Microbial antagonists to food-borne pathogens and biocontrol

Available online at www.sciencedirect.com

Microbial antagonists to food-borne pathogens and biocontrolAntonio Galvez, Hikmate Abriouel, Nabil Benomar and Rosario Lucas

Application of natural antimicrobial substances (such as

bacteriocins) combined with novel technologies provides new

opportunities for the control of pathogenic bacteria, improving

food safety and quality. Bacteriocin-activated films and/or in

combination with food processing technologies (high-

hydrostatic pressure, high-pressure homogenization, in-

package pasteurization, food irradiation, pulsed electric fields,

or pulsed light) may increase microbial inactivation and avoid

food cross-contamination. Bacteriocin variants developed by

genetic engineering and novel bacteriocins with broader

inhibitory spectra offer new biotechnological opportunities. In-

farm application of bacteriocins, bacterial protective cultures,

or bacteriophages, can decrease the incidence of food-borne

pathogens in livestock, animal products and fresh produce

items, reducing the risks for transmission through the food

chain. Biocontrol of fungi, parasitic protozoa and viruses is still

a pending issue.

Address

Area de Microbiologıa, Departamento de Ciencias de la Salud, Facultad

de Ciencias Experimentales, Universidad de Jaen, 23071 Jaen, Spain

Corresponding author: Galvez, Antonio ([email protected])

Current Opinion in Biotechnology 2010, 21:142–148

This review comes from a themed issue on

Food biotechnology

Edited by Dietrich Knorr and Carmen Wacher

Available online 9th February 2010

0958-1669/$ – see front matter

# 2010 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2010.01.005

IntroductionMicrobes elicit a variety of mechanisms that facilitate

colonization and prevalence in ecological niches. These

include adherence, competition for available nutrients,

production of toxic metabolites, and secretion of dedi-

cated antimicrobial substances such as antibiotics and

bacteriocins. The wise exploitation of these mechanisms

of microbial interference can be beneficial to human and

animal health, and economy. The transmission of food-

borne pathogens through the food chain is still an unre-

solved issue. The globalization of the food market, and

the new trends in food production and distribution,

together with changes in consumer habits and population

susceptibility (such as the elderly or immuno-comprom-

ised people) are always pointed as the main contributing

factors. In addition, the substantial economic losses


because of spoilage of raw materials or processed products

and the costly recalls because of microbial contamination

are matters of concern in a world that periodically faces

economic crisis and increasingly suffers from population

overgrowth, malnutrition and overexploitation of natural

resources. In developing countries, the incidence of ill-

nesses caused by food-borne pathogens in the younger

people has also a clear influence in malnutrition, which in

turn has a negative impact on health status and cognitive

potential.

Among the wide array of strategies being currently used

or proposed for food preservation, control strategies based

on living organisms and/or their antimicrobial products

(biocontrol, or biopreservation) have been used since

ancient times (such as in food fermentation) and are

becoming increasingly popular for several reasons: firstly,

natural preservation methods are regarded as health-

friendly by consumers, and are expected to have a lower

impact on the food nutritional and sensory properties (as

opposed to chemical or physico-chemical treatments);

secondly, they may decrease the processing costs while

at the same time extending the product shelf life period,

do not require advanced technological equipment or skills

and therefore can be exploited by smaller economies;

thirdly, may offer new opportunities to solve emerging

issues such as the increase of antibiotic resistance in the

food chain, the need to improve animal productivity by

natural means, or the control of emerging pathogens.

Microbial cell factories for biocontrolMicrobes may produce a wide spectrum of antimicrobial

substances. Most studies have focused on antimicrobials

produced by lactic acid bacteria (LAB) and associated

bacteria such as the propionic acid bacteria and the

bifidobacteria. The decreased pH value and antibacterial

activities of organic acids produced by LAB are the main

mechanisms for biopreservation of fermented foods.

