essay代写/report代写/paper代写-Microbes versus

essay代写/report代写/paper代写

3079

Review

Received: 14 October 2013 Revised: 7 February 2014 Accepted article published: 9 May 2014 Published online in Wiley Online Library: 30 May 2014

####### (wileyonlinelibrary.com) DOI 10.1002/jsfa.

Microbes versus microbes: control

of pathogens in the food chain

Kieran Jordan,

a*

Marion Dalmasso,

a

Juergen Zentek,

b

Anneluise Mader,

b

Geert Bruggeman,

c

John Wallace,

d

Dario De Medici,

e

Alfonsina Fiore,

e

Estella Prukner-Radovcic,

f

Maja Lukac,

f

Lars Axelsson,

g

Askild Holck,

g

Hanne Ingmer

h

and Mindaugas Malakauskas

i

Abstract

####### Foodborne illness continues as a considerable threat to public health. Despite improved hygiene management systems and

####### increased regulation, pathogenic bacteria still contaminate food, causing sporadic cases of illness and disease outbreaks world-

####### wide. For many centuries, microbial antagonism has been used in food processing to improve food safety. An understanding

####### of the mode of action of this microbial antagonism has been gained in recent years and potential applications in food and feed

####### safetyarenowbeingexplored.Thisreviewfocusesonthepotentialopportunitiespresented,andthelimitations,ofusingmicro-

####### bial antagonism as a biocontrol mechanism to reduce contamination along the food chain; including animal feed as its first link.

####### 2014 Society of Chemical Industry

####### Keywords: microbial antagonism; food/feed chain; food safety; bacteriophage; bacteriocins; biocontrol; probiotics; prebiotics

INTRODUCTION

####### In a globalised world, the food chain is becoming increasingly

####### complex. Feed is now recognised as the first step in the food chain

####### as animal welfare and feed can influence food safety. Many animals

####### are symptomless carriers of human foodborne pathogens. Antibi-

####### otics and antimicrobial growth promoters (AMGPs) have been

####### commonly used for over 50 years for the treatment of microbial

####### infectious diseases, and to improve animal performance in inten-

####### sive animal husbandry, respectively. Although antibiotics have

####### proven to be very effective against pathogens, their use is associ-

####### ated with at least three adverse effects. Firstly, they are not spe-

####### cific towards pathogens but also kill commensal flora with the

####### same efficacy, leading to imbalance of the normal microflora.

####### Secondly, their extensive use has resulted in evolutionary adap-

####### tations by microorganisms, resulting in resistance towards their

####### activity,^1 ^5 and thirdly there are public concerns about residues

####### in food derived from treated animals. The European Commu-

####### nity Strategy was adopted in June 2001 to combat the threats

####### to human and animal health posed by antimicrobial resistance

####### in pathogenic microorganisms in a response to several public

####### reports on health concerns, for example the WHO recommenda-

####### tions from 2001 at the Copenhagen meeting. Thus, the European

####### Commission decided to ban all commonly used feed antibiotics

####### from 2006 and also to reduce the therapeutic use of antibiotics

####### as much as possible.^6 ,^7 In considering phasing out or banning

####### AMGPs, the international search for substitutes of AMGPs contin-

####### ues to be assessed. The main way in which this can be achieved is

####### the development of substitutes to antibiotics that work via similar

####### mechanisms, promoting growth whilst enhancing the efficiency

####### of feed conversion and combating pathogens. In this context,

####### biological control to prevent pathogens in animal feed and to

####### eliminate hazardous components (such as antibiotics, hormones

####### and other chemotherapeutics) has some potential. An entirely

####### biological approach to the control of bacterial infections will be a

####### significant step forward at primary production.^8 ^10

####### Hygiene measures on their own are not sufficient to eliminate

####### the threat of foodborne pathogens in the food chain. Therefore,

####### additional control measures are necessary in order to reduce the

####### associated risks. For many years, the activities and metabolites of

####### harmless bacteria (e.g. during fermentation) have inadvertently

Correspondence to: Kieran Jordan, Teagasc Food Research Centre, Moorepark,
Fermoy, Co. Cork, Ireland. E-mail: kieran.jordan@teagasc.ie

aTeagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland

bInstitute of Animal Nutrition, Department of Veterinary Medicine, Freie Univer-
sitt Berlin, Knigin-Luise-Str. 49, 14195 Berlin, Germany

cNutrition Sciences N.V., Booiebos 5, 9031 Drongen, Belgium

dUniversity of Aberdeen, UK

eIstituto Superiore di Sanit, DSPVSA, Microbiological Foodborne Hazard Unit,
Rome, Italy

fFaculty of Veterinary Medicine, University of Zagreb, Heinzelova 55, 10 000
Zagreb, Croatia

gNofima  Norwegian Institute for Food, Fisheries and Aquaculture Research;
P.O. Box 210, N-1431 s, Norway

hDepartment of Veterinary Disease Biology, University of Copenhagen,
Stigbjlen 4, DK-1870 Frederiksberg C, Denmark

iLithuanian University of Health Sciences, Department of Food Safety and
Quality, Kaunas, Lithuania

J Sci Food Agric2014; 94 : 30793089 http://www.soci.org 2014 Society of Chemical Industry

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####### http://www.soci.org K Jordanet al.

####### been used to help control harmful bacteria, referred to as microbial

####### antagonism.^6 The mechanisms by which such antagonism lim-

####### its pathogens are now better understood and the deliberate use

####### of such antagonism is being realised, although not widely used.

