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Food Microbiology, 1990,7,177-l 98
A Hazard Analysis Critical Control Point Approach (HACCP) to ensure the microbiological safety of sous vide processed meat/pasta product J P. Smith’*, C. Toupin2, B. Gagnon3, R. Voye?, P. P. Fiset4 and M. v’. Simpson’ ‘Department of Food Science and Agricultural Chemistry, McGill University, Ste Anne de Bellevue, Q&bee, 2Agriculture Canada Food Research and Development Center, Ste. Hyacinthe, Q&bee, and 3Agriculture Canada Food Production and Inspection Branch, Ottawa, Ontario, and 4La Tour Eiffel, Montreal, Que’bec, Canada
Received 5 December 1989
Increasing consumer demands for microwaveable, convenience foods with extended shelf life yet retaining %loser to fresh’characteristics, has resulted in thegrowth of sous vide or vacuum cooking processing technology. However, this new generation of minimally processed sous vide products are not shelf stable and pose a potential public health risk if subjected to temperature abuse at any stage of the product’s production, storage, distribution and marketing. To ensure the microbiological safety of sous vide products, a Hazard Analysis Critical Control Point (HACCP) approach is recom- mended at all stages of sous vide processing and distribution of end product. The HACCP approach is a preventive approach to microbiological quality control and is intended to prevent problems before they occur rather than finding them in the finished product. Hazard Analysis identifies the microbiological hazards and potential entry points of these hazards in the sous vide process. Critical Control Points to control the identified microbiological hazards include quality of raw ingredients, time1 temperature relationship, sanitation and packaging control and incorporation of additional barriers, such as pH and water activity (ad reduction, in the formulated product. The practical application ofHACCP to ensure the microbiological safety ofa sous vide processed meat/pasta product are given.
Introduction There has been a tremendous growth, in recent years, in the use of ‘sous vide’ processing (vacuum cooking) technology to extend the shelf life and keeping qua- lity of fresh food. The growth of this tech- nology, and new generation of food prod- ucts, is in response to consumer needs for ready-to-eat, microwaveable, con- venience foods with extended shelf life and yet retaining ‘closer to fresh’ charac-
*Corresponding author
0740-0020/90/030177 + 22 $02.00/O
teristics. With a current market of approximately $20 million per year, sales of sous vide processed products in Canada are projected to triple within the next 10 years, mainly at the expense of frozen and canned food products (Fiset, P. pers. commun.).
Sous vide processing consists of prep- aration (if necessary), packaging in heat- stable, air-impermeable bags under vacuum to remove all the air, sealing, cooking (pasteurization) to a time and temperature for a specific food, cooling,
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178 J. P. Smith et 81.
FRESH, TOP-QUALITY INGREDIENTS
I BASIC PREPARATION
(composition of dish, i.e. seasonings, addition of ingredients and sauces under strict hygienic and quality control conditions)
PACKAGING (ingredients weighed, placed in a plastic dish and covered with a plastic seal, impermeable to air and contaminants)
AIR EXTRACTION AND HERMETIC SEALING (air removed with vacuum packaging machine
and produce is hermetically sealed)
PASTEURISATION (slow heating in an autoclave with
a precise electronic regulator)
QUICK-CHILLING (inside a quick chilling chamber)
STORAGE IN COLD CHAMBER (between 0 and 3°C)
I REHEATING
(for lrl-15 min in a boiling water bath or 4-5 min in the microwave)
SERVICE
Fig. 1. Steps in the sous vide (vacuum cooking) process.
and then storage under refrigeration. production, storage, distribution and The various steps involved in vacuum marketing. cooking or sous vide processing are Wyatt and Guy (1980) reported that shown in Fig. 1. Unlike conventional temperatures of supermarket display thermally processed foods, sous vide cases were consistently greater than products undergo only a minimal heat 74”C, with some as high as 176”C, while processing which does not produce a temperatures of home refrigerators shelf-stable product. Recently, concern ranged from l-7-20.2%. Therefore, the has been expressed about the public potential for temperature abuse-even health safety of such minimally processed mild temperature abuse - at some stage food, particularly if subjected to tempera- of the product’s life cycle, particularly ture abuse at some stage of the product’s during storage in the retail environment,
Microbiological safety of sous vide processed meat product 179
exists. Furthermore, since many of these products are marketed in packages that consumers view as trditionally contain- ing shelf stable items, there is a high risk for consumer temperature abuse, mishandling, and over extending the product’s shelf life (Corlett 1989).
In order to ensure the market growth of this new generation of minimally pro- cessed products, the onus lies with the processor to ensure the microbiological safety of sous vide processed products at all stages of processing, distribution, marketing and retailing up to the point of consumption by the consumer. While the traditional approach to microbiological quality control involves end product sam- pling and analyses, this approach has several disadvantages for sous vide pro- cessed products: (1) microbiological tests are laborious and time consuming and may generate results too late for correc- tive action to be taken for a specific batch of product, (2) the test methods employed may not be sensitive enough to detect low numbers of pathogen(s) present in sous vide products, and (3) microbiological test results provide no information concern- ing the sources of contamination/ microbial growth in the end product or the locations in the process for corrective action to prevent future microbial contamination/growth.
To overcome the limitations of conven- tional microbiological quality control and to ensure product safety, a Hazard Analysis Critical Control Point Approach (HACCP) is recommended at all stages of sous vide processing (Canadian Code of Manufacturing Practices for Pasteurized/ Modified Atmosphere Packaged/ Refriger- ated Food 1990). The HACCP approach is not a new concept and it has been used as a quality control tool in food processing plants (Bauman 1974, Petersen and Gun- nerson 1974, Warne et al. 1985) and also in food service and catering establish-
ments (Munce 1984, Bobeng and David 1977). The HACCP approach, which is essentially a preventative approach to quality control, particularly with regard to microbiological hazards, comprises the following inter-related stages: (1) prep- aration of a product description and flow process diagram for the manufacturing, storage and distribution of product, (2) assessment of the hazards associated with the purchase, processing, prep- aration, distribution and/or use of a given raw material or final product, (3) determi- nation of critical control points to control the identified hazards, and (4) establish- ment of procedures to monitor critical control points.
Unlike conventional quality control, the HACCP approach shifts the emphasis from microbiological testing of the final product to raw material and process con- trol. The HACCP approach is therefore a much more forward looking approach and is intended to prevent problems be- fore they occur rather than finding them in the finished product. The objectives of this paper are to briefly review each of the stages involved in the HACCP process and to discuss their practical application to ensure the microbiological safety of a sous vide processed meat/pasta product.
