Food Safety - New Food Magazine...Drug resistance in Campylobacter can confer enhanced food safety hazards, disease burden and economic costs in several distinct ways: ... water and

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www.newfoodmagazine.com 1 New Food, Volume 18, Issue 1, 2015

2 The drugs and bugs inyour birds: Food safetyimplications of antibiotic resistance in CampylobacterSophia Kathariou and Hannah Bolinger, North Carolina State University Dept of Food, Bioprocessing & Nutrition Sciences

7 Zoning classification in the food processing area François Bourdichon, Food Safety Consultant

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Humans with campylobacteriosis experience acute gastroenteritis withdiarrhea, cramping, abdominal pain and fever, generally recoveringwithin 5-7 days. However, a subset of patients can experience severeautoimmune sequelae such as arthritis and, in an estimated one of every1,000 cases Guillain-Barré syndrome, a form of paralysis that can require

months before resolution and leave life-long disability. Consumptionand handling of undercooked poultry is one of the most commonlyimplicated transmission routes for the disease1,2.

Up to 80% of poultry flocks at slaughter are positive forCampylobacter3. Although poultry-derived Campylobacter can make

The bacterium Campylobacter, especially C. jejuni and C. coli, is a leading cause of human foodborne illness and amajor concern for the poultry industry. In 2012, C. jejuni was the second most commonly reported bacterial foodborne illness and was found to be more frequent in that year than in the period from 2006-2008. But what do we knowabout antibiotic resistance in Campylobacter that can inform food safety measures?

The drugs and bugs in your birds: Food safetyimplications of antibioticresistance in Campylobacter

New Food, Volume 18, Issue 1, 2015 2 www.newfoodmagazine.com

F O O D S A F E T Y S U P P L E M E N T

■ Sophia Kathariou and Hannah Bolinger North Carolina State University Dept of Food, Bioprocessing & Nutrition Sciences

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humans sick, the birds themselves typically do not exhibit signs of illness.Growers and inspection agents cannot tell which birds do or do notharbour the bacteria without laboratory testing. Campylobacter iscarried in the intestinal tract (especially the cecum) of chickens andturkeys at levels as high as one billion viable bacterial cells per gram ofcecal content4. Poultry carcasses become contaminated duringslaughter and processing and human illness can result followingingestion of as few as 400-500 bacteria5.

Once Campylobacter enters a poultry house and some birds becomecolonised, further transmission within the flock is rapid and extensivedue in part to the close quarters and shared space within the poultryhouses (see Figure 1, page 4)6. Within-flock transmission is primarily viaingestion of faeces (coprophagy) or litter, feed and water contaminatedwith freshly excreted faeces.

What is the source of Campylobacter for the poultry industry pre-harvest? The ecology of this pathogen is complex and still poorly understood, but the following have been frequently implicated:� Insect vectors, primarily flies and darkling beetles� Other farm animals (e.g. poultry, cattle, swine) in the vicinity� Compromised biosecurity, resulting in farm employees, visitors and

equipment tracking bacteria from one contaminated site and farmto another

Growers and farm personnel should be aware of their potentialimportance in keeping a flock Campylobacter free. For instance,Campylobacter can survive in water for various lengths of time, especiallyat low temperatures, and one might easily track Campylobacter into thepoultry house from water puddles outside. Putting on single-use plasticover boots just before entering the poultry house may be helpful inminimising exposure to Campylobacter, and plastic over boots should bechanged between poultry houses in case the birds in just one house areinfected. Additionally, tools and equipment should always be cleanedand sanitised before being taken into a different house.

Antibiotic resistance in CampylobacterIn 2013, the Centers for Disease Control and Prevention (CDC) released alist of antibiotic-resistant microbes that are major threats to humanhealth. Drug-resistant Campylobacter was listed as a pathogen 'with athreat level of serious’, with approximately one quarter of theCampylobacter infections reported each year in the US being attributedto drug-resistant strains.