####### Such microbial antagonism can be applied in primary production

####### (in animals) or during food processing. In animals, opportunities

####### are offered by use of probiotics, prebiotics, competitive exclusion

####### (CE) and antimicrobial peptides. In food processing, the opportu-

####### nities are mainly in the use of fermentation, protective cultures

####### and bacteriophages. Due to concerns surrounding the over-use of

####### antibiotics (in livestock) and the development of microbial antibi-

####### otic resistance, alternatives to antibiotics are necessary. In addi-

####### tion, symptomless carriers of pathogens will not be treated with

####### antibiotics. In primary production, the use of processes that con-

####### trol growth of pathogens with microbial antagonism as the prin-

####### cipal mode of action offers advantages over antibiotic use. The

####### food industry is also constantly facing new challenges related

####### to microbial pathogens, including outbreaks of foodborne ill-

####### ness, product recalls, regulatory compliance and issues related

####### to pathogen control. There is also a pressure on the food indus-

####### try to reduce costs and waste and to increase shelf-life, with less

####### use of chemical preservatives and salt. With an increasing pop-

####### ulation that has reduced immune system activity (i.e. children,

####### the elderly and immunocompromised persons), these conflicting

####### requirements present a challenge. Using microbial antagonism

####### offers great opportunities to control pathogens along the food

####### chain, and therefore improve food safety.

SCOPE OF THE REVIEW

####### Current research has shown the extent to which some bacte-

####### ria or their products can be used to inhibit the growth of other

####### bacteria.^7 ,^11 Such microbial antagonism, while used inadvertently

####### for many years in processes such as fermentation, is now better

####### understood. However, the maximum benefit from this microbial

####### antagonism has not yet been realised. The scope of the review is

####### to assess current knowledge on microbial antagonisms that can be

####### used to reduce the pathogen load in the food chain. It focuses on

####### the technologies that can be used, particularly with respect to the

####### major pathogensSalmonella,Listeria,Campylobacter, pathogenic

####### Escherichia coli, although there are broader applications of such

####### technologies. The major issues surrounding such use are dis-

####### cussed. Up to now, less sustainable methods were used to improve

####### zootechnical performance in animals or to reduce pathogens from

####### feed, animals and food along the entire food chain. Examples

####### include antibiotics used as growth promoters, thermal processes

####### for lowering pathogen loads or supplementation with chemical

####### preservatives. These methods raise issues on antibiotic resistance

####### and toxicity or are energy demanding, and have an influence on

####### the organoleptic quality of food and the ecological footprint of

####### animal and human life. There is a need for wider use of more sus-

####### tainable methods of improving animal performance or enhancing

####### food safety with respect to pathogens and using microbial antag-

####### onism can offer this more sustainable option.

MICROBE-TO-MICROBE DIRECT CONTROL

OF PATHOGENS

####### Microbial antagonism can be used for the biocontrol of pathogens

####### at primary production, in food production facilities and in foods.

####### Direct biocontrol of pathogens by other bacteria implies a sci-

####### entific approach to improving microbial safety of foods and may

####### involve the use of probiotics and CE at primary production,

####### and of bacteriophages (although not strictly microbial), bacte-

####### riocins (peptides secreted by one species that inhibit another),

####### siderophores (molecules that sequester iron), quorum sensing

####### (where the presence of an auto-inducer of one species may influ-

####### ence the growth of another), competitive organisms during food

####### production.

####### Probiotics at primary production

####### Probiotics, defined as a live microbial feed supplement that bene-

####### ficially affects the host, are believed to improve the overall health

####### of an animal by improving the microbial balance in its gut and

####### its intestinal metabolic activity, and by stimulating its immune

####### system. In recent years it has become increasingly clear that in

####### addition to feed composition, the use of probiotics represents an

####### interesting option for modification of the gut microbial flora in

####### animals. In Europe, probiotics are classified as zootechnical addi-

####### tives, which must be approved by the European Commission fol-

####### lowing a defined procedure. The exact definition of feed additives

####### and the applicable approval criteria are stated in the relevant EU

####### regulations.^12 Currently, most probiotics are lactic acid-producing

####### vegetative or spore-forming bacteria, but one strain of yeast,

####### Saccharomyces cerevisiae, is also included. It is important to note

####### that the use is strain-specific and restricted for specific groups

####### of animal species. A detailed list of authorised probiotics can be

####### found in the Community Register of feed additives, which is con-

####### tinually updated and is available on the internet.^13 In other regions

####### registration of probiotic additives is not as regulated as it is in

####### the EU.

####### Inordertobeeffective,probioticbacteriamustbeabletosurvive

####### the harsh conditions of the production process in the compound

####### feed industry. Thus, it is often necessary to use special manu-

####### facturing methods, for example end-of-line-coating processes.^14

####### Probiotics must be able to survive the storage conditions and

####### to temporarily colonise the gastro-intestinal tract of the animal.

####### This colonisation is counteracted by the prevailing adverse condi-

####### tions, in particular the acidic pH in the stomach, bile and digestive

####### enzymes, and the stability and concentration of the endogenous

####### microflora. The concentration of the endogenous microflora is

####### generally several orders of magnitude higher than the concentra-

####### tion of the probiotic.^15

####### Despite these apparently stringent requirements, it can be

####### shown for various probiotics that they have the ability to colonise

####### the digestive tract of animals.^16

####### The mechanism of action of probiotics has not been fully estab-

####### lished, although it has been hypothesised that they colonise the

####### gut in large numbers, thus excluding pathogens and prevent-

####### ing them from causing infection. They act as a stimulus for the

####### immune system (immunomodulation), possibly macrophages.^17

####### As the immune system is engaged following exposure to probi-

####### otic bacteria, any pathogens that are detected, following increased

####### surveillance by leukocytes, can be eliminated.^18 Probiotics can

####### have a strong, positive influence on intestinal metabolic activi-

####### ties, such as increased production of vitamin B 12 , antimicrobial

####### peptides (like bacteriocins), and short-chain fatty acids, such as

####### lactic and propionic acids. They also have a beneficial role on

####### the intestinal mucosa which relies on different mechanisms such

####### as cytoprotection, cell proliferation and migration, resistance to

####### apoptosis, synthesis of proteins and gene expression. They also

####### strengthen the epithelial tight junctions and consequently pre-

####### serve the mucosal barrier function.^19 In general, probiotics can

####### help to stabilise the digestive process, and are most effective in

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####### newborn animals or those that have been treated with antibiotics.