1. Product description and preparation of flow process diagram The first stage in the HACCP approach begins with a product description. This description should include information on raw ingredients and their commercial specifications used in the product formulation, details of product compo- sition, including a, and pH, information on packaging materials/specifications. processing conditions and labelling instructions. An example of a product description for a sous vide processed meat/pasta product is shown in Table 1. The information will assist in the hazard
180 J. P. Smith et al.
0 . J3
cl D v El
OPERATION. An operation occurs when an object is intentionally changed from another object; or is arranged for another operation, transportation, inspection, or storage. An operation also occurs when information is given or received or when planning or calculating takes place. An operation symbol is also used to represent a person doing work.
TRANSPORTATION. A transportation occurs when an object is moved from one place to another, except when such movements are a part of the operation or are caused by the operator at the work station during an operation or inspection.
INSPECTION. An inspection occurs when an object is examined for identification or is verified for quality or quantity in any of its characteristics.
DELAY. A delay occurs to an object when conditions, except those which intentionally change the physical or chemical characteristics of the object, do not permit or require immediate performance of the. next planned action.
STORAGE. A storage occurs when an object is kept and protected against unauthorized removal.
COMBINED ACTIVITY. When it is desired to show activities performed either concurrently or by the same operator at.the same work station, the symbols for those activities are combined, as shown by the circle placed within the square to represent a combined operation and inspection.
Fig. 2. Symbols used in the construction of a flow process diagram.
analysis of the raw ingredients, processes or storage conditions which could result in a hazardous situation occurring and also to determine if suppliers of raw in- gredients comply with commercial and/or regulatory specifications.
The next step is the production of a detailed flow diagram for the sous vide process. A flow process diagram is essen- tially a diagrammatic scheme of a plant’s operations from receipt of raw materials through processing to packaging, storage and distribution of finished product and should be constructed by production spe- cialists with expertise in these areas.
Each step in the process should be writ- ten down systematically and then recorded diagrammatically using the flow diagram symbols shown in Fig. 2 (Apple 1977). Even minor steps, such as delays in the production process, should be listed, because even though they may not be considered important, they could have an additive effect on the safety of the product at some other stage further on in the process. An example of a flow process chart, summarizing the oper- ations for a sous vide processed meat/ pasta product, is shown in Fig. 3. Process flow charts have several important func-
Microbiological safety of sous vide processed meat product I731
Table 1. Product description for a sous vide processed meat/pasta product
Product description
Ingredients
Meat/pasta heat-and-serve product (28 day shelf life at refrigerated storage conditions)
Lean meat (1ean:fat 80:20), pasta, fresh mushrooms, tomato paste, spices (salt/pepper), water
Product compositiona
Packaging specifications
Processing conditions
Labelling specifications
Moisture (30%), fat cl%), protein (16%), carbohydrate (50%), ash (3%) Water activity (aJ0-98 pH 5.3
Tbermoformed polypropylene trays (10 mill polypropylene top web (2 mil) Net weight of packaged product 375 g
Pasteurize at 70°C for 45 min. Cool to 4°C within 2-3 h of processing. List of ingredients. Keep refrigerated at 4°C. Expiry date. Cooking/microwave instructions.
% Wet weight basis.
tions in food processing operations and can be used: (a) to analyze material move- ment and to show interrelationships be- tween product lines, (b) to highlight ex- cessive transportation steps, (c) to predict potential ‘bottlenecks’ and delays in pro- duction, and (d) to optimize the use of space and equipment. However, the most important function of a flow diagram is that it facilitates the Hazard Analysis and Critical Control Point (HACCP) evaluation of the sous vide process.
2. Hazard analysis .
In order to establish the safety of sous vide products, a hazard analysis must be undertaken at each stage of a product’s transition from raw ingredients to fin- ished product and distribution. Hazard analysis has been defined as ‘any system which analyses the significance of a hazard to consumer safety or product acceptability’ (Thorpe and Leaper 1988). A hazard has been defined as a ‘potential to cause harm to the consumer (safety) or the product (spoilage)’ (Thorpe and Leaper 1988). Since the hazard analysis must cover the entire flow process dia-
gram, it should be conducted by a team with expertise in procurement of raw materials, food processing operations, food packaging, food microbiology, food chemistry, toxicology, quality assurance and regulatory affairs. The objectives of the hazard analysis are: (a) to identify all the potential food hazards, specifically microbiological hazards, which are a threat to consumer safety, (b) to identify potentially hazardous foods or ingredi- ents, and (cl to identify the process points in the sous vide process where a potential mirobiological hazard may exist (ICMSF 1988, Peterson and Gunnerson 1974). Each of these parts of the hazard analysis will be briefly reviewed.
(a) Identification of food hazards
The major categories of food hazards associated with food processing are sum- marized in Table 2 (Stauffer 1988). While the HACCP evaluation is intended to address all potential physical, chemical and microbiological hazards which compromise product safety, microbiologi- cal hazards (specifically food borne patho- gens) pose the greatest threat to con-
182 J. P. Smith et al.
0 1
9
0,
0 2
w
D 1
0 3
w
0 4
0 5
0 6
w
0 7
w
D 2
0 8
Receipt of raw materials (meat, vegetables. spices, packaging materials)
Transfer to controlled storage
Controlled storage
Transfer to production area
Formulation of raw ingredients
Transfer to filling area
Delay prior to filling/during filling
Filling/vacuum packaging of product
Transfer to retort
Filling of retort
Pasteurization/cooling of product
Removal of product from retort
Transfer to cooling area
Rapid cooling of product
Transfer to labelling area
Delay prior to/during labelling due to product buildup
Labeling
Fig. 3. A flow process diagram for a sous vide processed meat/pasta product.
sumer safety because of their ubiquitous nature, and must receive priority in any HACCP evaluation, and so will be the only hazards addressed in this paper.
Waites (1988) subdivided food borne pathogens into three main groups: those that present severe hazards, those that present moderate hazards with poten- tially extensive spread, and those that present moderate hazards with limited spread. Examples of food borne patho-
gens within each group are shown in Table 3 (Waites 1988).