Specific strains of LAB may also produce other inhibitory

substances (such as diacetyl, reuterin, reutericyclin), anti-

fungal compounds (such as propionate, phenyl-lactate,

hydroxyphenyl-lactate, cyclic dipeptides, and 3-hydroxy

fatty acids), bacteriocins and bacteriocin-like inhibitory

substances (BLIS), which can be exploited against food-

borne pathogens and spoilage bacteria (Figure 1). LAB

bacteriocins can be grouped in different classes, such as

the lantibiotics, the Class II bacteriocins and subclasses,

or the circular bacteriocins [1��]. Nisin is the paradigm of

lantibiotic bacteriocins, and is licensed as a food preser-

vative. The pediocin AcH/PA-1 is also available as a

commercial preparation, while other bacteriocins such

as lacticin 3147 or the cyclic peptide enterocin AS-48

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http://dx.doi.org/10.1016/j.copbio.2010.01.005

Microbial antagonists and biocontrol Galvez et al. 143

Figure 1

Biocontrol of pathogenic bacteria through the food chain using microbial antagonistic bacteria and/or their antimicrobial products. Antagonistic strains

can be applied: (1) as living cultures on livestock and fresh produce; (2) as protective cultures on ready-to-eat food products; (3) as starter or protective

cultures in fermented foods. They are expected to grow and produce antimicrobial substances in situ, displacing unwanted bacteria. Alternatively,

food-grade preparations containing antimicrobials produced at industrial scale by antagonistic strains can be applied as biopreservatives or as food

additives to inhibit transmission of food-borne and/or spoilage bacteria through the food chain (1–4). Since the food microbiota may change

considerably from farm to fork, biocontrol strategies must be designed specifically for each type or category of food product.

can be produced on cheap by-products from the dairy

industry in the form of lyophilized powders amenable for

commercial exploitation [2]. Bacteriocins offer a wide

spectrum of potential applications against pathogenic

and spoilage bacteria in foods [3��].

One of the main limitations of many bacteriocins is their

narrow antibacterial activity. Genetic engineering inves-

tigation led to the discovery of nisin derivatives with

increased activity against Gram-positive pathogens in-

cluding Listeria monocytogenes and/or Staphylococcus aureus[4�]. This major step forward in the bioengineering of

nisin may open new possibilities to modify the spectrum

and specific activity of other lantibiotics. Although most

bacteriocins are only active on Gram-positive bacteria,

some LAB bacteriocins described recently are active on

Gram-negative bacteria of concern in foods [5�,6�,7�,8�].Although there are very scarce or no reports yet on their

efficacy in food systems, they may provide novel tools to

control food-borne pathogens.

Bacteriocins from non-LAB bacteria, such as variacin

(from Kocuria varians), cerein 8A (from Bacillus cereus)or the colicins and microcins are also being investigated

for food biopreservation [3��,9�,10]. Microcins are inter-

esting small peptides for the inhibition of Gram-negative

bacteria. Microcin J25 (MccJ25) is active against Salmo-


nella spp., Shigella spp., and Escherichia coli O157:H7.

Since MccJ25 is highly resistant to digestive proteases

and could affect the normal gastrointestinal microbiota

when ingested with foods, a chymotrypsin-susceptible

MccJ25 variant has been developed recently, which may

be used as a food preservative against the Gram-negative

pathogens [11�].