####### In many cases, probiotics are used in compound feed for piglets

####### around weaning in order to stabilise the gut function or for the

####### feeding of poultry to reduce pathogen loads. For example, probi-

####### otics have in some cases successfully reducedSalmonellainfection

####### in broilers and turkeys.^20

####### It was found that excretion ofSalmonellaserovar Typhimurium

####### increased after application of a probiotic strain ofEnterococcus fae-

####### ciumto pigs.^21 On the other hand, after application of a probiotic

####### strain ofBacillus cereus, animal health was improved but the elim-

####### ination ofS.Typhimurium was reduced. Therefore, the effect of

####### probiotics on the colonisation of the gastro-intestinal tract should

####### be evaluated specifically on a case-by-case basis. It is also appar-

####### ent that the interaction of probiotic bacteria with the endogenous

####### microflora will vary.^21

####### Theimmuneresponsemayalsovary,dependingontheprobiotic

####### strain used. The colonisation of the intestinal epithelium with

####### lymphocytes was affected differently byE. faeciumandB. cereusin

####### piglets.E. faeciumresulted in a reduced immune response, while

####### B. cereusseemed to be effective towards an enhanced immune

####### response. This could be demonstrated both in the intestinal tract

####### and in the peripheral immune system.^22 ^24

####### Despite the potential uses in reduction of pathogens, the main

####### use of probiotics is, however, the growth performance of farm ani-

####### mals. The use of probiotics for the reduction of zoonotic bacteria

####### is not yet common practice and the influence on zoonotic agents

####### has only been substantiated by relatively few studies.^25 ^27

####### Competitive exclusion along the food chain

####### Competitive exclusion at primary production

####### Competitive exclusion treatment (for example application of the

####### microflora of a healthy adult poultry digestive tract to newly

####### hatched chicks) is another type of preventive measure that may

####### be used to control pathogenic enterobacteria in poultry flocks.

####### CE treatment is most effective when used as part of an over-

####### all control programme that includes comprehensive biosecu-

####### rity measures.^28 Competitive exclusion was first used on newly

####### hatched chicks which were pretreated by oral administration of

####### suspensions or cultures of gut-content from suitable adult donor

####### birds or by defined mixtures of intestinal bacteria.^29 Currently

####### available treatment products contain many of the elements of a

####### normal adult microflora, but their exact composition is usually

####### unknown and therefore they are not acceptable for commercial

####### use in all countries.^30 ,^31 Nevertheless, such products have a long

####### history of safe use, not only in Scandinavia,^32 ^35 butalsoinmany

####### other countries, and this concept is well established especially for

####### SalmonellaandCampylobacter.^9 ,^36 ^38 In the control ofSalmonella

####### infection in poultry, rapid establishment of an adult intestinal

####### microflora in young chicks increases their resistance to colonisa-

####### tion by pathogenic bacteria. This is based on the fact that young

####### chicks are particularly susceptible toSalmonella, because they lack

####### a fully developed intestinal microflora that would otherwise pre-

####### vent the colonisation of pathogens.^39 ,^40 AlthoughSalmonellais

####### rarely excluded completely, there is usually a significant reduction

####### in prevalence and in levels of intestinal carriage among positive

####### birds.^41 For older birds that may be given a therapeutic dose of

####### antibiotics to clear an existingSalmonellainfection, CE treatment

####### can be used to regenerate the intestinal microflora and reduce the

####### risk of re-infection.^42 ,^43 The effects of treatment with a CE prod-

####### uct, an experimental dietary probiotic, and the abiotic -glucan,

####### on caecal colonisation, organ invasion, and serum and intestinal

####### IgG and IgA levels duringSalmonellachallenge in broiler chicks

####### has been investigated.^44 It was shown that the combination of a

####### CE product and -glucan, with or without probiotic, during the first

####### week of life, resulted in a superior inhibition of caecal colonisation

####### and organ invasion bySalmonella.

####### In poultry production, there are limitations on the use of unde-

####### fined CE preparations in many countries, although in Brazil CE

####### treatment and probiotics (or dietary organic acids) are used in

####### combination with biosecurity measures. Biosecurity measures and

####### vaccination remain the commonSalmonellacontrol measures in

####### many European countries.

####### Protective cultures and competitive exclusion during

####### food production

####### To date, the biocontrol approach with the greatest consumer

####### acceptance is the use of lactic acid bacteria (LAB) and/or their

####### antimicrobial metabolites, as antagonistic bacteria during food

####### production. Bacterial antagonism represents one of many defen-

####### sive systems provided by the microorganisms. For example, LAB

####### control can inhibit other organisms by different mechanisms,

####### such as nutrient competition, immunostimulation, competition

####### for binding sites, production of antimicrobial substances such as

####### organic acids, hydrogen peroxide (H 2 O 2 ) and proteinaceous com-

####### pounds such as bacteriocins that can kill or inhibit growth of other

####### bacteria in food.

####### The application of LAB as protective cultures to enhance food

####### safety has been extensively reviewed.^45 Such cultures can be

####### added as additional cultures to the fermenting bacteria already

####### added, or they may be a natural feature of the normal fermentation

####### culture in that they produce antimicrobial compounds naturally.

####### The main considerations for this type of approach include the dose

####### required for effective antagonism in the food, inhibitory effects of

####### food components and the potential effects on sensory properties.