The major microbiological hazard associated with sous vide processing is the growth of, and toxin production by, Clostridium botulinum types A, B and E spores. These sporeforming organisms pose the greatest threat to consumer safety due to the ability of this sporeform- ing pathogen to withstand the mild heat processing conditions of sous vide pro-
Microbiological safety of sous vide processed meat product 183
w Transfer to cartoning area
D 3 Delay prior to/during cat-toning
0 9 Cartoning
w Transfer to warehouse
v Storage in warehouse
is/t Transfer to loading area
D 4 Delay prior to/during loading
0 10 Loading of transport container
0 11 Transportation to retail outlet
v Storage in supermarket
SUMMATION OF EVENTS:
11 Operations,
9 transfers,
3 controlled storages,
4 major delays.
cessing, the complete or partial destruc- tion of non-sporeforming competing mic- roflora and potential indicators of incipi- ent spoilage, and the presence of anaerobic packaging conditions condu- cive to the growth of, and toxin pro- duction by, C:botulinum in the processed product. Control of this pathogen is therefore critical to product safety in view of the fact that non-proteolytic strains of C. botulinurn are capable of growth and toxin production at temperatures as low as 35”C, while C. botulinurn type A and B spores can grow at temperatures of lO- 12°C (Palumbo 1986).
Non-sporeforming, food borne patho- gens of public health significance in sous vide processed products include entero- pathogenic strains of Escherichia coli,
Salmonella, Staphylococcus, Aeromonas, Listeria and Yersinia species. Recent studies have shown that L. monocyto- genes and Y. enterocolitica are capable of growth at refrigeration temperatures (<5”C) over an extended time period (7- 21 days) (Wyatt and Guy 1980, Palumbo 1986). They also reported that traditional food borne pathogens, such as Salmo- nella species and Staph. aureus, are capable of growth at temperatures 5- 12”C, i.e. conditions of slight temperature abuse.
While all of these non-sporeforming pathogens should be destroyed during thermal processing, they pose a potential threat to consumer safety if the raw in- gredients are of poor microbiological qua- lity or the product becomes heavily con-
184 J. P. Smith et 81.
Table 2. Food hazards (Stauffer 1999)
A.
B.
C.
D.
E.
F.
G.
Bacteria Clostridium botulinum Clostridium perfringens Salmonella Staphylococcus aureus
Molds Aspergillus flavus Penicillium cyclopium
Parasites Tape worms Trichinellae
H.
I.
J.
Radioactive isotopes Cesium 137 Iodine 131 Potassium 90
Extraneous matter Filth Glass splinters Peeling paint Tramp metal
Pests Birds Insects Rodents
K.
Naturally occurring toxins Ciguatera poisoning Gilseed toxins Nutritional deficiencies Instant formula exceptions Processed foods
Residues Antibiotics Chlorinated insecticides Grganophosphate insecticides
L.
M.
Regulatory hazards Label errors Short weights
Industrial chemicals Hexabromobiphenyl Polychlorinated biphenyls Vinyl chloride
Heavy metals Arsenic Cadmium Lead Mercury Selenium
Functional hazards Packaging defects Particle size deviations
Table 3. Groups of food borne pathogens (Waites 19331
Group 1. Severe Hazards
Brucella abortus Salmonella sendai Brucella melitensis Salmonella typhi Brucella suis Shigella spp. Clostridium botulinum Vibrio cholerae Mycobacterium bovis Hepatitis B virus Salmonella cholerae-suis Fish and shellfish toxins Salmonella paratyphi A Some mycotoxins
Group 2. Moderate hazards with potentially extensive spread
Pathogenic Escherichia coli Salmonella spp. Listeria monocytogenes Streptococcus pyogenes
Group 3. Moderate hazards with limited spread
Bacillus cereus B. licheniformis B. subtilis Campylyobacterjejuni Clostridiumperfringens Coxiella burnetii
Staphylococcus aureus Streptococcus zooepidemicus Trichinella spiralis Vibrio parahaemolyticus Yersinia enterocolitica
Microbiological safety of sous vide processed meat product 185
taminated during processing as a result evaluation of a product and its ingredi- of poor manufacturing practices and the ents according to their hazard character- pasteurization process is inadequate to istics, using ‘+’ for yes and ‘0’ for no. destroy the high microbial load of non- According to Bauman (19741, the hazard sporeforming pathogens. categories based on decreasing risk are:
(6) Identification of hazard categories
An important step in the hazard analysis is the identification of the ingredients’ and finished product’s hazard character- istics and identification of their appropri- ate hazard category. According to Peter- son and Gunnerson (1974), a product and its ingredients may be a significant health risk ifit has the following hazard characteristics.
Category I: Foods intended for use by infants, the aged and the infirm.
Category II: Foods with all three hazards (+++I.
Category III: Foods with two hazards t+o+, o++, ++oj.
Category IV: Foods with one hazard coo+, +oo, o+oj.
Category V: Foods with none of these hazards (000).
They contain sensitive ingredients and therefore potentially harmful organisms.
The manufacturing process does not contain a controlling processing step that does not effectively destroy all harmful micro-organisms and microbial toxins.
There is a potential for microbiological abuse (temperature abuse) in distri- bution or in consumer handling that could render the product harmful when consumed.
The risk characteristics and hazard categories of a sous vide meat pasta prod- uct and the ingredients used in its formu- lation are shown in Table 4. It is evident from Table 4 that a sous vide meat/pasta product has a high degree of risk due to the fact that they contain sensitive in- gredients, they are subject to a minimal heat processing step, and there is a real potential for consumer abuse.
The combination of all these factors can be used to classify food/ingredients into hazard categories based on a risk assess- ment. A risk has been defined as the probability of hazard occurring (ICMSF 1988). A risk assessment is a yes/no
(c) Identification of critical operations
Having identified the hazard character- istics and categories of the raw ingredi- ents and finished product, the next stage in the hazard analysis is to identify the critical operations in the sous vide pro-
Table 4. Risk assessment of a sow vide meat/pasta product
Risk characteristics
Item
Product Sous vide meat/pasta product (a, 0.98/pH 5.6)
Ingredients Fresh ground beef Pasta Fresh mushrooms Tomato paste Water Spices/sugar
Sensitive Microbes Abuse Hazard ingredient not destroyed potential category
+ + + II
+ + + II 0 + 0 IV + + 0 0 + 0 if + 0 0 Iv 0 0 0 V
186 J. P. Smith et al.
cess. A critical operation is a point in a process where a potential microbiological hazard may exist or arise. Examples of potential critical operations for a sous vide process product are shown in Table 5. Many of the critical operations are obvious - e.g. quality and storage of raw ingredients, thermal processing - but others may be less apparent, such as prolonged delays between processing stages which could increase the risk of temperature abuse and microbial growth.