Human Campylobacter infections are typically self-limited andresolve without the need for antibiotic treatment. However, antibiotictreatment may be indicated for certain patients, e.g. those with invasiveillness and high risk individuals such as infants, the elderly and HIVpatients. In such cases, fluoroquinolones (e.g. ciprofloxacin) andmacrolides (e.g. azithromycin or erythromycin) are drugs of choice.However, ciprofloxacin resistance has become frequently encounteredin Campylobacter7. Fortunately, incidence of macrolide resistance in C. jejuni has remained low, ensuring continued therapeutic effectivenessof these antibiotics.

The emergence of ciprofloxacin resistance in Campylobacter fromhuman cases in the US temporally coincided with the approval of

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New Food, Volume 18, Issue 1, 2015

fluoroquinolones (specifically enrofloxacin, closely related tociprofloxacin) to control poultry diseases. A review article by Nelson et al.(see suggested reading) highlights two studies that found increasingCampylobacter isolates with resistance tofluoroquinolones. From 1990 to 1999, theprevalence of fluoroquinolone resistantCampylobacter increased from 0% to 18%. Theother study found no resistant Campylobacterisolates during the years of 1982-1992, but afterthe introduction of fluoroquinolones into thepoultry industry in the early 1990’s there was ajump up to 41% in 20018. Such findings led to an eventual government-mandated ban in 2005 of fluoroquinolone use in poultry pre-harvest.

What are the public health and food safety concerns relatedto drug resistance in Campylobacter?Drug resistance in Campylobacter can confer enhanced food safetyhazards, disease burden and economic costs in several distinct ways:1. Resistance to drugs of choice for treatment of human campylo -

bacteriosis can compromise treatment outcomes for those patientsfor whom treatment may be indicated.

2. Drug resistance may be associated with higher disease burden. Forinstance, drug-resistant strains may result in longer lasting illnessthan strains lacking resistance7. It is also possible (but not yetdemonstrated) that additional pathogenicity attributes areimpacted in drug-resistant strains. Possible outcomes might include lower numbers required for human infection and moresevere symptoms.

3. Drug resistance may also confer enhanced ability to colonise birds,thus increasing prevalence of Campylobacter in the food supply.

In certain strains of C. jejuni, ciprofloxacin resistance wasaccompanied with higher ability to colonise the intestine ofchickens9. On the contrary, and as a fortuitous public health boon, in

C. jejuni acquisition of macrolide resistanceresults in impaired overall fitness and birdcolonisation potential10, thus contributing to the continuing low prevalence of suchresistance in C. jejuni and ensuring effectivenessof macrolides as drugs of choice whentreat-ment of human illness is indicated. 4. Drug-resistant strains may be more able to

survive in vectors and environments relevant to transmission andfoodborne disease risks, including excreted faeces, water, insectsand protozoa. Survival may be also impacted on raw poultry, inwater and milk, and on utensils, surfaces and equipment in thekitchen, food processing and food service environments.Appropriately designed studies are needed to characterise fitnessimpacts such as these and those listed in point five.

5. Drug-resistant strains may have enhanced ability to tolerate abioticstresses such as ambient oxygen (Campylobacter is an obligatemicroaerophile), sub-optimal temperature, dehydration, exposureto disinfectants or other treatments.

In addition to ciprofloxacin, resistance is commonly encountered toseveral other antibiotics11. Figure 2 shows 15 turkey derived C. jejuni andC. coli isolates grown with and without specific antibiotics. It is evidentthat different isolates exhibit different antibiotic susceptibility profiles.