####### The primary objective for use of LAB is to reduce the incidence

####### of foodborne illness by reducing the prevalence and/or numbers

####### of human pathogens. Secondly, LAB may also reduce spoilage

####### organisms and increase the shelf-life of food.

####### Lactobacilli have been exploited to improve safety in a variety

####### of food applications including meats, fish, vegetables and dairy

####### products.^46 ^49 Similarly, several species of bifidobacteria have

####### been applied in order to extend shelf life or improve the safety

####### of fish, seafood, poultry and dairy foods. An extension of food

####### shelf-life ranging from 3 to 14 days has been reported when using

####### bifidobacteria.^45

####### Fermentation processes for food production

####### Processes involved in the manufacturing of most fermented foods

####### are not favourable, and can even be inhibitory, to many microor-

####### ganismspresentinfoods.Theantimicrobialeffectsoffermentation

####### are not limited to food spoilage microorganisms but usually can

####### also affect pathogens that might be present. Therefore, using tra-

####### ditional food fermentation processes, potentially hazardous raw

####### materials (e.g. raw milk and meat) may be used for production of

####### food with improved quality and increased safety. The extent to

####### which fermented foods inhibit pathogens and how fermentation

####### processes should be conducted to achieve a desired level of safety

####### are key questions.^1

####### Currently, 62 genera are considered as microbial food cultures

####### with a history of safe use for fermentation purposes.^50 Evolution

####### in taxonomy, the extension of varied usages in different matrices,

####### yeast fermentations and foods produced by fungi have extended

####### the current list of microbial food cultures up to 195 bacterial and

####### J Sci Food Agric2014; 94 : 30793089 2014 Society of Chemical Industry wileyonlinelibrary.com/jsfa

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####### http://www.soci.org K Jordanet al.

####### 69 species of yeasts and moulds with demonstration of safe food

####### usage.

####### In recent years, there has been a particular focus on the appli-

####### cation of antimicrobial compounds produced by LAB and other

####### microbial food cultures as natural preservatives to control the

####### growth of spoilage and pathogenic bacteria in food.^51 ,^52 Sev-

####### eral LAB bacteriocins produced during fermentation could poten-

####### tially be used for food preservation, thereby the food industry

####### could reduce the application of chemical preservatives, tempera-

####### ture intensity of heat treatments and addition of chemicals. Such

####### changes in food production would benefit consumers, by provid-

####### ing desirable properties, more naturally preserved foods that are

####### richer in sensory attributes and nutritional properties while main-

####### taining safety.

####### There is a lack of knowledge about the dynamics of microbial

####### populations involved in food fermentation processes. LAB, with

####### the status of Generally Recognised As Safe (GRAS) or Qualified

####### Presumption of Safety (QPS), produce lactic acid and other func-

####### tional antimicrobial metabolites, such as diacetyl, acetoin, hydro-

####### gen peroxide, bacteriocins and others, that are potentially useful

####### as natural substitutes for chemical preservatives.^53 LAB have great

####### potential in the context of biocontrolling the growth of pathogens

####### and spoilage bacteria in food and thus enhancing food safety,

####### quality and extending shelf life.Listeria monocytogenes,E. coli

####### O157:H7,S.Typhimurium andStaphylococcus aureushave been

####### extensively studied in relation to their survival during fermenta-

####### tion processes of different types of food.^54 ,^55 However, limited data

####### are available about reduction of other pathogens during fermen-

####### tation processes.

####### Any microbial strain intended for use as a microbial food cul-

####### ture should be free from any associated risks. The inability to

####### form biogenic amines (certain amino acid decarboxylase activ-

####### ities), ability to produce antibiotics (fungi) and the absence of

####### mycotoxin genes are important.^50 ,^56 ,^57 Lactic acid bacteria widely

####### used as starter cultures in dairy products enter our intestines

####### in large numbers and interact with the intestinal microbiota.^58

####### Therefore, they should not contain antibiotic resistance genes,

####### to minimise the risk of transferring such genes to pathogenic

####### bacteria.^59 As a general rule, lactobacilli have a high natural resis-

####### tancetobacitracin,cefoxitin,ciprofloxacin,fusidicacid,kanamycin,

####### gentamicin, metronidazole, nitrofurantoin, norfloxacin, strepto-

####### mycin, sulfadiazine, teicoplanin, trimethoprim/sulfamethoxazole,

####### and vancomycin.^60 A specific risk assessment should be conducted

####### on strains presenting these undesirable properties to determine

####### whether resistance is intrinsic or possibly transferable, even if they

####### belong to a species with a long history of safe use.^61 ,^62

####### Bacteriocins in food production

####### Bacteriocins are small peptides that can be produced by bacteria

####### to inhibit other bacteria in their environment. They can have a

####### narrow spectrum of activity where they inhibit only closely related

####### organisms, or a broad spectrum of activity where they inhibit a

####### broad number of bacteria. Within the bacteriocins, there are a

####### number of different classifications that have been reviewed.^63 The

####### most widely studied are the bacteriocins of the LAB and much

####### attentionhasbeenfocusedontheseintermsoffoodsafetydue

####### to their GRAS status.^64 ,^65 LAB bacteriocins usually exhibit activity

####### against Gram-positive pathogens such asL. monocytogenesand

####### Staph. aureus,^66 but are not active against Gram-negative bacteria,

####### unless their outer membrane is destabilised.^67

####### Although having similar effects, bacteriocins differ from antibi-

####### otics due to their synthesis, mode of action, toxicity and resistance

####### mechanisms. However, they have been shown to be effective in

####### food,^64 and are also safe for use in the food supply chain. For this

####### reason, they have potential application in the food industry as

####### natural bio preservatives as well as for bio-decontamination, to

####### produce food with high safety standards.

