Fish and Fishery Products Hazards and Controls Guidance

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse

This guidance represents the Food and Drug Administration’s (FDA’s) current thinking on this topic. It does not create or confer any rights for or on any person and does not operate to bind FDA or the public. You can use an alternative approach if the approach satisfies the requirements of the applicable statutes and regulations. If you want to discuss an alternative approach, contact the FDA staff responsible for implementing this guidance. If you cannot identify the appropriate FDA staff, call the telephone number listed on the title page of this guidance.

UNDERSTAND THE POTENTIAL HAZARD. Time and temperature abuse occurs when a product is allowed to remain at temperatures Pathogenic bacteria growth and toxin formation favorable to pathogenic bacteria growth for as a result of time and temperature abuse of fish sufficient time to result in unsafe levels of and fishery products can cause consumer illness. pathogenic bacteria or their toxins in the product. This hazard is limited to bacterial pathogens since Therefore, management of time and temperature viral pathogens (viruses) are not able to grow in of product exposure is important to producing food. Of particular concern in seafood are the a safe product. Table A-1 (Appendix 4) provides pathogenic forms of Listeria monocytogenes (L. guidance concerning the conditions under which monocytogenes), Vibrio vulnificus( V. vulnificus), certain pathogenic bacteria can grow. The bacteria Vibrio parahaemolyticus (V. parahaemolyticus), listed are those of greatest concern in fish and Vibrio cholera (V. cholera), Escherichia coli (E. fishery products. coli), Salmonella spp., Shigella spp., Staphylococcus Managing time and temperature of exposure aureus (S. aureus), Clostridium perfringens Time and temperature management relies (C. perfringens), Bacillus cereus (B. cereus), on identification of time and temperature Campylobacter jejuni (C. jejuni), and Yersinia combinations that ensure the safety of your enterocolitica (Y. enterocolitica). See Appendix 7 product. The following factors should be for a description of the public health impacts of considered: these pathogens. • The types of pathogenic bacteria that are Pathogenic bacteria can enter the process on raw reasonably likely to be present; materials. They can also be introduced into foods • Whether those pathogens can grow in the during processing from the air, unclean hands, food; insanitary utensils and equipment, contaminated water, or sewage and through cross-contamination • The infective dose of the pathogenic bacteria; between raw and cooked product. The primary • The expected initial level of the pathogenic method for control is to reduce levels through bacteria in the food. cooking or other treatments, when feasible, Presence of pathogenic bacteria minimize the potential for recontamination and to maintain products at temperatures that do not It is reasonable to assume that pathogenic bacteria support growth of pathogenic bacteria. of various types that are not associated with specific food sources, including those listed in Table A-1 (Appendix 4), will be present on raw fish

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 209 and fishery products and non-fishery ingredients. Table A-1 (Appendix 4) provides guidance They might be present only at low levels or only on some conditions that limit the growth sporadically, but even such occurrences warrant of those pathogenic bacteria that are most consideration because of the potential for growth relevant to fish and fishery products. Table A-1 and toxin production under temperature abuse provides minimum and maximum values of conditions. However, certain pathogenic bacteria pathogenic bacteria growth. This table can help are associated with specific food sources, and it you to decide whether particular pathogenic may not be necessary to assume that they will be bacteria will grow in your food if it is time and present in other foods unless introduced from a temperature-abused. contaminated source. For example, V. vulnificus, Certain pathogenic bacteria grow well in time V. parahaemolyticus, and V. cholerae non-O1 and temperature-abused raw fish and fishery and non-O139 are generally associated with products (e.g., raw molluscan shellfish), and marine and estuarine species of fish and not with freshwater species or non-fishery ingredients. others do not. Those that grow well in time and temperature-abused raw fish include: V. Pathogenic bacteria can also be introduced vulnificus, V. parahaemolyticus, V. cholerae, and during processing, even after cooking. Well- L. monocytogenes. Others may grow if the natural designed sanitation programs will minimize condition of the raw fish is changed, such as their introduction. However, in most cases, through salting or reduced oxygen packaging. it is not reasonable to assume that sanitation Those that ordinarily do not grow well, because programs will fully prevent the introduction of they compete poorly with the normal spoilage pathogenic bacteria. For this reason, controls bacteria, include: C. jejuni, pathogenic strains of should be in place to minimize the risk of E. coli, Salmonella spp., Shigella spp., S. aureus, pathogenic bacteria growth. C. perfringens, B. cereus, and Y. enterocolitica. Pathogenic bacteria growth Most pathogenic bacteria will grow well in Fish and fishery products generally provide temperature-abused cooked fish if their growth is sufficient nutrients for pathogenic bacteria not controlled by means such as drying, salting, growth. However, chemical and physical or acidification, because competing bacteria are characteristics of the product and its packaging destroyed by the cooking process. could limit or enhance pathogenic bacteria Infective dose growth and toxin formation. Furthermore, these characteristics could restrict competing The infective dose or toxic dose is the total microorganism growth and provide conditions number of a pathogen, or the total amount of a favorable to pathogenic bacteria growth. toxin, that is necessary to produce human illness. The dose often varies considerably for a single Consider: pathogen based on the health of the consumer • The moisture available to support pathogenic and the virulence (infective capacity) of the bacteria growth in the product (i.e., water particular strain of the pathogen. activity); The typical infectious dose is known or • The amount of salt and preservatives in the suspected to be very low (i.e., one to several product (e.g., water phase salt and nitrates); hundred organisms can cause illness) for