3. Determination of critical control points An important stage of the HACCP evalu- ation is the identification of critical con- trol points (CCP) in the process to control
identified microbiological hazards to ensure product safety. Several defi- nitions for critical control point exist. The National Advisory Committee on Micro- biological Criteria for Foods (1989) de- fined Critical Control Points as any point or procedure in a specific food system where loss of control may result in an unacceptable health risk. Bobeng and David (19771, defined Critical Control Points as the points in a process which eliminate or reduce a microbiological hazard from occurring. Bauman (19741, defined Critical Control Points as those processing factors where loss of control would result in an unacceptable food safety risk. Baird-Parker and Hayes (1990) defined a Critical Control Point (CCP) as a location, practice, procedure
Table 5. Control and Critical Points for a sous vide processed meat/pasta product
Critical control points
Raw Sanitation Time ingredient equipment/ temperature Additional
Critical operations control personnel relationship Packaging ‘barriers’
Receipt of raw ingredients X
Controlled storage of raw X X ingredients
Formulation X X X X
Delay prior to filling X X
Filling of product X X X
PasteurizationCooling X X in retort
Rapid cooling of product on X X leaving retort
Delay prior to labelling X
Labeling X X
Delay prior to cartoning X
Car-toning X X
Delay prior to loading X container
Loading of container X X
Transportation to retail X outlet
Storage in retail outlet X X
Microbiological safety of sous vide processed meat product 187
Table 6. Sensitivity categories for food ingredients (Stauffer 1966)
I. Ingredients for special groups Infants IIlfmn Geriatric
II. Susceptible ingredients
III. Insensitive ingredients
Dairy products Em Fish Meat soup
Flour Shortening SOY Starch
IV. Ingredients free of pathogens Baking Soda Citric Acid Food colors Monosodium Glutamate Salt Sugar
or stage in the food production, distri- bution and use chain which can be used to control the risk (probability of occur- rence) of an identified hazard to an acceptable level, i.e. safe level. Critical Control Points can take a variety of forms such as raw ingredient quality, heat pro- cesses, chemical and physical changes to the food, such as acidification, reduction of a, and addition of preservatives and specific hygiene practices. Examples of CCPs, either alone or in combination with each other, which reduce the risk of contamination by, and survival and pro- liferation of, the identified microbial hazards are: quality of raw ingredients, sanitation (personnel/equipment), time/ temperature relationship, packaging and levels of additional barriers.
It is evident from Table 5 that more than one CCP may influence product safety at a specific critical operations dur- ing the process. For example, during the formulation stage, the microbiological quality of the raw ingredients, equipment and personal sanitation, the time sensi- tive ingredients are held at a particular temperature and levels of additional bar- riers used in the final product formulation are all important critical control points
affecting the microbiological safety of the end product. Each critical control point must therefore be monitored on a regular basis as loss of control of any one of these critical control points could have an addi- tive effect on the microbial load of the finished product and result in a hazar- dous situation occurring. Specific control options for each critical control point and their contribution to microbiological safety of sous vide processed meat/pasta product are briefly discussed.
(a) Quality of raw ingredients
Raw ingredients are the primary vectors of harmful or potentially harmful micro- organisms in all processed food products. According to Stauffer (1988) food ingredi- ents can be arranged into categories on the basis of their sensitivity to microbial contamination (Table 6). While certain raw ingredients are free or essentially free of micro-organisms, care must be taken with the purchase and storage of more sensitive ingredients, particularly those of animal origin such as meat, fish and poultry which may be contaminated with pathogenic organisms (Stauffer 1988). The hazard analysis should iden- tify all the ingredients at risk in the for-
188 J. P. Smith et al.
mulation and identify the food borne pathogens commonly associated with each raw ingredient. To minimize the potential risks from hazardous micro- organisms, procurement of raw materials of the best possible microbiological qual- ity is essential. Physical inspection of sen- sitive raw ingredients for visible signs of contamination, e.g. hair, dirt, slime should be done to ensure the microbiolo- gical quality of raw ingredients. Tem- perature checks should also be done on all refrigerated/frozen product to ensure that the product has not been subjected to any temperature abuse during transpor- tation to the plant. Laboratory testing of ingredients should be done on a regular basis by food processors and ingredient suppliers to ensure ingredients conform to regulatory and commercial microbiolo- gical specifications.
(b) Sanitation (equipment and personnel)
An important critical control point in the sous vide process is sanitation. This CCP is important since the effectiveness of the pasteurization treatment will depend on the microbial load of the product. Bryan (1974) reported that two factors contribu- ting to food borne disease outbreaks were inadequate cleaning of equipment and cross-contamination of products. Cross- contamination of in-process product from raw product can be avoided through good manufacturing practices. Procedures should be established by each processor for cleaning and sanitizing of storage facilities, food contact surfaces, tools and utensils and processing equipment. In addition, detailed schedules specifying methods of disassembling equipment, methods and frequency of cleaning, and tests for cleaning efficiency should all be clearly specified. It is also imperative to prevent/minimize cross-contamination of the in-process and finished product from raw ingredients. Raw vegetables, fish,
meat, etc. should be segregated in specific storage areas and cleaned/prepared in separate processing areas. Furthermore, traffic patterns should be established to control movement of food products be- tween processing areas of the plant to prevent cross contamination and build up of product. Buildings and processing equipment should be well designed to facilitate cleaning operations and to ensure a forward and regulated flow in the process operations from arrival of raw ingredients to shipping of finished prod- uct.
In addition to plant and equipment sanitation, employee hygiene and good handling practices are important in pre- venting inoculation of food materials with pathogenic bacteria. Bryan (1974) reported that infected persons practicing poor personal hygiene contributed to 151 of 725 food poisoning outbreaks reported during 1961-1972. It is the repsonsibility of management to ensure that employees be properly attired during food handling/ processing, to minimize product contami- nation. Any person suffering from a food borne illness should not be working in any food handling or preparation area. All employees must feel a sense of per- sonal responsibility for the microbiologi- cal safety of food products. Adequate and continuing education of personnel in food and personal hygiene should be an im- portant priority of both employer and employee.
