to be different

depending on the specific strain and the culture medium

(Benkerroum and Sandine, 1988). The MIC was similar tothat reported for nisin against L. monocytogenes ATCC

15313 on TSA (Grower et al., 2004), but was different, for

example, from those reported by Singh et al. (2001), who

found there was a considerable variation in MIC of nisin

from 6 to 200IU ml1 for six strains of L. monocytogenes.

The antimicrobial activity of bacterial cellulose films was

shown to be proportional to the concentration of the nisin

solution used and the minimum nisin level for effective film

in vitro was established as 625 IU ml1. Establishing the

lower level of nisin necessary for activity aimed to reduce

the amount of this antimicrobial required and so produce a

more cost-effective active film.

Although nisin-containing cellulose films were effective

against L. monocytogenes on TSA, they were not effective

in controlling this pathogen on the surface of frankfurters

at 625IUml1. This may be attributed to the extrinsic

environmental conditions of food affecting the activity of

nisin and the behavior of L. monocytogenes (Han, 2003).

Previous studies have also shown that nisin displays a

greater antimicrobial activity against L. monocytogenes in

synthetic media than in foods because some components of

food can reduce the efficacy of this compound (Delves-

Broughton et al., 1996; Rose et al., 1999). In order to

obtain a greater antimicrobial effect against L. monocyto-

genes on frankfurters, a higher level (2500 IU ml

1) of nisin

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0

1

2

3

4

5

6

7

8

9

10

0 2 4 6 8 10 12 14

Time (days)

TotalAerobicPlateCount(log10

CFU

g-1)

Fig. 6. Numbers of total aerobic bacteria on frankfurters packed with

active cellulose films exposed to nisin solutions at 625IU ml1 (m) and

2500IUml1 (K), or with no exposure to nisin (n) and with no cellulose

film (J) during storage over 14 days at 4 1C. Error bar represents the

standard deviation for triplicate experiments.

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was incorporated into the film which was an approach that

had been used in other studies (Luchansky and Call, 2004;

Delves-Broughton, 2005). The film with the higher nisin

concentration gave encouraging results by sharply reducing

L. monocytogenes counts on frankfurters. Our study

showed some similarities to that of Franklin et al. (2004),

who demonstrated that packaging films containing156IUml1 were not as effective as films containing

2500IU ml1 in controlling L. monocytogenes on the

surface of hot dogs.

The cellulose films prepared with both 625 and

2500IU ml1 nisin were effective in reducing the TPC on

the surface of frankfurters, indicating that the use of nisin-

containing bacterial cellulose films might result in an

extension of the microbiological shelf life of frankfurters.

These results agreed with those of Scannell et al. (2000)

who used active cellulose-based inserts to control the TPC

in ham during 2 weeks of storage when packaged under a

modified atmosphere. An increase in TPC in frankfurters

packaged with active cellulose films from day 6 may cause

some concern. This phenomenon may be associated with

the early release of nisin molecules from cellulose films

which may reduce the concentration of nisin on the surface

of films to a level below the MIC. The release rate of

preservative agents has been considered an important

factor affecting the storage time of food products in

previous studies. It has been suggested that in order to

increase the shelf life of food products, it is important to

control the release of the agent to maintain the concentra-

tion of active compound above the MIC over the storage

period (Han, 2005). Further work is required to control the

release of nisin from cellulose films before they could beapplied commercially. The more rapid rate of increase in

TPC for the control with cellulose film not containing

nisin, as compared to the control without cellulose film, is

noteworthy. This feature may be attributed to the hydrated

cellulose film providing a better microenvironment for

bacterial growth than the surface without cellulose in the

absence of nisin.

In conclusion, our study demonstrates that it is feasible

to develop self-assembled bacterial cellulose films into

active packaging materials by the incorporation of nisin.

Nisin-containing bacterial cellulose films showed effective-

ness in controlling L. monocytogenes and reducing TPC

on the surface of frankfurters, indicating that the use of

active bacterial cellulose films would be a promising

method to enhance the safety and extend the shelf life of

processed meats. The absence of a readily available system

for the commercial production of bacterial cellulose and

the high price of nisin may hinder application of this

approach in practice. However, as indicated in Section 1,

the potential exits to produce the cellulose in-house from

waste streams. Furthermore, the unique properties of

bacterial cellulose may allow the more efficient absorption

of nisin under the right conditions, thus reducing the

cost of raw material. It would also be expected that

this system would be used with higher value meat products

than frankfurters and may be perceived as more natural

or novel by consumers giving a market advantage.

Substantial work is still required, however, to make the

production of active bacterial cellulose films economically

feasible.

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