How does Campylobacter acquire resistance to antibiotics?There are numerous methods by which Campylobacter can acquire



Figure 1: Turkey house showing the closeproximity of the birds, which serves to facilitatetransmission of Campylobacter through a flock

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Once Campylobacter enters apoultry house and some birds becomecolonised, further transmission withinthe flock is rapid and extensive due inpart to the close quarters and sharedspace within the poultry houses

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resistance to an antibiotic. An innate system to pump outantibiotics (the multi-drug resistance efflux pump CmeABC)has been extensively characterised in Campylobacter for itsmultiple roles not only in drug resistance but numerous otheradaptations as well. This intrinsic ability of Campylobacter topump harmful compounds out of the cell provides it withbaseline resistance to a number of antibiotics and other toxiccompounds. At higher doses, a drug can overcome the pump’sability to get rid of the compound and additional dedicatedmechanisms will be required for resistance11,12. However, inCampylobacter the simple presence of dedicated resistancedeterminants may not be sufficient for high levels of resist-ance to the corresponding antibiotics, unless a functional,intact CmeABC efflux system is also present.

Resistance mechanisms vary depending on the antibiotic.For instance, resistance to macrolides (e.g. erythromycin) andfluoroquinolones is typically conferred by simple single-basemutations in the sequence of pre-existing chromosomal genes(the 23S rRNA gene and the gene encoding DNA gyrase,respectively). Poultry can carry extremely high levels ofCampylobacter. This means each bird can carry billions of cellsand there are generally thousands of birds in each flock. Eachone of those bacterial cells has the potential to undergo amutation that would lead to macrolide or fluoroquinoloneresistance. Once established in one strain, such mutations can bedisseminated to others via natural transformation: as cells harbouringthe mutation propagate and die they release DNA which becomes takenup by other Campylobacter cells in the vicinity, with the potential for

the mutated sequence to replace the previous wild type gene.Campylobacter is well known for its propensity to acquire DNA via suchnatural transformation.

Such mutation and gene replacement events take place at various


Figure 2: Campylobacter spp. on Mueller-Hinton agar plates with a) no antibiotic; b) 8µg/mlerythromycin; c) 16µg/ml tetracycline; d) 4µg/ml ciprofloxacin.

frequencies, but the presence of the relevant antibiotic can constitute a powerful selection pressure, with the resistant version of the geneeventually predominating in the population. Potential impacts onanimal colonisation can constitute alternative selection pressures, as may be the case with ciprofloxacin resistance in certain C. jejunistrains: if resistant strains with the mutantversion of the DNA gyrase gene have enhancedcapacity to colonise the chicken intestine theywill eventually out-compete their wild typeparental counterparts.

Resistance can also involve acquisition ofnew genes, frequently from other bacteria. For instance, tetracyclineresistance is typically mediated by a specific gene, tet(O), which appearsto have been originally acquired from other bacteria (likelyEnterococcus), but now seems to have infiltrated the genome of moststrains of C. jejuni and C. coli from an agricultural source13. This gene isfrequently harboured on autonomously replicating genetic elements(plasmids), though integration into the chromosome has also beendocumented. Again, stable integration of the resistance gene in thechromosome opens the way for subsequent dissemination to other

Campylobacters via natural transformation. In contrast, genes onplasmids become disseminated not by transformation, but insteadprimarily via transfer of the plasmid during conjugation: direct cell to cellcontact between a live donor cell (which harbours the plasmid) and a liverecipient cell (which will acquire the plasmid).

Mutations in pre-existing genes andacquisitions of new resistance genes areexpected to take place all the time, withfrequencies dependent on environmentalconditions, the genetic attributes of the strainsinvolved and the composition of the microbial

community in which Campylobacter finds itself. Selective pressure fromthe use of antibiotics is not a requirement for emergence of theresistance attributes. If antibiotics are used however, the resistanceattributes will confer a powerful selective pressure in favour of the cellsharbouring the resistance determinant. As discussed above, similarselective pressures can accrue from fitness impacts of the resistance (e.g. to colonisation or environmental persistence).

Concluding remarks The issue of antibiotic resistance in Campylobacter and other zoonoticfoodborne pathogens is complex, with diverse sources for resistance andmultiple factors determining the persistence of resistant strains.Agricultural and human uses of antibiotics are two major sources ofselective pressure for resistance, with great potential for interventionsinvolving reduced and judicious antibiotic use both in the farm and in theclinic. However, selection acts at the level of not only the entire microbialcell but also the entire population and the entire microbial communitiesof which Campylobacter and other pathogens are but members.