• The acidity of the product (i.e., pH); many of the pathogenic bacteria listed in Table • The availability of oxygen in the product A-1 (Appendix 4). These include C. jejuni, (i.e., aerobic or anaerobic conditions); E. coli, Salmonella spp., Shigella spp., and Y. • The presence of competing spoilage enterocolitica. The typical infectious dose for organisms in the food. other pathogenic bacteria is considered to be

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 210 somewhat higher (i.e., several thousand to less pathogenic bacteria that have a relatively high than 100,000). These include V. vulnificus and infective dose, the initial number of pathogenic V. parahaemolyticus. In the case of both of bacteria may be a significant consideration. these categories of pathogens, it is advisable to Practical considerations for unrefrigerated prevent any significant growth so that the typical processing infective dose is not exceeded. In other words, product temperatures should be maintained Consider the above described factors to identify below the minimum growth temperature for the the pathogen(s) that presents the greatest pathogen or should not be allowed to exceed challenge with respect to managing time and that temperature for longer than the lag growth temperature exposure in your product. This then phase (i.e., the slow growth phase during becomes the target pathogen(s) for time and which a pathogenic bacteria acclimates to its temperature control. Table A-2 (Appendix 4) can environment before proceeding to rapid growth) then be used to establish safe exposure times of the pathogenic bacteria at the exposure for the target pathogen(s) at the temperatures at temperature. which you expect your product to be exposed. Still other pathogenic bacteria require large As an alternative, you can use predictive numbers in order to cause disease. The typical microbiology models, such as the U.S. infectious dose of V. cholerae is suspected to be Department of Agriculture Pathogen Modeling 1,000,000 cells. S. aureus and B. cereus toxin do Program (http://ars.usda.gov/Services/docs. not normally produce sufficient toxin to cause htm?docid=6786) or ComBase (http://www. illness until numbers of the pathogen reach combase.cc/default.html) for product-specific 100,000 to 1,000,000/gram. time and temperature exposure calculations. However, you should validate the reliability of C. perfringens typically does not produce toxin predictions from such models for your food. in the human gut unless at least 100,000,000 bacteria are consumed. Limited growth of these Growth rates of pathogens are highly pathogens might not compromise the safety of temperature dependent. Ordinarily, pathogenic the product. However, time and temperature bacteria growth is relatively slow at temperatures controls must be adequate to prevent growth below 70°F (21.1°C). In most cases, growth is before the infectious or toxic dose is reached. very slow below 50°F (10°C), and 40°F (4.4°C) is below the minimum growth temperature of Levels of pathogenic bacteria most pathogenic bacteria, although there are The levels of a pathogen that are likely to be some exceptions. On the other hand, pathogenic present in a fish or fishery product is dependent bacteria grow relatively fast at temperatures on factors such as the quality of the harvest above 70°F (21.1°C). Product temperatures should water, how the raw material was handled be maintained below the minimum growth before it was delivered to your plant, and the temperature for the pathogen or should not be effectiveness of your sanitation control program. allowed to exceed that temperature for longer than the lag growth phase of the pathogen As a practical matter, the initial number of low growth cycle. to-moderate infectious dose pathogenic bacteria in a food is usually of limited importance when Consider the following recommendations when you develop a time and temperature management developing a product monitoring program. Product strategy because these pathogens should be surface temperature or ambient temperature controlled by a time and temperature strategy generally should be monitored when the ambient that does not permit their growth to pass the temperature (e.g., air) is warmer than the product lag phase. On the other hand, when controlling internal temperature. Internal temperature in the