####### Bacteriocins may be present in food due to the presence of the

####### LAB (that produce them) used as starter cultures, or because puri-

####### fied product is added directly in food. To date, however, only two

####### LAB bacteriocins, nisin and pediocin PA-1, are commercially avail-

####### able and have applications in food systems.^68 Extensive research

####### on a range of other bacteriocins has been undertaken, including

####### research on variants of nisin that have increased efficacy.^69

####### Developments in bacteriocins continue; bacterial antago-

####### nism of probiotic bacteria and foodborne pathogens shows

####### that the bacteriocins nisin, coagulin and thermophilin pro-

####### duced byLactococcus lactissubsp.lactis,Bacillus coagulansand

####### Streptococcus thermophilus, respectively, are able to inhibit the

####### growth of botulinum neurotoxin (BoNT)-producing clostridia and

####### Cronobacterspp. (Fioreet al., personal communication). Further

####### information on bacteriocins is detailed on BACTIBASE, a spe-

####### cific online database dedicated to bacteriocins (http://bactibase

####### .pfba-lab-tun.org/main.php), which is a great resource for bacteri-

####### ocin research.

####### Such bacteriocin-based biocontrol strategies offer particular

####### advantages, mainly because they are perceived as natural by con-

####### sumers. Bacteriocins are powerful foodborne pathogen inhibitors;

####### organisms that show resistance to antibiotics are generally not

####### cross-resistant with bacteriocins, and unlike antibiotic resistance,

####### bacteriocin resistance is not usually genetically determined. How-

####### ever, food matrixes and food production conditions could affect

####### the efficacy of bacteriocins. Adsorption to proteins and interac-

####### tions with fat are suspected to reduce bacteriocin activity. Prote-

####### olytic activity of psychrotrophic bacteria may also reduce the effi-

####### cacy of bacteriocins as a decreased activity for some of them has

####### beenobservedduringcoldstorageoffood.^70 Furtherstudyonbac-

####### teriocins should focus on chemical identification and characterisa-

####### tion, and their use and efficacy tested, the manufacturing process

####### described and assays used for quantification and standardisation

####### of the peptides devised. In addition, toxicological data on the fate

####### of the molecule after ingestion are needed in order to evaluate the

####### effectiveness of the use of these agents in real scenarios. Further

####### studies are also needed to investigate the possibility in using LAB

####### to reduce the risk of infection due to BoNT-producing clostridia

####### andCronobacterspp.

####### Bacteriophages as biocontrol agents along the food chain

####### First discovered in 1917, bacteriophages are natural enemies of

####### bacteria. With the advent of antibiotics in the 1940s, studies on

####### bacteriophage therapy were discontinued in the Western world,

####### although the use of bacteriophages as therapeutic agents con-

####### tinued in the former Soviet Union.^71 Studies on applications of

####### bacteriophages continued at the Eliava Institute of Bacteriophage,

####### Microbiology and Virology, Tbilisi, Georgia.^72

####### Bacteriophages have a number of attributes that make them

####### logical candidates for control of foodborne pathogens such as

####### L. monocytogenes, including their self-perpetuating nature, their

####### relative stability during storage, their ability to target their host

####### bacterium with high specificity without impacting on the com-

####### mensal microflora present, and their history of safe use.^73 Within

####### the last few years, food growers and producers have begun to use

####### a novel and innovative means of improving food safety through

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####### the use of bacteriophages. Also known as lytic viruses, bacterio-

####### phages take up residence inside certain strains of foodborne bac-

####### teria, begin multiplying, and eventually destroy the bacterial cell.

####### Bacteriophages are remarkably stable through the food chain and

####### are readily recovered from soil, sewage, water, farm and processing

####### plant effluents, faeces and retail foods.^74

####### The consensus among microbiologists is that bacteriophages

####### do not have any known adverse effects on humans, animals, or

####### the environment, and in fact they gravitate toward wherever

####### bacteria live, including the animal and human body, water, and

####### the environment. For this reason, many scientists and food safety

####### experts predict that bacteriophages could become a useful tool

####### in the reduction of dangerous pathogens in the food chain. How-

####### ever, there are concerns that limited safety data testing has been

####### undertaken, although bacteriophages have been widely used for

####### treatment of human diseases in the former Soviet Union.^72 Some

####### further concerns relating to biopreservation with bacteriophages

####### are a limited host (pathogen) range, limited accessibility of bac-

####### terial targets in foods, development of phage resistance and for

####### practical purposes, the requirement for obtaining sufficiently high

####### phage titres and the confirmation of absence of lysogeny (ability

####### of bacteriophages to integrate the bacterial chromosome without

####### involving lysis).^75

####### In September 2006, the US Food and Drug Administration (FDA),

####### under the category of food additives, approved a bacteriophage

####### mixture that could be sprayed on specific food products to reduce

####### thepresenceofL.monocytogenes. Bacteriophage-based strategies

####### for control of foodborne pathogens have been approved by the

####### FDA for meat and chicken products. In the European Union, a

####### similar product has also been approved, although distinction must

####### be made between food additive (not permitted) and processing

####### aid (permitted).

####### The use of bacteriophages as biocontrol agents of pathogens in

####### foods has been largely reviewed^76 and can follow two strategies.