In the face of reduced antibiotic exposure or even complete absenceof drug use, the fate of established or newly emerging (e.g. via mutationand gene acquisition events) populations of resistant strains will be shaped by those strains’ fitness trajectories, to which resistance itself may make important contributions. The case of the 2005fluoroquinolone ban in poultry is a poignant example: no markedreductions are yet seen in prevalence of fluoroquinolone resistance in poultry-derived Campylobacters. However, would this not be expected, if the resistant strains had higher ability to colonise birds andto survive, persist and disseminate in the farm ecosystem? Research that further characterises these fitness trajectories of resistant strains is clearly needed for better estimates and predictions of theorganisms’ persistence and ecological success in agriculture and inhuman disease.



1. Centers for Disease Control and Prevention (CDC) (2014). National Center for Emerging andZoonotic Infectious Diseases. Campylobacter [Accessed: December 20, 2014].http://www.cdc.gov/nczved/divisions/dfbmd/diseases/campylobacter/#what.

2. Centers for Disease Control and Prevention (CDC) (2012). Trends in Foodborne Illness in theUnited States, 2012 [Accessed: December 23, 2014]. http://www.cdc.gov/features/dsfoodnet2012/.

3. Hermans, D et al. (2012). Poultry as a host for the zoonotic pathogen Campylobacter jejuni.Vector Borne Zoonotic Dis. 12(2):89-98. doi: 10.1089/vbz.2011.0676. Epub 2011

4. Humphrey, S et al. (2014). Campylobacter jejuni is not merely a commensal in commercialbroiler chickens and affects bird welfare. MBio. 5(4): doi: 10.1128/mBio.01364-14

5. Food and Drug Administration (2012). Campylobacter Jejuni. In Bad Bug Book, FoodbornePathogenic Microorganisms and Natural Toxins, pp. 14-17.

6. Adkin, A, Hartnett, E, Jordan, L, Newell, D, Davison, H ( 2006). Use of a systematic review toassist the development of Campylobacter control strategies in broilers. J Appl Microbiol.100(2):306-15.

7. Centers for Disease Control and Prevention (CDC) (2013). Antibiotic Resistance Threats in TheUnited States [Accessed 20, 2014]. http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf#page=49

8. Nelson, JM, Chiller, TM, Powers, JH, Angulo, FJ (2007). Fluoroquinolone-resistantCampylobacter species and the withdrawal of fluoroquinolones from use in poultry: a publichealth success story. Clin Infect Dis. 44(7):977-80.

9. Luo, N et al. (2005). Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacterjejuni in the absence of antibiotic selection pressure. Proc Natl Acad Sci USA. 102(3):541-6.

10. Luangtongkum, T (2012). Impaired fitness and transmission of macrolide-resistantCampylobacter jejuni in its natural host. Antimicrob Agents Chemother.56(3):1300-8. doi:10.1128/AAC.05516-11.

11. Ge, B, Wang, F, Sjölund-Karlsson, M, McDermott, PF (2013). Antimicrobial resistance inCampylobacter: susceptibility testing methods and resistance trends. J Microbiol Methods.Oct;95(1):57-67. doi: 10.1016/j.mimet.2013.06.021. Epub 2013 Jul 1

12. Guo, B, Lin, J, Reynolds, DL, Zhang, Q (2010). Contribution of the multidrug efflux transporterCmeABC to antibiotic resistance in different Campylobacter species. Foodborne Pathog Dis.Jan;7(1):77-83. doi: 10.1089/fpd.2009.0354

13. Taylor, DE, Hiratsuka, K, Ray, H, Manavathu, EK (1987). Characterization and expression of acloned tetracycline resistance determinant from Campylobacter jejuni plasmid pUA466. J Bacteriol. 169(7):2984-9.