Biocontrol of Gram-positive bacteria in foodsL. monocytogenes

Among the Gram-positive bacteria, L. monocytogenes is

considered the food-borne pathogen of greatest concern

owing to its capacity to survive and grow in a wide variety

of food substrates and environmental conditions, in-

cluding refrigeration. Many studies have investigated

the effects of bacteriocins and bacteriocin-producing

strains on L. monocytogenes in different food systems and

in combination with different physico-chemical hurdles

[3��], although the efficacy of lantibiotics and Class IIa

bacteriocins against this food-borne pathogen is com-

promised by the emergence of bacteriocin resistant

strains and the cross-resistance observed between bacter-

iocins [12,13�]. Among the different approaches tested,

surface application of bacteriocins (by dipping, washing,

or film immobilization) alone or in combination with other

hurdles or treatments is gaining attention to decrease the

levels of listeria and avoid cross-contamination in raw as


144 Food biotechnology

well as processed foods such as sprouts, fruits, liquid

foods, ready-to-eat meat products such as ham and sau-

sages, cheeses, and fish products such as smoked salmon

[3��,14–21]. Novel food processing technologies such as

pulsed electric fields (PEF) [22], high-hydrostatic pres-

sure (HHP) [17], high-pressure homogenization [23�], in-

package pasteurization [24], pulsed light [21], or ionizing

radiation [20] could be used in combination with bacter-

iocins as effective antilisterial steps in the production of

ready-to-eat foods and drinks.

Selected LAB protective cultures can control L. mono-cytogenes in foods [3��,25–28]. These can be applied

either by surface inoculation or mixed with the food,

and produce antilisterial substances during storage,

fermentation or ripening. Understanding the microbial

ecology of food-borne pathogens is crucial to control

their transmission. L. monocytogenes can survive attached

to biofilms in food processing plants. Protective

culture bacteria with antilisteria activity could find

application in the control of Listeria biofilms in places

refractile to cleaning and disinfection, such as floor

drains [29�].

Other Gram-positive bacteriaBiocontrol of staphylococci has focused considerably on

the prevention and treatment of mastitis and improve-

ment of animal health. In food systems (such as sauces,

desserts, meat or milk) addition of bacteriocins alone or in

combined treatments causes a variable degree of inacti-

vation of S. aureus [30–32]. Microbial inactivation of

staphylococci in milk increases remarkably with com-

bined treatments by PEF and antimicrobial peptides

(such as nisin, enterocin AS-48, lysozyme, or combi-

nations of these) [33]. In fermented sausages, survival

of S. aureus decreases after the addition of nisin or

inoculation with bacteriocinogenic strains [34,35].

Although staphylococci are much more resistant than

L. monocytogenes to bacteriocin treatments, different bio-

control approaches are now available to inhibit prolifer-

ation and staphylococcal toxin production in foods.

Inactivation of spores from food poisoning bacteria

(mostly B. cereus and Clostridium botulinum) is still a

concern in the food industry. Many bacteriocins have

shown antimicrobial activity against endospore-forming

bacterial cells and germinating spores in food systems, as

exemplified by nisin [3��]. Promising results have been

reported recently for combined treatments (such as

HHP, nisin, or moderate heat) on the inactivation of

C. botulinum and B. cereus spores [36,37�]. Such combined

treatments could improve food safety and decrease the

impact of the intense heat treatments required for endo-

spore inactivation. In addition, the residual bacteriocin in

the finished product affords natural protection against

bacterial growth and toxin production during the product

shelf life.


Biocontrol of Gram-negative bacteria in foodsOne of the main concerns in food safety is the trans-

mission of pathogenic enterobacteriaceae, because of

their high incidence in food-borne illness and the emer-

gence of new virulent serotypes and transmission routes.

Outbreaks related to the consumption of fresh produce

have been increasingly reported. Pathogenic bacteria may

contaminate fresh produce from dust, animal excreta,

manure, irrigation water, cross-contamination from pro-

cessing wash or postharvest handling. Adhesion of human

pathogenic bacteria to leaf surfaces and invasion of the

inner leaf tissue have been documented, decreasing the

efficacy of decontamination treatments [38�]. Tissue

damage may enhance the growth of human pathogens

on produce [39�]. Control of food-borne pathogens in

fresh produce is difficult as a result of the limited treat-

ments that can be applied without compromising the

food’s organoleptic properties and shelf life.