(c) Timeltemperature relationship
It is evident from Table 5 that time- temperature is one of the most important CCPs influencing product safety. The time/temperature relationship, i.e. the time a product is held at a specified tem- perature, is critical to minimize microbial growth during product preparation, stor- age and distribution and in the retail environment. All sensitive ingredients used in sous vide products should be
Microbiological safety of sous vide processed meat product k39
stored under strict temperature con- trolled conditions. Longree (1972) recom- mended optimal refrigerated storage temperatures by food CategoryAairy product and eggs 2 to 4”C, meat and poultry -1 to 2”C, fish - 1 to 0°C and fruits and vegetables 2-4”C. Refrigerated storage time limits should be specified for all potentially hazardous raw ingredients and a first-in, first-out system of inven- tory control should be used. Refrigerated storage areas should be well designed to permit a free flow of cold air between and around ingredients/products and be equipped with a mechanical refrigera- tion system capable of maintaining ingredient/product temperature at - 1 to 4°C under normal conditions of outside humidity, temperature and peak loading capacity. The general principles outlined above are also applicable to storage, dis- tribution, and retail display of end prod- uct. If a breakdown occurs in any of the refrigerated units, product temperature should be checked and if within accept- able limits (<4”C), the product should be transferred to another refrigerated unit. If product temperature is significantly above the acceptable range established for products, expert advice should be sought from the manufacturer, process authority or from regulatory agency officials.
The temperature of’ all preparation/ packaging areas should be maintained at 10°C or below to minimize the growth of food borne pathogens prior to heat pro- cessing. If there is a delay at any process- ing operation, e.g. product build up at filling operations or pasteurization, the product should be diverted and stored at ~4% until product build up decreases and normal flow is resumed.
The time/temperature relationship is also critical to maximize microbial des- truction during pasteurization. Longree (1972) recommended that food should be heated to 74-77”C, in order to destroy
vegetative cells of common pathogens that cause food borne illness. Sous vide products should therefore be heat pro- cessed until all parts of the food are at least 60°C or above and held at this tem- perature for a specified time period, as determined by a process authority. The maximum time a product will be held at temperature will depend on the types and numbers of micro-organisms contami- nating the product, the heat resistance of each organism, the physicochemical nature of the food product, and the desired organoleptic quality of the final product. In most cases, a thermal process is designed to achieve a 12-13 log cycle of a target organism with the highest D value. The most common organism used is Streptococcus faecalis which has a D value of 2.95min at 70°C (Rosset and Poumeyrol1986). Therefore, thermal in- activation of this organism would ensure the destruction of vegetative cells of non- spore forming pathogens such as L. monocytogenes and Y. enterocolitica (Rosset and Poumyrol 1986). The ther- mal processing requirement for each product should be carried out during the product development phase in order to verify the efficacy of the heat process. Operation of the heat processing equip- ment, thermal process calculations of the lethal potential of the pasteurization treatment, and adequacy of the pasteur- ization treatment should all be carried out by appropriately trained personnel. Any process deviations should be brought to the immediate attention of competent process authority for immediate correc- tive action. It is important for all thermal process parameters to be reassessed on a continuous basis if changes are made to formulation/portioning/filling weights of product.
While the pasteurization treatment should inactivate all vegetative cells of non-sporeforming food borne pathogens, it will have little effect on the C. botuli-
190 J. P. Smith et al.
num spores. However, whenever a prod- uct can tolerate a more severe heat pro- cess, the product could be processed at temperatures sufficient to inactivate less heat resistant spores C. botulinum type E which have a D value of O-33 min at 90°C. Processing at this temperature will have no effect on C. botulinurn type A and B spores which have D values of 200 min at 90°C (Basset and Poumeyrol 1986). Con- trol of these organisms can be achieved through proper refrigeration and/or the use of additional barriers which are dis- cussed below.
In addition to heating, cooling should be carried out as quickly and efficiently as possible to bring the temperature of the warmest point of food from 60°C and above to less than 7.2% within l-5 h and to 4°C within 3 h. This is essential to prevent the growth of C. botulinurn species or any other food borne pathogen which may have survived thermal pro- cessing. The processed product should be stored at 4°C or less and maintained at that temperature throughout the distri- bution chain until consumed.
(d) Additional barriers
The growth of food borne pathogens can be inhibited if proper temperature control (0 to 2°C) can be maintained throughout all stages of processing, storage and dis- tribution. However, refrigeration by itself cannot be guaranteed as an ade- quate barrier for the microbiological safety of sous vide products, or any other minimally processed food product, and additional barriers may be necessary to ensure the public health safety of the end product (Palumbo 1986). The combined use of several barriers or preservative factors is best explained by the ‘hurdle concept’ of Leistner (1978) which states that ‘several barriers, even if any of them individually cannot inhibit microbial growth, will nevertheless prevent mi- crobial growth if the barriers are incor-
porated into a food in sufficient number and height’. Barriers which could be used in conjunction with temperature to in- hibit surviving micro-organisms, specifi- cally C. botulinurn in sous vide products, include water activity (~1, pH, and pre- servatives. Combinations of a, and pH reduction have proved effective in con- trolling growth of C. botulinurn type E in caviar stored at room temperature while combinations of heat treatment, smoking and brine have been used to control growth of C. botulinum type E in smoked fish (Hauschild and Hilsheimer 1979, Christiansen et al. 1968). The effective- ness of additional barriers in sous vide products should be evaluated using inoculated pack studies during the prod- uct development stage in order to estab- lish the levels of barrier(s) to ensure both safety and organoleptic quality of the product. This testing should be done under temperature abuse conditions in order to demonstrate the effectiveness of the additional barriers to prevent growth of, and toxin production by, C. botulinum. Product a,, pH and level of preservative must be monitored on a continual basis to ensure that this critical control point is within commercial and regulatory speci- fications.