Suggested Reading:• Nelson, JM, Chiller, TM, Powers, JH, Angulo, FJ (2007). Fluoroquinolone-resistant

Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a publichealth success story. Clin Infect Dis. 44(7):977-80.

• http://www.fda.gov/food/foodborneillnesscontaminants/causesofillnessbadbugbook/ucm070024.htm

• http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf#page=49

References

Sophia Kathariou is a professor at North Carolina StateUniversity. Her laboratory researches the adaptation, evolutionand ecology of bacterial foodborne pathogens, especiallyListeria and Campylobacter.

Hannah Bolinger is a PhD student in the Food Science program at North Carolina State University. She is interested inthe application of molecular techniques to real life solutions in food policy.

About the Authors

Growers and farm personnel shouldbe aware of their potential importance inkeeping a flock Campylobacter free

Zoning is the distinct division of a facility into process areas with differenthygiene levels. Appropriate zoning of process areas with its barriers andcleaning procedures is designed to protect products from potentialhazards originating in the factory environment and its surroundings.Zoning is an important prerequisite of HACCP plans. The appro-priate zoning of process areas with its barriers has to be designed toprotect each type of product and its consumers and prevent contamina -tion according to potential hazards as defined by the HACCP study.

But which hazards should be addressed? While zoning is commonly

implemented to prevent pathogen contamination, this is not the solehazard to be considered. Allergen management, pest control and foreignmatter management also require a proper zoning approach. Addition -ally, depending on food product composition, the process, and thepathogen and spoilers of concern, cleaning practices are also different between food operation factories, even within the same factory. A cheese manufacturing site, chilled and wet, with Listeriamonocytogenes as a pathogen of concern in the environment does notundergo the same sanitation schedule as a confectionary site, which is a

A food processing area is commonly segregated for technological and hygiene purposes and so the design is meant toobtain production in the most economically achievable hygienic conditions. The rationale for plant design has beencontinuously challenged in recent years by a risk mitigation approach to put all identified hazards under control, to correct initial design of factories when those hazards were unknown or ignored and to promote ‘hygienic design in new factories.

Zoning classification in the food processing area

www.newfoodmagazine.com 7 New Food, Volume 18, Issue 1, 2015


■ François BourdichonFood Safety Consultant

low moisture food production environment with Salmonella spp. as thepathogen of concern.

At least four criteria can define a spot within a processing site: highrisk zone, soy free, controlled and cleaned, and non-food contactsurface. As for cleaning tools, these must be identified to be compliantwith those four criteria as well. Zoning classification is not always simple!

Zoning in the ISO 22002 Food Safety Management System standardZoning is defined by ISO in the 22002 Part 1 (2009) Standard1 as ‘thedemarcation of an area within an establishment where specificoperating, hygiene or other practices may be applied to minimise thepotential for microbiological cross-contamination’. The recent version 7of the BRC Standard2, Appendix 2 – Guidelines on defining production

risk zones, proposes ‘a classification of risk zones within the processingand storage facilities, with corresponding levels of hygiene andsegregation to reduce the potential for product contamination’.Separation is made between open product areas, enclosed productareas (e.g. warehouses and storerooms) and non-product areas (e.g. canteens, laundries and offices). More specifically, open productareas are classified as: high risk (chilled and frozen), high care (chilled andfrozen), ambient high care and low risk.

While reminding that factory hygiene, finish of buildings, equipment,protective clothing and staff hygiene should reflect the potential risks tothe product, the proposed decision tree only focuses on pathogencontamination potential, not spoilers orallergens. For example, raw meat intended to becooked before consumption would be classifiedin a low risk area, where it is still reasonable toexpect raw meat, to be cooked or not, to behygienically operated to ensure it is not spoiledbefore cooking.