####### Bacteriophages can be used as a passive treatment where they

####### are added in sufficient quantities to overwhelm all target organ-

####### isms by primary infection. An advantage of this approach is that,

####### since much of the effect is a result of lysis from without, natu-

####### ral resistance due to restriction enzymes present in host bacteria

####### will not be an issue. Lysis from without occurs when a sufficiently

####### high number of phage particles adhere to the target cell. Lysis of

####### the cells then occurs in absence of phage replication due to alter-

####### ation of the membrane electric potential, and/or the activity of cell

####### wall degrading enzymes. Bacteriophages can also be used as an

####### active treatment where bacteriophages are actively replicating. A

####### relatively small dose of bacteriophages may be required for effi-

####### cacious elimination of the undesirable bacteria, as most bacteria

####### are killed by secondary infections due to replication and trans-

####### mission from neighbouring organisms. Since phages are relatively

####### robust and can be administered via feed or drinking water, they

####### are attractive candidates for control purposes, once the necessary

####### treatment conditions have been established. The use of bacterio-

####### phages against the proliferation of pathogenic bacteria in foods

####### is diverse. In primary production, research on preslaughter treat-

####### ment of food animals has demonstrated bacteriophage control

####### of salmonellosis in chickens, enteropathogenicE. coliinfections

####### in calves, piglets, and lambs, andE. coliO157:H7 shedding by

####### beef cattle.^77 Lytic bacteriophages have been shown to decrease

####### SalmonellaandCampylobacter contamination on chicken skin.^78 ,^79

####### Bacteriophages can be used to prevent and treat colibacillosis in

####### poultry, suggesting that this approach may provide an effective

####### alternative to antibiotic use in animal production.^80 In the same

####### way, the use of bacteriophages to reduce intestinal carriage ofS.

####### Enteritidis orS.Typhimurium in artificially challenged chicks has

####### been investigated by several research groups.^81 ^84 During food

####### processing, bacteriophages have also been applied to control the

####### growth of pathogens such asL.monocytogenes,Salmonellasp. and

####### Campylobacter jejuniin a variety of refrigerated foods such as fruit,

####### dairy products, poultry, and red meats.^77 Immobilised bacterio-

####### phages as bioactive packaging materials to control the growth of

####### L. monocytogenesandE. coliO157:H7 have also proven to be an

####### effective strategy to control pathogen development in foods.^85

####### The utility of bacteriophage tailspike proteins (Tsps) instead of

####### wholephageswasalsoexamined.^86 Amongthebest-characterised

####### Tsps is that from thePodoviridaeP22 bacteriophage, which recog-

####### nises the lipopolysaccharides ofS. entericaserovar Typhimurium.

####### Administered orally to chickens, P22Tsps significantly reduced

####### Salmonellacolonisation in the gut and its further penetration into

####### internal organs. Although some reduction inSalmonellacolonisa-

####### tion was observed, the effect was generally small. These results are

####### promising in terms of opening novel Tsps-based oral therapeutic

####### approaches against bacterial infections in animals.

####### The use of bacteriophages as biocontrol agents is complicated

####### by factors such as an apparent requirement for a threshold level

####### of host (bacteria) before replication, whether bacteriophages are

####### able or unable to protect against recontamination of food with

####### bacterial pathogens, possible resistance in bacterial pathogens

####### (bacteriophage resistant mutants) and labelling issues (from a

####### consumer perspective).

####### Future research will need to focus on assessing the persis-

####### tence of bacteriophage in foods, and their ability to prevent

####### recontamination with bacterial pathogens. Research on specific

####### bacteriophagepathogenfood combinations is needed. In addi-

####### tion, there is need for better knowledge of phage replication kinet-

####### ics and the influence of factors such as inoculum size and timing of

####### the treatment.

####### If bacteriophages treatments are to be used commercially, for

####### removal of surface contamination of foods of animal origin or for

####### reduction of pathogens on food surfaces, then it is recommended

####### that a Guidance Document on the submission of data for their

####### evaluation is provided.

####### Quorum sensing control of pathogenic bacteria in foods

####### Quorum sensing (QS), or cell signalling, is a well-established phe-

####### nomenon that coordinates bacterial behaviour through the pro-

####### duction of small signal molecules, known as auto-inducers.^87

####### QS regulates many different bacterial activities including surface

####### attachment, biofilm formation, expression of virulence factors

####### and secondary metabolite production. Some of the QS regu-

####### lated microbial activities are involved in food spoilage and sur-

####### vival of pathogens within the food matrix and many of the bac-

####### terial species found in food are capable of producing and/or

####### detecting signalling molecules.^88 ,^89 Traditionally, QS enables bac-

####### teria to sense the population size in a local environment and

####### respond by altering gene expression. A classic example is the

####### Staph. aureus agrquorum sensing system. It orchestrates the

####### timely production of virulence factors with the early expression

####### of those needed for adhesion while the production of toxins

####### and other tissue degrading enzymes is restricted to the station-

####### ary growth phase.^90 While for a long timeagrwas believed to

####### be confined to staphylococci, homologues have been demon-

####### strated more recently in other Gram-positive organisms including

####### L. monocytogenes. Also in this organism theagrsystem controls

####### the expression of a number of central virulence genes.^91 Similarly

####### J Sci Food Agric2014; 94 : 30793089 2014 Society of Chemical Industry wileyonlinelibrary.com/jsfa

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####### http://www.soci.org K Jordanet al.

####### toStaph. aureus, the induction of the QS system requires the pro-

####### duction and secretion of an auto-inducing peptide and sensing of

####### its presence by a two-component signal transduction system.^92 In

####### addition to virulence gene expression, theagrsystem influences

####### biofilm formation. Accordingly, expression of theagrgene prod-

####### ucts depended on the stage of biofilm development, as the levels

####### are lower during initial attachment than during biofilm growth.^93

####### agrmay even be important for survival during food processing as

####### it has been associated with tolerance to high pressure.^94

####### In addition to the species-specific quorum sensing systems, a

####### global QS system was discovered some years ago with the poten-

####### tial of communicating across species barriers.^95 Important in the

####### system is the production of theluxSencoded autoinducer 2 (AI2)

####### signal molecule that is sensed in a traditional manner byVibriohar-

####### veyibut is recognised in less well-known ways by other bacteria.^95

####### luxSalleles have been found in many food associated bacteria

####### includingL. monocytogenes,C. jejuniand enterohaemorrhagicE.