LAB bacteriocins could be applied for the inactivation of

Gram-negative pathogens in foods in combination with

other hurdles or treatments to induce cell damage and

partial disorganization of the outer cell membrane pro-

tective layer [3��]. Application of bacteriocins in combi-

nation with other antimicrobials such as sanitation or

washing treatments can reduce the microbial load on

fresh produce and inactivate Gram-negative bacteria (in-

cluding S. enterica, E. coli O157:H7, Shigella spp., Enter-obacter aerogenes, Yersinia enterocolitica, Aeromonashydrophila and Pseudomonas fluorescens) [40�]. Such treat-

ments can also decrease the risk for transmission of

pathogenic bacteria from fruit surfaces to sliced fruits

during processing [3��]. Biocontrol based on bacterio-

phages or protective LAB cultures has also been proposed

[41�,42], although the efficacy of such treatments greatly

depends on ecological factors such as phage specificity

and inactivation, or the capacity to grow and produce

antimicrobials in situ by the protective cultures.

Microbial inactivation of E. coli and S. enterica in fruit

juices can be enhanced with treatments based on various

types of bacteriocin combinations (with organic acids,

chelators, lysozyme, PEF, high-pressure homogenization,

or HHP) [22,23�,43�,44,45]. These mild treatments allow

a better preservation of nutrients and organoleptic proper-

ties of the juices compared to thermal treatments.

In foods of animal origin such as meat and poultry

products, bacteriocins have been tested for carcass decon-

tamination by washing or spraying, with varying degrees

of success [3��]. Spray intervention with colicin E1 pro-

vides a strong reduction of E. coli O157:H7 on beef

carcasses under refrigeration, although high bacteriocin

concentrations are required [9�]. In meat and poultry

products, application of bacteriocins (like nisin, pediocin,

or enterocins A, B and AS-48) in film coatings or in

combination with HHP can reduce the growth and



survival of Salmonella [19,30,32,46,47] and E. coliO157:H7 [16,19]. Application of bacteriophage mixtures

dramatically reduces the levels of enterobacteria (such as

Salmonella Typhimurium and Campylobacter jejuni) on

meats [48�]. Reducing the concentrations of enterobac-

teria in foods decreases the risks of human infection

through food consumption. Nevertheless, incomplete

inactivation of microbial populations may increase

the risks for the selection of resistant or adapted strains.

This phenomenon has not yet been studied in depth on

Gram-negatives.

Cronobacter (Enterobacter) sakazakii is an emerging

pathogen of concern in infant formula. C. sakazakii can

be inhibited under laboratory conditions by antimicrobial

peptides (lactoferrin, nisin, and nisin combination with

diacetyl) [49] but not in reconstituted infant formula [50].

Therefore, it is necessary to investigate other antimicro-

bial treatments against this bacterium in infant foods. In

ethnic cereal foods, survival of the surrogate E. aerogenesas well as other Gram-negative bacteria decreases after

fermentation with LAB strains producing BLIS [51].

Since much ethnic fermented gruel is consumed as infant

weaning foods as well as by elderly people, the appli-

cation of specific protective cultures to produce antimi-

crobial substances could improve the sanitary conditions

of such fermented foods for these higher risk populations.

Bioactive extracts from such BLIS-producing strains

could also find applications as hurdles against trans-

mission of pathogenic bacteria in several other kinds of

infant formula.

Biocontrol of enteric pathogens in farmanimalsLivestock (such as pigs, cattle and poultry) are the main

reservoirs of important food-borne pathogens such as E.coli, Salmonella, Shigella or Campylobacter strains. The

application of antibiotics in animal breeding and in animal

health results in training of pathogenic bacteria against

antibiotics of clinical use, and infections caused by the

resulting multi-resistant strains are increasingly difficult

to treat. Several microbial antagonists (mostly colicins and

microcins) have been proposed or marketed for appli-

cation in livestock [52��].

Administration of bacteriocins in feed before poultry

slaughter appears to provide the control of C. jejuni to

effectively reduce human exposure. Microencapsulated

bacteriocin preparations from Paenibacillus polymyxa and

Lactobacillus salivarius in chicken feed dramatically

reduced both intestinal levels and frequency of coloniza-

tion by campylobacters (C. jejuni, C. coli) in broiler chick-

ens and in turkey poults [5�,53�,54�]. Bacteriocin

administration also had an impact on the gut morphology

of turkey poults, reducing crypt depth and goblet cell

density [54�], although it is not clear whether this was a

direct or indirect effect of treatment. The influence of


such alterations on colonization by Campylobacter as well

as by other enteropathogens remains to be deciphered.