Pathogen management is more complicated and highly related to the production type and its specific risks. For example, on the proposalof the Working Group for Machinery and Equipment in the ConfectioneryIndustry, zoning can be commonly separated, regardless of dry or wetzones in the following scheme3: � Zone 0: Reception/storage/processing of open products with strong

microbiological contamination

� Zone 1: Reception/delivery/storage/processing of packed product inareas with strong contamination risks

� Zone 2: Storage/processing of packed products/secondarypackaging areas, storage of packed raw material/storage of liquidsin closed systems

� Zone 3: Low moisture foods: Storage/processing of open semi-finished products and unpacked end products

� Zone 4: Wet products: Open processing of microbiologically sensitive products

Design and layoutProper hygienic design and layout of premises and rooms are essentialto ensure that entry of hazards (pathogens, spoilers, allergens) into theestablishment is controlled (e.g. minimising the potential for entry and,

in the case of entry, preventing the hazardfrom becoming established in the environ -ment through proper design and cleaningprocedures). Physical separation within the food establishment based on specifichygiene requirements will help minimisetransfer from one area to another, usingphysical barriers, such as walls, doors, splitconveyers, air filters etc.

Alternatively, separation of areas andcontrol of dust can also be achieved by theappropriate design of ventilation systems andairflow. Overhead structures should bedesigned to minimise the accumulation ofdust and dry materials, especially when they are directly above exposed products.

Panels, walls, and floors, should be designed to eliminate hollow areasthat could serve as microbial harbourage sites or accumulation ofallergen residues.

Principles of air handling to zoningThe movement of dust from one area to another should be prevented orminimised using air filters and by maintaining a positive air pressure inthe area requiring a more stringent hygiene control relative to the otherareas in the establishment (Figure 1). Properly designed air handlingsystems control airborne particulates and odours, minimising the risks to products from airborne contamination by pathogens and

spoilage microorganisms4.Irrespective of the air flow rate, care needs

to be taken that the air is moving from high tolow care areas or from low to higher dustloading areas. Attention should also be given tothe location of the air intake for the establish -ment in relation to sources of contamination.

Where air is used in the facility or in processing lines for specific purposessuch as for cooling or transportation of products, direct contact with theproduct is possible and the air quality should be appropriate consideringthe intended consumer of the finished product produced. Processingsites should always aim to work with positive pressure, traditionally F5 filtered air in case of open product areas. Three levels of pressure at least should be considered:



Figure 1: Proposed air handling and cleaning classification for low moisture food production with highlycontaminated material (e.g. almonds, nuts, cocoa, etc.)

While reminding that factoryhygiene, finish of buildings, equipment,

protective clothing and staff hygieneshould reflect the potential risks

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� Highest: Processing zone, high care/highrisk. The airflow shall begin from thehighest level of hygiene to lower, i.e. fromopen air production zones to pack-aged goods

� Intermediate: Storage rooms, rawmaterial, packaging, finished product

� Slightly above 0Pa: Entry areas(personal, goods)

It is quite difficult in some cases to giveprecise values of what correct pressuresshould be but if proper separation betweenzones cannot be obtained, no differential ofpressure can be monitored. Airflow only canbe considered for a low moisture food facilityand should be verified regularly that it fits its purpose.

Cleaning and sanitation proceduresA processing site should not be segre-gated only by the levels of operationalhygiene expected in different areas, but alsoupon different cleaning procedures in place(Figure 2, uses powdered infant formulaproduction as an example), as prerequisiteprograms for pathogen management, if notas a CCP for allergen management (cleaningbeing the only control measure to lower therisk). The type of cleaning practices to be usedin different hygiene areas should be decided upon the hazard analysis to mitigate pathogen contamination.

For low moisture foods like powder, a safe environment is notnecessarily a clean one, as for high moisture food facilities. In thatspecific case, water is the enemy, as it can revive microorganisms presentin ingredients. If not correctly done, cleaning procedures can becounterproductive and enhance risk.