(e) Packaging
Packaging is an important critical control point and plays an essential role in pro- tecting the food from external contami- nation before, during and after thermal processing. The packaging material itself should not be a source of microbial con- tamination and/or lack protective charac- teristics, particularly under thermal pro- cess conditions. Upon receipt, all packaging materials should be tested visually for their integrity and physical cleanliness and stored in a clean area at a specified temperature/relative humidity in accordance with the manufacturer’s
Microbiological safety of sous vide processed meat product 191
specifications. Specifications (structural, chemical and microbiological) of packag- ing materials and the final paackage should be defined and monitored for each batch of product. If possible, packages should be chosen to avoid confusion with those used for shelf stable products. Monitoring procedures should be applied to ensure filling temperatures/weights, sealing pressures/temperatures comply with both commercial and regulatory specifications. Careful control of filling temperature is critical to prevent mi- crobial growth prior to pasteurization while correct filling weights ensure ade- quate heat distribution and proper pro- cessing of product. Packaging integrity should be monitored routinely in order to prevent contamination by micro- organisms prior to and after thermal pro- cessing and during storage, distribution and sale. Improper labeling may also in- crease the risk for consumer abuse and the growth of potentially hazardous bac- teria. Each package should be promi- nently labeled ‘keep refrigerated’ or ‘keep under refrigeration’ and also contain a ‘use by’ date or a ‘sell by’ date. The con- sumer should also be advised of proper handling and preparation procedures to ensure product safety.
4. Monitoring of critical control points For each CCP in the processing oper- ation, detailed monitoring procedures for control options influencing product safety should be determined and written down. Such information should include methods of monitoring, frequency of monitoring, acceptable limits or specifications for specific control options, and corrective action if a CCP is out of specification. Sampling plans should be developed according to ICMSF (1986) guidelines based on the hazards a food contains and the intended end use of the product. An
example of a sampling plan based on the hazard characteristics of ingredients/ finished product is shown in Table 7. It is evident from this plan that the more hazards a food contains, the greater the frequency and stringency of sampling. Wherever possible, CCPs should be moni- tored continuously, e.g. critical tempera- tures during processing should be moni- tored with a temperature recording device or temperature/time integrator. It is important that all monitoring devices be efficient and well designed, checked regularly and accurately calibrated. When monitoring by automatic methods is not possible, monitoring should be done by appropriately trained personnel in- volved with processing operations. Moni- toring may involve visual observations (e.g. visual inspection of meat, cleanli- ness of work surfaces), physical measure- ments (filling temperature/weights, tem- peratures of coldrooms/work areas), and chemical measurements (e.g. Q, pH). Examples of monitoring procedures at specific critical control points for a sous vide processed meat/pasta product are shown in Table 8. Results of monitoring must be recorded to serve a documen- tation that the process is under control at all time. Several methods can be used to record observations, e.g. use of control charts, which can be used to visualize when a critical control point parameter is out of specification. Once the HACCP plan is put into operation, it should be continuously checked to ensure that each step is being carried out, that results are being recorded, and that prompt action is taken when control limits for control op- tions are out of specification. The serious- ness of a failure to control the identified CCP must then be determined. A concern has been defined as ‘an expression of the seriousness of a failure to control a criti- cal control point, derived from knowledge of a hazard and the risk of it occurring’ (Thorpe and Leaper 1988). According to
Tabl
e 7.
Exa
mpl
es
of m
icro
biol
ogic
al
sam
plin
g pl
ans
depe
ndin
g on
deg
ree
of h
ealth
ha
zard
Cond
itions
in
which
th
e fo
od
is ex
pect
ed
to b
e ha
ndled
an
d co
nsum
ed
afte
r sa
mpl
ing,
in
the
usua
l co
urse
of
eve
nts’
Degr
ee
of c
once
rn
relat
ive
Cond
itions
re
duce
.to
utili
ty
and
healt
h ha
zard
de
gree
of
con
cern
Co
nditio
ns
caus
e no
ch
ange
in
conc
ern
Cond
itions
m
ay
incre
ase
conc
ern
No d
irect
he
alth
haza
rd
Utilit
y (e
.g.
shel
f Iif
e an
d sp
oilag
e)
Incr
ease
sh
elf
life
Case
1
3-cla
ss
n =
5, c
= 3
b
No c
hang
e Ca
se
2 3-
class
n
= 5,
c =
2
Redu
ce
shel
f life
Ca
se
3 3-
class
n
= 5,
c =
1
Heal
th
haza
rd
Low,
ind
irect
(indic
ator
or
gani
sms)
Re
duce
ha
zard
Ca
se
4 3-
class
n
= 5,
c =
3
No c
hang
e Ca
se 5
3-
class
n
= 5,
c =
2
Incr
ease
ha
zard
Ca
se
6 3-
class
n
= 5,
c =
1
Mod
erat
e,
dire
ct,
limite
d sp
read
Ca
se 7
Ca
se 6
Ca
se 9
3-
class
n
= 5,
c =
2
3-cla
ss
n =
5, c
=
1 3-
class
n
= 10
, c
= 1
Mod
erat
e,
dire
ct,
pote
ntial
ly ex
tens
ive
Case
10
Ca
se
11
Case
12
sp
read
a-
class
n
= 5,
c =
0
a-cla
ss
n =
10,
c =
0 2-
class
n
= 20
, c
= 0
Seve
re,
dire
ct
Case
13
Ca
se
14
Case
15
2-
class
n
= 15
, c
= 0
2-cla
ss
n =
30,
c =
0 a-
class
n
= 60
, c
= 0
aMor
e st
ringe
nt
sam
pling
pla
ns w
ould
gene
rally
be
use
d fo
r se
nsitiv
e fo
ods
desti
ned
for
susc
eptib
le
popu
lation
s. by
= n
umbe
r of
sam
ple
units
pe
r lo
t. c
= m
axim
um
allow
able
num
ber
of s
ampl
e un
its y
ieldin
g an
uns
atisf
acto
ry
resu
lt.
Sour
ce:
ICM
S (1
986)
.
Table
8.
M
onito
ring
of C
ritica
l Co
ntro
l Po
ints
fo
r a
sow
vide
mea
t/pas
ta
prod
uct
Crit
ical
op
erat
ion
Pote
ntia
l ha
zard
/risk
C
ritic
al
Con
trol
Poin
t(s)
Prev
enta
tive,
co
ntro
l an
d m
onito
ring
proc
edur
es
Rec
eipt
of r
aw i
ngre
dien
ts
(fres
h m
eat)
Pres
ence
of s
poila
ge/p
atho
geni
c ba
cter
ia,
e.g.
Sal
mon
ella
, Li
ster
ia
mon
ocyt
ogen
es a
nd C
lost
ridiu
m
botu
linum
.
Con
trolle
d st
orag
e of
raw
in
gred
ient
s G
row
th
of s
poila
ge/p
atho
geni
c ba
cter
ia.
. C
ross
-con
tam
inat
ion
of ra
w
ingr
edie
nts.