Some enterocins produced by enterococci isolated from

poultry also show promising results. Beneficial effects

reported for the administration of enterocins E50-52

and E-760 in feed or water to broilers included a dramatic

reduction of cecal levels of C. jejuni and Salmonellaenteritidis, and reduction of the systemic dissemination

of salmonellae in liver and spleen [7�,8�]. Although the

total LAB content in the ceca of birds apparently was not

affected by the administration of enterocins, the impact of

bacteriocins on the global composition of the intestinal

microbiota (including the LAB composition) needs to be

further investigated. Since these enterocins also display

strong antibacterial activity against other food-borne

pathogens (Salmonella spp., Shigella spp., E. coliO157:H7 and Y. enterocolitica) they could probably be

used to control pathogen colonization of poultry as well

as other farm animals. Nevertheless, bacteriocin inacti-

vation by proteases of the gastrointestinal tract, differ-

ences in strain sensitivity to bacteriocins, and the

emergence of bacteriocin resistant or adapted strains need

to be evaluated. For these reasons, administration of

cocktails containing several bacteriocins should be recom-

mended rather than single bacteriocins. It is also likely

that bacteriocin treatments eliminate pathogenic bacteria

from most but not all enteric locations. In order to prevent

recolonization of the gut by the remaining survivors,

bacteriocin challenges could be applied just before mar-

keting.

Conclusions and perspectivesResearch on biocontrol of pathogenic bacteria through the

food chain has provided a wide array of treatment options

based on natural antimicrobials. In spite of the large

number of laboratory studies carried out with different

bacteriocins, there is still a long way to industrial appli-

cations, with little innovation with respect to classical

commercial preparations such as nisin and pediocin PA-1/

AcH. Antimicrobial activity of bacteriocins can be modi-

fied by genetic engineering, and hybrid bacteriocin mol-

ecules are to be expected in the future. However,

heterologous bacteriocin production and development

of large-scale production processes are challenging. Eth-

nic foods are valuable sources for new bacteriocin-produ-

cing strains better adapted to their food substrates and

maybe also with novel and interesting biotechnological

properties. Several novel bacteriocins capable of inhibit-

ing Gram-negative bacteria of concern in foods have been

described recently, and conceivably this will open new

possibilities for their application in food preservation.

Some of them have been already tested with satisfactory

results in the control of pathogenic bacteria in farm

animals. However, the impact of bacteriocin-producing

strains on the microbial ecology of the gastrointestinal

tract and on animal health is far from being understood.



One major pending issue is extending the spectrum of

bacteriocins to food-borne parasitic protozoa and viruses.

These are of major concern in foods that are eaten without

cooking or not cooked sufficiently. Remarkably, enteric

viruses always rank in outstanding positions in statistics of

food-borne illnesses. The antifungal activity of LAB has

not been exploited satisfactorily, in spite of the great

interest to control food spoilage caused by yeasts and

filamentous fungi as well as mycotoxin production.

Screening for novel antifungal LAB strains from less

explored environments such as ethnic foods, together

with genetic engineering approaches, may contribute to

fill the existing gap in this field. Nevertheless, antifungal

compounds may also have toxic effects on other eukar-

yotic cells, and may not meet the qualified presumption of

safety (QPS) status attributed to bacteriocins and other

antimicrobials produced by LAB.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

1.��

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3.��

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4.�

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5.�

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6.�

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7.�

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9.�

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23.�

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29.�

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32. Ananou S, Garriga M, Jofre A, Aymerich T, Galvez A, Maqueda M,Martınez-Bueno M, Valdivia E: Combined effect of enterocin AS-48 and high hydrostatic pressure to control food-bornepathogens inoculated in low acid fermented sausages. MeatSci, in press.