####### coli.^95 ^99 Interestingly,luxSseems to be a negative regulator of

####### biofilm formation as deletion ofluxSgreatly enhances the ability to

####### form biofilm.^96 ,^99 This property may be related to the finding inC.

####### jejuniwhere the gene was one of only a few that was differentially

####### expressed in chicken juice compared to broth medium.^100

####### Biocontrol strategies that exploit bacterial QS are based on a

####### number of different classes of molecules (QS inhibitors) that block

####### quorum sensing, including enzymes that degrade the signal, sig-

####### nal analogues and signal antagonists as well as the use of naturally

####### derived signal molecules to stimulate an inappropriate response

####### leading to cell death.^101 ^106 Several of these molecules have been

####### derived from plants commonly used in the food industry. Extracts

####### of garlic have been shown to block QS byPseudomonas aerug-

####### inosa, in a cystic fibrosis mouse model, limiting the production

####### of biofilm and thereby aiding clearance of the bacteria.^107 Sim-

####### ilarly, vanilla extracts have been demonstrated to interfere with

####### QS ofChromobacterium violaceum, suggesting that the consump-

####### tion of vanilla-containing foods may be beneficial.^108 Another food

####### additive that exhibits QS inhibiting property is cinnamaldehyde.^109

####### Interestingly, a compound was recently isolated fromLactobacillus

####### reuterithat interferes withagrquorum sensing inStaph. aureus.^110

####### Compounds have also been isolated from lactic acid bacteria like

####### L.acidophilusand other bacteria such asBifidobacteriumthat inter-

####### fere with luxS mediated quorum sensing and down-regulate viru-

####### lence genes in a variety of enteric pathogens.^111 ^115

####### Importantly, this finding suggests that traditional quorum sens-

####### ing systems respond to signals produced by other species and that

####### lactic acid bacteria in general could be producers of compounds

####### able to interfere with QS systems.

####### Some studies suggest that QS systems are substrate- and

####### most probably organism-dependent.^116 Furthermore, not all QS

####### inhibitors are able to block QS systems and prevent food spoilage.

####### Some QS inhibitors were also shown to be able to decrease prote-

####### olytic activity ofPectobacterium, but their activity did not prevent

####### spoilage of bean sprouts by these bacteria.^117 Furthermore, garlic

####### extract did not prevent spoilage of bean sprouts byPectobac-

####### teriumbut rather appeared to induce it. It is clear that spoilage is

####### multi-factorial, with other regulatory pathways involved.

INDIRECT MICROBIAL CONTROL

OF PATHOGENS

####### Control of pathogens along the food chain is also possible by

####### using adequate management practices and hygiene rules, espe-

####### cially at primary production. The use of prebiotics, antimicrobial

####### peptides and microbially produced enzymes can favor microbial

####### antagonism by creating the good conditions for microbial activity

####### against pathogenic bacteria.

####### Influence of management practices and hygiene levels

####### in animal housing on microbial antagonisms

####### Improved management practices can influence the animal gut

####### microflora and help to control pathogenic bacteria. There are

####### many and varied management practices used across the world,

####### from intensive indoor rearing to extensive largely outdoor rear-

####### ing. In Europe, there is a clear trend towards improved welfare of

####### farm animals.^118 Therefore, in the pig industry for example, out-

####### door green and more sustainable production systems are again

####### being used and in some cases integrated with intensive indoor

####### housing.^119 This may have a dual effect on the health of the ani-

####### mals. On the one hand, outdoor reared animals may possess a

####### more complex microflora and therefore may be naturally more

####### resistant to infections. However, such pigs have increased con-

####### tact with potentially pathogenic microorganisms from the envi-

####### ronment, which can be (re)-introduced to intensive indoor hous-

####### ing systems. The right balance between outdoor and indoor pig

####### production systems in terms of impact on the complexity of their

####### microflora, gut physiology and immune system development is

####### therefore a critical issue.

####### Another management practice consists of the all-in, all-out

####### method of livestock production. This is a system used to replace

####### the (older) technique of having a constant stream of pigs mov-

####### ing through the farm. Instead of having a range of ages, all ani-

####### mals with similar characteristics are designated into a single

####### cohort and are housed together in one shed. Mixing with animals

####### from other cohorts and cross-infection between groups are pre-

####### vented. In this context, segregated early weaning identifies the

####### sow as an important source of pathogens. If piglets are weaned

####### early, they are less likely to come into contact with pathogens from

####### their mothers. However, care must be taken not to create welfare

####### problems by weaning animals too early.

####### Vaccination (by microbially produced vaccines) is used as a man-

####### agement practice to offer protection against certain pathogens,

####### such as enterotoxigenicE. coliand various mycoplasma infections

####### in poultry.^120

####### However, one of the major drawbacks to all these management

####### practices is the substantial cost involved. In Australia and the

####### US, many of the farms are very large by European standards, so

####### they can afford to implement these measures. However, some

####### EU farmers have started to adopt infection control methods, in

####### particular all-in, all-out husbandry.

####### Prebiotics at primary production

####### Prebiotics are defined as indigestible carbohydrates, mostly with a

####### relativelyshortchainlength,thatcanbefermentedinthedigestive

####### tract. Used as a feed additive, they can have a beneficial effect on

####### the intestinal milieu of the host, and can affect directly or indirectly

####### the composition of the gut microflora. On the one hand, they can

####### selectively stimulate the growth/activity of one or a limited num-

####### ber of bacteria in the small and large intestine, such asBifidobac-

####### teriumspp. andLactobacillusspp.^74 ,^121 ^123 On the other hand,

####### they can have a suppressive effect on invading pathogens.^124 The

####### microbial fermentation of indigestible carbohydrates leads to the

####### release of organic acids in the gastro-intestinal tract. The acidifica-

####### tion is mainly explained by lactic acid and short-chain fatty acids,

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####### Microbial control of pathogens in the food chain http://www.soci.org

####### especially acetate, propionate and butyrate.^125 Prebiotics, in addi-

####### tion to influencing the microflora, can have an effect on the intesti-

####### nal and general immune system^126 and gut morphology.^127 ,^128

####### Therefore, effects of prebiotics are likely to be similar to those of

####### probiotics.