Form
ulat
ion
Mic
robi
al
load
of
raw
ing
redi
ents
.
Del
ay p
rior
to f
illin
g
Con
tam
inat
ion
by e
quip
men
U
hand
lers
. G
row
th
of s
poila
ge/p
atho
geni
c ba
cter
ia.
Gro
wth
of
sur
vivi
ng
path
ogen
s af
ter
proc
essi
ng,
parti
cula
rly
unde
r te
mpe
ratu
re
abus
e co
nditi
ons.
Mic
robi
olog
ical
qu
ality
of
raw
in
gred
ient
s.
Tem
pera
ture
co
ntro
l.
Sani
tatio
n of
sto
rage
co
nditi
ons.
Mic
robi
olog
ical
qu
ality
of
raw
in
gred
ient
s.
Equi
pmen
t an
d pe
rson
nel
sani
tatio
n.
Tem
pera
ture
co
ntro
l.
Form
ulat
ion
cont
rol.
Cro
ss c
onta
min
atio
n G
row
th
of s
poila
ge/p
atho
geni
c ba
cter
ia.
Sani
tatio
n.
Tem
pera
ture
co
ntro
l.
Visu
al i
nspe
ctio
n of
mea
t fo
r di
rt,
hair,
sl
ime.
If m
eat
disc
olor
ed/
smel
ls,
do m
icro
biol
ogic
al
anal
ysis
. N
ote
on p
rodu
ctio
n ca
rd.
If pr
oduc
ts o
ut o
f com
mer
cial
sp
ecifi
catio
n,
retu
rn
to s
uppl
ier.
Mea
sure
te
mpe
ratu
re
of fr
esh
mea
t. C
heck
tem
pera
ture
/rela
tive
hum
idity
of
sto
rage
con
ditio
ns.
Adju
st
tem
pera
ture
s.
Not
e ph
ysic
al c
lean
lines
s of
sto
rage
ar
eas/
sepa
ratio
n of
raw
fro
m
proc
esse
d pr
oduc
t. Vi
sual
ins
pect
ion
of ra
w
ingr
edie
nts.
M
easu
re
tem
pera
ture
of
tem
pere
d m
eat.
Che
ck p
hysi
cal
clea
nine
ss o
f wor
k ar
eas.
Not
e pe
rson
nel
hygi
ene
of a
ll fo
od
hand
lers
. En
sure
all
food
han
dler
s pr
oper
ly
attir
ed
to h
andl
e fo
od.
Che
ck t
empe
ratu
re
of a
ll pr
oces
sing
are
as (
10 f
1°C
). C
heck
fo
rmul
atio
n,
flnal
a,
and
pH o
f pr
oduc
t. If
any
chan
ges
in
form
ulat
ion
notif
y pr
oces
sing
au
thor
ity.
Che
ck p
hysi
cal
clea
nlin
ess
of
area
s w
here
bui
ld u
p of
pro
duct
oc
curs
. Not
e te
mpe
ratu
re
of
prod
uct.
Not
e tim
e/le
ngth
of
del
ay.
If pr
olon
ged
dela
ys a
ntic
ipat
ed,
stor
e pr
oduc
t at
l-2
%.
Con
tinue
d
Tabl
e 8.
C
ontin
ued
Crit
ical
op
erat
ion
Pilli
ng o
f pro
duct
Pote
ntia
l ha
zard
/risk
Gro
wth
of
pat
hoge
nic
bact
eria
pr
ior
to p
roce
ssin
g.
Und
erpr
oces
sing
of
pro
duct
an
d su
rviv
al
of n
on-s
pore
for
min
g pa
thog
enic
ba
cter
ia.
Crit
ical
C
ontro
l Po
int(s
)
Equi
pmen
t/per
sonn
el
sani
tatio
n.
Tem
pera
ture
co
ntro
l. Pa
ckag
ing/
fillin
g/se
alin
g op
erat
ion
Prev
enta
tive,
co
ntro
l an
d m
onito
ring
proc
edur
es
Che
ck p
hysi
cal
clea
nlin
ess
of
fillin
g eq
uipm
ent/a
rea.
C
heck
hy
gien
e pr
actic
es o
f foo
d ha
ndle
rs.
Ensu
re a
ll ra
w p
rodu
ct
is
phys
ical
ly r
emov
ed f
rom
pro
cess
ed
prod
uct.
Che
ck t
empe
ratu
re
of
fillin
g ar
ea (
10 +
1°C
). C
heck
in
tegr
ity
of p
acka
ging
m
ater
ials
. C
heck
fill
wei
ght/v
acuu
m/p
acka
ge
head
spac
e. I
f pr
oduc
t ov
erfil
led,
ad
just
fill
ers.
If
impr
oper
ly
seal
ed
or to
o hi
gh r
esid
ual
Oz,
rese
t va
cuum
/hea
t se
al s
ettin
g.
Not
e on
pr
oduc
tion
card
. N
otify
pa
ckag
ing
supe
rvis
or o
f var
iatio
n fro
m
stan
dard
s.
Past
euriz
atio
n of
pro
duct
/ co
olin
g Su
rviv
al
and
grow
th
of s
pore
and
Ti
me/
tem
pera
ture
of
ther
mal
no
n-sp
ore
form
ing
path
ogen
ic
proc
essi
ng/c
oolin
g.
bact
eria
. Pa
ckag
ing
inte
grity
.
Che
ck p
roce
ssin
g tim
e/
tem
pera
ture
an
d ac
cura
cy o
f th
erm
omet
ers.
C
heck
tem
pera
ture
at
cen
tre o
f pro
duct
dur
ing
heat
ing.
Ve
rify
ther
mal
pr
oces
sing
ca
lcul
atio
n.
Not
e on
pro
duct
ion
card
. N
otify
th
erm
al
proc
essi
ng
auth
ority
de
viat
ions
fro
m
esta
blis
hed
proc
essi
ng p
roce
dure
s.
Che
ck p
acka
ging
in
tegr
ity
prio
r to
pa
ckag
ing.
C
heck
for
bul
ging
pa
ckag
es.
Rem
ove
from
bat
ch.
Cont
inued
Tabl
e 8.
Con
tinue
d
Crit
ical
op
erat
ion
Rap
id c
oolin
g of
pro
duct
Pote
ntia
l ha
zard
/risk
Gro
wth
of
sur
vivi
ng
path
ogen
ic
bact
eria
. C
onta
min
atio
n of
pro
duct
by
sp
oila
ge/p
atho
geni
c ba
cter
ia.