33. Sobrino-Lopez A, Viedma-Martınez P, Abriouel H, Valdivia E,Galvez A, Martin-Belloso O: The effect of adding antimicrobialpeptides to milk inoculated with Staphylococcus aureus andprocessed by high-intensity pulsed-electric field. J Dairy Sci2009, 92:2514-2523.

34. Sparo M, Nunez GG, Castro M, Calcagno ML, Garcıa Allende MA,Ceci M, Najle R, Manghi M: Characteristics of an environmentalstrain. Enterococcus faecalis CECT7121, and its effects asadditive on craft dry-fermented sausages. Food Microbiol 2008,25:607-615.

35. Hampikyan H: Efficacy of nisin against Staphylococcus aureusin experimentally contaminated sucuk, a Turkish-typefermented sausage. J Food Prot 2009, 72:1739-1743.

36. Black EP, Linton M, McCall RD, Curran W, Fitzgerald GF, Kelly AL,Patterson MF: The combined effects of high pressure and nisinon germination and inactivation of Bacillus spores in milk. JAppl Microbiol 2008, 105:78-87.


37.�

Gao YL, Ju XR: Exploiting the combined effects of highpressure and moderate heat with nisin on inactivation ofClostridium botulinum spores. J Microbiol Methods 2008,72:20-28.

Bacterial endospores are refractile to high-hydrostatic pressure (HHP)treatments. This work describes an interesting approach to inactivateendospores in foods processed by HHP.

38.�

Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D,Granot D, Sela S: Internalization of Salmonella enterica inleaves is induced by light and involves chemotaxis andpenetration through open stomata. Appl Environ Microbiol2009, 75:6076-6086.

This work is an illustrative example on the microbial ecology of entericpathogens outside their natural hosts and how they can interact withvegetables in order to survive and multiply.

39.�

McEvoy JL, Luo Y, Conway W, Zhou B, Feng H: Potential ofEscherichia coli O157:H7 to grow on field-cored lettuce asimpacted by postharvest storage time and temperature. Int JFood Microbiol 2009, 128:506-509.

This interesting work illustrates how the changes in harvesting practicesmay have an impact on transmission of food-borne pathogens such as E.coli through fresh produce.

40.�

Cobo Molinos A, Abriouel H, Lucas Lopez R, Valdivia E, BemOmar N, Galvez A: Combined physico-chemical treatmentsbased on enterocin AS-48 for inactivation of Gram-negativebacteria in soybean sprouts. Food Chemical Toxicol 2008,46:2912-2921.

The proposed decontamination treatments based on the cyclic bacter-iocin in combination with other antimicrobials reduce the microbial load ofGram-negative bacteria on sprouts and afford protection againstregrowth during refrigeration storage.

41.�

Abuladze T, Li M, Menetrez MY, Dean T, Senecal A,Sulakvelidze A: Bacteriophages reduce experimentalcontamination of hard surfaces, tomato, spinach, broccoli,and ground beef by Escherichia coli O157:H7. Appl EnvironMicrobiol 2008, 74:6230-6238.

This work strengthens the potential of bacteriophages as biocontrolagents for decontamination against E. coli O157:H7, decreasing the risksfor transmission of this pathogenic bacterium through different routessuch as beef meat, fresh produce, and contact surfaces.

42. Trias R, Baneras L, Badosa E, Montesinos E: Bioprotection ofGolden Delicious apples and Iceberg lettuce againstfoodborne bacterial pathogens by lactic acid bacteria. Int JFood Microbiol 2008, 123:50-60.

43.�

Martınez-Viedma P, Sobrino A, Ben Omar N, Abriouel H, LucasLopez R, Valdivia E, Martın Belloso O, Galvez A: Enhancedbactericidal effect of high-intensity pulsed-electric fieldtreatment in combination with enterocin AS-48 againstSalmonella enterica in apple juice. Int J Food Microbiol 2008,128:244-249.

The combined treatment of HIPEF and enterocin AS-48 increased themicrobial inactivation of salmonellae in fruit juice, decreasing the risks fortransmission of this pathogen through fresh fruit juices.