Codex Alimentarius suggests following the definitions for cleaningprocedures based on the amount of water used vs the consideredmicrobiological hazards:� Wet cleaning: The removal of soil, including food residues, dirt,

grease or other objectionable matter using water and detergents� Controlled wet cleaning: The removal of soil, including food

residues, dirt, grease or other objectionable matter using a limitedamount of water

� Dry cleaning: The removal of soil, including food residues, dirt,grease or other objectionable matter by actions such as sweeping,brushing, scraping, or vacuuming the residues from equip-ment surfaces and the food establishment environment without the use of water

The objective of dry cleaning is to remove residues without the use ofwater by using tools or cleaning aids that do not involve the applicationof water or other aqueous solutions, e.g. dry abrasives. Hot oil is

sometimes used to flush the interior of equipment used to handle highviscosity, low moisture products such as peanut butter or chocolate, butit cannot be considered as a sanitation step. Separate tools should beprovided for the dry cleaning of floors. Tools and vacuums that are usedfor cleaning food contact surfaces should not be used to clean non-foodcontact surfaces. Dry cleaning tools should be cleanable, durable,without loose parts, designed for purpose, dedicated to the area, andstored in a dedicated place.

Portable vacuum cleaners are recommended to remove non-fat andnon-viscous residues and should be dedicated to specific areas, to betested as part of an environmental monitoring program. Cleaners shouldbe well maintained so they do not become carriers of contaminationwith their filters properly maintained on a regular basis. While watershould be avoided as much as possible, alcohol-based disinfectantsprovide a means to disinfect equipment. Compressed air can also beused for dry cleaning in special situations (e.g. to dislodge dust frominaccessible points). It then should be dried and filtered to excludemicroorganisms and moisture prior to use.

Controlled wet cleaning procedures should be used when residuescannot be further removed by dry cleaning. Only the minimum amountof water should be used, with specific procedures to collect water toprevent it spreading to other non-wet cleaned areas. As such, wateraerosols and high pressure water systems should not be used. Wherepossible, parts of equipment should be removed and wet cleaning



Figure 2: Proposed zoning for powdered infant food formula. Adapted from Mullane et al. (2007) Int. J. FoodMicrobiol. 116: 73-81.

conducted in a dedicated room. Complete and active drying of all areasand components involved should be done after controlled wet cleaning.

When the product by itself has a high range of moisture, and whenthe production environment must be considered wet, then wet cleaningdoes apply. Water use should yet be minimised and isolated to specificareas wherever possible and complete drying of all areas should be doneafter wet cleaning.

Monitoring effectivenessFood processing establishments should put inplace an environmental monitoring program toverify the effective implementation of zoning to maintain production in a hygienic environ -ment. Environmental monitoring allowsundertaking corrective actions in a timelymanner. The purpose of the monitoringprogram is to find where target organisms are present in theenvironment. Decision criteria and their rationale should be articulatedprior to the establishment of the program, from no action (no risk ofcontamination), to intensified cleaning, tosource tracing (increased environmentaltesting), to review of hygienic practices,holding and testing of product, up to productdisposition. Cleaning procedures should alsobe monitored (e.g. ATP bioluminescencewhere applicable or visual observation) andverified (swabbing for enterobacteriaceae and allergen residues). Cleaning verification isnot environmental monitoring.

While it is reasonably expected to findpositive results out of the swabbing, sincemicroorganisms are ubiquitous in the environ -ment, one has to be able to differentiate thedegree of concern depending on the location.Two approaches are currently proposed in the different guidelines, from the CodexAlimentarius, Health Agencies or professionalsyndicates5-7. The separation is made betweenfood contact surfaces (FCS) and non-foodcontact surfaces (nFCS). Since the early 2000s,a US driven approach suggests four zones foran environment program (confusingly, theterm ‘zone’ is used to describe environmentsas well as areas of hygienic segregation):� Zone 1: Food contact surfaces – Surfaces

in the plant that are in direct productcontact after the lethality or microbialreduction step