####### Various carbohydrates, such as fructo-oligosaccharides (e.g.

####### inulin and oligofructose), galacto-oligosaccharides, xylo-

####### oligosaccharides, polydextrose and lactulose can be used as

####### prebiotics, but mannan-oligosaccharides (MOS) are currently the

####### only in-use prebiotic obtained from microorganisms.

####### MOS, from yeast cell walls ofSaccharomyces cerevisiae,are

####### widely used in animal feed. Meta-analyses and holo-analyses

####### of trials with broiler chickens have shown that MOS fed broil-

####### ers exhibit significantly greater weight gain, improved feed con-

####### version, and lower mortality.^129 ^131 Few studies have addressed

####### the mechanisms underlying these performance parameters. The

####### addition of MOS can have a beneficial impact on the pH, bac-

####### terial population, nutrient digestibility and morphology of the

####### gastro-intestinal tract.^123 ,^124 ,^127 ,^132 ^138 Studies in the presence and

####### absence of a pathogen challenge have shown that MOS can influ-

####### ence blood characteristics, immune response and can modulate

####### gene expression.^127 ,^132 ,^139 ^143

####### Compared to other prebiotics in use, MOS have the ability to

####### agglutinate type-1-fimbriae pathogens likeE. coli.^134 ,^144 ,^145 This

####### outstanding effect can be traced to the fact that mannose, found

####### on most mammalian cell surfaces, and its polymer, the plant

####### polysaccharide mannan known to be contained in the yeast cell

####### surface, act as receptor for binding of Enterobacteriaceae, such as

####### E. coliandSalmonellaspp.^145 ^147 Pathogenic bacteria that display

####### mannose/mannan-specific fimbriae can therefore be removed

####### from the gastro-intestinal tract by blocking of adhesins on the cell

####### surface of pathogens, which prevents them from binding to and

####### colonising the intestinal wall and, thus, from initiating an enteric

####### infection.^144 ,^148 ,^149

####### In general, the results of prebiotic supplementation are incon-

####### clusive for livestock animals. Significant effects on microorganisms

####### of the digestive tract were not always clearly described. This vari-

####### ability in the results obtained can be explained by the interaction

####### with other food ingredients, the composition of the endogenous

####### intestinal microbiota and general hygiene factors.

####### The combination of a prebiotic and a probiotic in one product

####### (synbiotics) has been shown to confer benefits beyond those of

####### either the pre- or probiotic on its own.^150 Such synbiotic combina-

####### tions may prove to be the next step towards reducing the risk of

####### intestinal diseases and eliminating specific microbial infections in

####### animals.

####### Antimicrobial peptides

####### Antimicrobial peptides are polypeptides of approximately 100

####### amino acids, water soluble, and broad-spectrum antibiotics that

####### are present naturally in microorganisms, plants, and animals, such

####### as defensins.^151 These antimicrobial peptides have the capacity to

####### kill or inactivate a particular spectrum of bacteria, fungi, and some

####### enveloped virusesin vitro^152 and can improve the growth per-

####### formance, increase the intestinal ability to absorb nutrients, and

####### improve the mucosal immunity of the intestine in chicken.^153 How-

####### ever, under current legislation the use of antimicrobial peptides is

####### not permitted in animal nutrition.

####### Microbially produced feed enzymes

####### Particular functional feed ingredients and additives are known to

####### haveamodulatingeffectonmicrofloracompositionandpathogen

####### susceptibility in livestock, improving livestock performance, feed

####### efficiency and animal health. These include in-feed enzymes,

####### organic acids, medium chain fatty acids and plant extracts and

####### essential oils.^154

####### Microbially produced in-feed enzymes are routinely added to

####### livestock feeds and work by helping to break down certain com-

####### ponents of the feed, such as -glucans, proteins and phytates, that

####### are difficult for the animal to digest, or that act as antinutritional

####### factors.^155 The most commonly used in-feed enzymes, applicable

####### as functional feed ingredients, are -glucanase, xylanase, phytase

####### and -mannanase. Most enzymes are produced as fermentation

####### productsfromfungiandbacteriaandareveryeffectiveatmaximis-

####### ing feed conversion efficiency with very few drawbacks. As a result,

####### research is focussed on improving the quality of existing enzymes,

####### by broadening the range of substrates such as by-products from

####### the food chain with potential in animal feed or by increasing

####### their stability during feed processing (such as high temperature

####### and pressure during pelletising).^156

CONCLUSIONS

####### Microbial antagonism has great potential to improve safety in the

####### food chain and thus reduce the associated public health risk. Cur-

####### rently, this potential has been confined, for the most part, to labo-

####### ratoryexperimentsandlimitedexperimentaltrials.Althoughsome

####### commercial products are available, the true potential of microbial

####### antagonism for food safety improvement has yet to be realised.

####### As mechanisms of action are further investigated and understood,

####### use of microbial antagonism will become more widespread in its

####### use. It is noteworthy that the combination of these treatments

####### along the food chain and in foods can help to improve the control

####### ofpathogensandcontributetotheproductionofsaferfoods.^157 ,^158

####### Besides control of pathogens by means of microbial antagonism,

####### new perspectives are also being offered by the use of essential oils

####### containing antimicrobials like phenols (catechins and carvacrol)

####### for the production of safe foods.^159 ,^160

ACKNOWLEDGEMENTS

####### This work was supported by the European Union 7thFrame-

####### work Programme under the projects FOODSEG (project number

####### 266061) and PROMISE (project number 265877).

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