44. Buzrul S, Alpas H, Largeteau A, Demazeau G: Inactivation ofEscherichia coli and Listeria innocua in kiwifruit and pineapplejuices by high hydrostatic pressure. Int J Food Microbiol 2008,124:275-278.

45. Ukuku DO, Zhang H, Huang L: Growth parameters ofEscherichia coli O157:H7, Salmonella spp., Listeriamonocytogenes, and aerobic mesophilic bacteria of applecider amended with nisin-EDTA. Foodborne Pathog Dis 2009,6:487-494.

46. Jofre A, Aymerich T, Garriga M: Assessment of the effectivenessof antimicrobial packaging combined with high pressure tocontrol Salmonella sp. in cooked ham. Food Control 2008,19:634-638.

47. Santiago-Silva P, Soares NFF, Nobrega JE, Junior MAW,Barbosa KBF, Volp ACP, Zerdas ERMA, Wurlitzer NJ:Antimicrobial efficiency of film incorporated with pediocin(ALTA

W2351) on preservation of sliced ham. Food Control

2009, 20:85-89.

48.�

Bigwood T, Hudson JA, Billington C, Carey-Smith GV,Heinemann JA: Phage inactivation of foodborne pathogens oncooked and raw meat. Food Microbiol 2008, 25:400-406.



This work exemplifies the use of bacteriophages in biocontrol strategiesto reduce the microbial load of relevant food-borne pathogens (Salmo-nella Typhimurium and Campylobacter jejuni) on meat.

49. Lee SY, Jin HH: Inhibitory activity of natural antimicrobialcompounds alone or in combination with nisin againstEnterobacter sakazakii. Lett Appl Microbiol 2008,47:315-321.

50. Al-Nabulsi AA, Osaili TM, Al-Holy MA, Shaker RR, Ayyash MM,Olaimat AN, Holley RA: Influence of desiccation on thesensitivity of Cronobacter spp. to lactoferrin or nisin in brothand powdered infant formula. Int J Food Microbiol 2009,136:221-226.

51. Sanchez Valenzuela A, Dıaz Ruiz G, Ben Omar N, Abriouel H,Lucas Lopez R, Martınez Canamero M, Ortega E, Galvez A:Inhibition of food poisoning and pathogenic bacteria byLactobacillus plantarum strain 2.9 isolated from ben saalga,both in a culture medium and in food. Food Control 2008,19:842-848.

52.��

Diez-Gonzalez F: Applications of bacteriocins in livestock. CurrIssues Intest Microbiol 2007, 8:15-23.


An excellent overview on application of bacteriocins and bacteriocin-producing strains in livestock for preharvest control of food-borne patho-gens or as growth promoters.

53.�

Stern NJ, Svetoch EA, Eruslanov BV, Kovalev YN, Volodina LI,PerelyginVV,MitsevichEV,Mitsevich IP,LevchukVP:Paenibacilluspolymyxa purified bacteriocin to control Campylobacterjejuni in chickens. J Food Prot 2005, 68:1450-1453.

The authors investigated paenibacilli as a novel source of antimicrobialsubstances for application in broiler chickens, and demonstrated theprotective effects of microencapsulated bacteriocin against chicken colo-nization by campylobacters. Feeding bacteriocin before slaughter appearsto effectively control campylobacters to reduce human exposure.

54.�

Cole K, Farnell MB, Donoghue AM, Stern NJ, Svetoch EA,Eruslanov BN, Volodina LI, Kovalev YN, Perelygin VV, Mitsevich EVetal.: Bacteriocinsreduce Campylobactercolonization andaltergut morphology in turkey poults. Poult Sci 2006, 85:1570-1575.

Dietary administration of bacteriocins (B602 from P. polymyxa and OR7from L. salivarius) reduced the levels of C. coli (the most prevalentCampylobacter species in turkey) in turkey poults. This work also demon-strates for the first time the effect of bacteriocin ingestion on gut mor-phology.


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Microbial antagonists to food-borne pathogens and biocontrol