� Zone 2: Non-food contact surfaces, Environ -ment E1: Surfaces in the plant closelyadjacent to product contact surfaces

� Zone 3: Non-food contact surfaces,Environment E2: Surfaces in open post-lethality product processing areas, but notclosely adjacent to FCS

� Zone 4: Non-food contact surfaces, Environment E3: Surfacesremote from product contact surfaces outside the processing roombut which could impact processing areas through the movement ofpeople, equipment or materials

Depending of the ecology of the factory and the target consumer, the microbial hazard of concern can be either Listeria monocytogenes in

wet and/or chilled production sites, Salmonellain the environment of low moisture food plants, Cronobacter spp. in infant food plants.Indicators can also be monitored, i.e. germsshowing similar ecological characteristics.Enterobacteriaceae show similar resistance to drying as Salmonella spp. and are morecommon in processing facilities. Consequently,the monitoring of Enterobacteriaceae as

well as Salmonella in the environment may provide an early indication that the conditions necessary for Salmonella colonisationmay exist, and hence provide an earlier indication of potential

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problems8,9. The same approach is valid for Listeria spp. as an indicator for the pathogenic species Listeria monocytogenes. Entero -bacteriaceae are not good indicators for Listeria, but are classicallymonitored in high moisture food facilities for the spoilage and hygieneissues their presence could cause.

Preferential locations for sampling should focus on areas whereharbourage or entry leading to contamination is likely to occur. Samplinglocations should be reviewed on a regular basis and additional ones mayneed to be included in the program, depending on special situationssuch as major maintenance or construction activities or where there isobserved indication of poor hygiene. The frequency of the environmentalmonitoring program should be adjusted according to the findings andtheir significance in terms of risk of contamination. In particular, thedetection of pathogens in the finished product should lead to increasedenvironmental and investigational sampling to identify thecontamination sources. The frequency should also be increased insituations where an increased risk of contamination can be expected,e.g. in case of maintenance or construction activities.

Conclusion – Food for thoughtWhile the cleaning procedures and environmental monitoring detailed inthe present article mostly refer to microbial hazard management forpathogens and spoilers, the approach is similarly valid for allergenmanagement. While segregating a factory for production purposes, onemust consider not only the ecology of the finished products and rawmaterials, but also the ecology of the factory itself, and the consumertarget, either for the stringency expected or specific hazard.

The control measures in place should be properly validated to be fit for purpose, monitored to ensure hygienic and safe production,verified for compliance and regularly reviewed. Zoning might beunderstood as basic and easy to achieve, yet proper care should be taken to avoid recurrent issues from flawed design or in case ofchange of production.



1. ISO/TS 22002-1:2009. Prerequisite programmes on food safety. Food Manufacturing.

2. BRC Global Standard for Food Safety Version 7 (2015). Available at:http://www.brcglobalstandards.com/.

3. Working Group for Machinery and Equipment in the Confectionery Industry.Recommendations for Air-Conditioning in Production and Storage Areas in the ConfectioneryIndustry (04/2002).

4. EHEDG. Guidelines on air handling in the food industry. EHEDG Update / Trends in FoodScience & Technology 17 (2006) 331–336.

5. Almond Board of California (2010). Pathogen Environmental Monitoring Program (PEM).

6. Health Canada (2011). Policy on Listeria in ready to eat foods.

7. United Fresh Produce Association (2013). Guidance on Environmental Monitoring and Controlof Listeria for the Fresh Produce Industry.

8. GMA (2009). Control of Salmonella in Low Moisture Foods, pp 1-81.

9. GMA (2010). Industry handbook for safe processing of nuts.

References

François Bourdichon is a Food Safety and Hygiene Consultantwith 15 years of experience in the food, dairy, infant nutritionand confectionary industries. His work focuses onprerequisites, which are often the forgotten part of the FoodSafety Management System. Without these strong basesproperly implemented, the whole approach cannot be asefficient or resilient as possible. He can be contacted at:[email protected].

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