Crit
ical
C
ontro
l Po
int(s
)
Tim
e/te
mpe
ratu
re.
Pack
agin
g co
ntro
l.
Prev
enta
tive,
co
ntro
l an
d m
onito
ring
proc
edur
es
Che
ck in
tern
al
tem
pera
ture
of
pr
oduc
t du
ring
cool
ing
to 4
°C.
Rec
ord
time
to r
each
thi
s te
mpe
ratu
re.
If th
e tim
e ta
ken
to
reac
h th
is t
empe
ratu
re
is g
reat
er
than
30
min
out
side
spe
cific
atio
n re
cord
on
prod
uctio
n ca
rd a
nd
notif
y pr
oduc
tion
supe
rvis
or.
Che
ck p
acka
ging
in
tegr
ity
and
do
rand
om
leak
tes
ts o
n se
lect
ed
sam
ples
. O
bser
ve f
or le
akag
e/
spilla
ge.
Del
ay p
rior
to la
belin
g G
row
th
of s
urvi
ving
pa
thog
enic
ba
cter
ia.
Tim
e/te
mpe
ratu
re.
Labe
ling
Gro
wth
of
sur
vivi
ng
path
ogen
ic
bact
eria
. C
onsu
mer
ab
use
of p
rodu
ct.
Tim
e/te
mpe
ratu
re.
Labe
ling
inst
ruct
ions
.
Car
toni
ng
Gro
wth
of
sur
vivi
ng
path
ogen
ic
bact
eria
. C
ross
-con
tam
inat
ion.
Tim
e/te
mpe
ratu
re.
Pack
gagi
ng.
Che
ck p
rodu
ct
tem
pera
ture
at
re
gula
r in
terv
als.
If
prod
uct
build
up
exc
essi
ve, r
emov
e to
re
frige
rate
d st
orag
e un
til
prod
uct
build
up
decr
ease
s. N
ote
on
prod
uctio
n ca
rd.
Che
ck p
rodu
ct
tem
pera
ture
as
ab
ove.
Che
ck la
bellin
g in
stru
ctio
ns
for
stor
age
cond
ition
s ‘K
eep
refri
gera
ted’
. C
heck
use
by
date
and
coo
king
/mic
row
ave
inst
ruct
ions
.
Che
ck t
empe
ratu
re
of c
arto
ning
ar
ea (
10°C
) and
pot
entia
l si
gns
of
prod
uct
build
up/
tem
pera
ture
ab
use.
C
heck
wei
ghts
/inte
grity
of
se
cond
ary
cont
aine
rs
and
labe
ling
inst
ruct
ions
on
ext
erna
l pa
ckag
es.
Cont
inued
Tabl
e 8.
C
ontin
ued
Crit
ical
op
erat
ion
Del
ay p
rior
to lo
adin
g co
ntai
ner
Load
ing
of tr
ansp
ort
cont
aine
r
Pote
ntia
l ha
zard
/risk
Gro
wth
of
sur
vivi
ng
path
ogen
ic
bact
eria
.
Cro
ss-c
onta
min
atio
n of
pro
duct
. G
row
th
of s
urvi
ving
pa
thog
enic
ba
cter
ia.
Crit
ical
C
ontro
l Po
int(s
)
Tim
e/te
mpe
ratu
re.
Sani
tatio
n.
Tim
e/te
mpe
ratu
re.
Prev
enta
tive,
co
ntro
l an
d m
onito
ring
proc
edur
es
Che
ck t
empe
ratu
re
of lo
adin
g do
ck a
rea/
tem
pera
ture
of
pro
duct
. N
ote
on p
rodu
ctio
n ca
rd.
Che
ck p
hysi
cal
clea
nlin
ess
of
trans
port
cont
aine
r. C
heck
ref
riger
ated
te
mpe
ratu
re
of
cont
aine
r/loa
ding
of
con
tain
ers/
air
circ
ulat
ion.
Tran
spor
tatio
n to
ret
ail
Gro
wth
of
sur
vivi
ng
path
ogen
ic
outle
t ba
cter
ia.
Tim
e/te
mpe
ratu
re.
Stor
age
in r
etai
l ou
tlet
Gro
wth
of
sur
vivi
ng
path
ogen
ic
bact
eria
. Ti
me/
tem
pera
ture
.
Mon
itor
time/
tem
pera
ture
in
dica
tors
on
pac
kage
s. C
heck
te
mpe
ratu
re
of p
rodu
ct
at s
elec
ted
area
s in
tra
nspo
rt co
ntai
ner.
Keep
al
l chi
ll ch
ecks
. Not
e on
pro
duct
ion
reco
rd.
Advi
se t
rans
porte
r of
te
mpe
ratu
re
abus
e/pr
oduc
t/out
of
te
mpe
ratu
re
spec
ifica
tion.
Mon
itor
time/
tem
pera
ture
on
pac
kage
s. P
erfo
rm
rand
om
tem
pera
ture
ch
eck
on
prod
uct,
if pr
oduc
t te
mpe
ratu
re
grea
ter
than
4°
C re
com
men
ded
tem
pera
ture
, no
tify
stor
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Microbiological safety of sous vide processed meat product 197
these authors, there are four main levels of concern:
High Concern: An expert judgment that without control there is a life threa- tening risk;
Medium Concern: An expert judgment that there is a threat to consumer or to the product which must be controlled;
Low Concern: An expert judgment that there is little threat to the consumer or the product. It may still be advantageous to control;
No Concern: An Expert judgment that there is no threat to the consumer.
In any HACCP system, it is prudent to recognize that no system can give 100% security. Occasionally, products which pose a public health threat may appear on the market. It is essential for the industry to respond quickly to such threats and to implement a rapid and effective product recall plan. Each com- pany should have a detailed product recall plan. This includes the keeping of accurate process control and monitoring records for each batch of product. In addi- tion, proper preparation also includes identifying all internal and external per- sonnel involved in the recall, their func- tions and responsibilities and channels and means of communication. Mock recall plans should be.carried out on a regular basis to ensure the effectiveness of the plan in case of an emergency and also to modify and improve the plan where possible.
Conclusion While the HACCP concept is commonly used by the food canning industry to
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Acknowledgments The authors wish to thank Agriculture Canada and the Natural Sciences and En@- neering Research Council of Canada (NSERC) for funding this study.
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