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 211 center of the thickest part of the product should acidified products, and by Chapter 13 for be monitored when the ambient temperature refrigerated acidified products); (e.g., air, ice, and brine) is cooler than the product • Controlling the introduction of pathogenic internal temperature. Similarly, when selecting a bacteria after the pasteurization process product for temperature measurement, consider (covered in Chapter 18); the location of the product selected in relation to • Controlling the source of molluscan shellfish the environment and select the likely worse case and the time from exposure to air (e.g., by product. For example, a product in the center of harvest or receding tide) to refrigeration to a pile of products will take longer to cool than a control pathogens from the harvest area product at the surface. (covered in Chapter 4). • Strategies for control of pathogenic bacteria There are a number of strategies for the control DETERMINE WHETHER THE POTENTIAL of pathogenic bacteria in fish and fishery HAZARD IS SIGNIFICANT. products. They include: The following guidance will assist you in • Managing the amount of time that food is determining whether pathogenic bacteria growth exposed to temperatures that are favorable and toxin formation as a result of time and for pathogen growth and toxin production temperature abuse is a significant hazard at a (covered generally in this chapter; for processing step: Clostridium botulinum (C. botulinum), in Chapter 13; and for S. aureus in hydrated 1. Is it reasonably likely that unsafe levels of batter mixes, in Chapter 15); pathogenic bacteria will be introduced at this • Killing pathogenic bacteria by cooking processing step (do unsafe levels come in with the or pasteurization (covered in Chapter 16) raw material or will the process introduce them)? or by retorting (covered by the Thermally It is reasonable to assume that pathogenic Processed Low-Acid Foods Packaged in bacteria of various types that are not Hermetically Sealed Containers regulation, 21 associated with specific food sources, CFR 113 (hereinafter, the Low-Acid Canned including those listed in Table A-1 (Appendix Foods (LACF) Regulation); 4), will be present on raw fish and fishery • Killing pathogenic bacteria by processes products and non-fishery ingredients. that retain the raw product characteristics However, certain pathogenic bacteria are (covered in Chapter 17); associated with specific food sources, and it • Controlling the amount of moisture that is may not be necessary to assume that they available for pathogen growth (water activity) in will be present in other foods unless they the product by drying (covered in Chapter 14); have been cross-contaminated. For example, • Controlling the amount of moisture that is V. vulnificus, V. parahaemolyticus, and V. available for pathogen growth (water activity) cholerae non-O1 and non-O139 are generally in the product by formulation (covered in associated with marine and estuarine species Chapter 13); of fish and not with freshwater species or non-fishery ingredients. • Controlling the amount of salt or preservatives, such as sodium nitrite, in the Pathogenic bacteria also could be introduced product (covered in Chapter 13); during processing, even after cooking. Well- • Controlling the level of acidity (pH) in the designed sanitation programs (prerequisite product (covered by the Acidified Foods programs) will minimize the introduction of regulation, 21 CFR 114, for shelf-stable pathogenic bacteria. However, in most cases

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 212 it is not reasonable to assume that they will In summary, under ordinary circumstances fully prevent the introduction of pathogenic (e.g., without data to the contrary), you bacteria. Additional information on this should consider that it is reasonably likely topic is presented in the previous section, that a pathogenic bacteria in Table A-1 “Understand the Potential Hazard.” (Appendix 4) will grow to an unsafe level or produce toxin in your product at a particular 2. Is it reasonably likely that pathogenic bacteria processing step if all of the following will grow to unsafe levels and/or produce toxin conditions are met: at this processing step? • It is reasonably likely to be present; In order to answer this question, you must first determine which of those pathogenic • Its growth is not prevented by bacteria that are reasonably likely to be a condition of the food; present in your product would be able • It is reasonably likely that, in the to grow under time and temperature absence of controls, cumulative time abuse conditions. Information on this and temperature abuse conditions topic is presented in the previous section, such as those described in Table A-2 “Understand the Potential Hazard.” (Appendix 4) could occur during Time and temperature abuse at one step processing of the product, and the alone might not result in an unsafe product. processing step could contribute However, time and temperature abuse significantly to that cumulative abuse. that occurs at successive processing steps 3. Can unsafe levels of pathogenic bacteria and/ (including storage steps) might be sufficient or toxin production that are reasonably likely to to result in unsafe levels of pathogenic occur be eliminated or reduced to an acceptable bacteria or toxins. For this reason, you should level at this processing step? consider the cumulative effect of time and temperature abuse during the entire process. Pathogenic bacteria growth and toxin Table A-2 (Appendix 4) provides guidance formation due to time and temperature abuse about the kinds of time and temperature should be considered a significant hazard abuse that might cause a product to be at any processing step where a preventive unsafe. A study may need to be conducted to measure is, or can be, used to eliminate determine time and temperature exposure of the hazard (or reduce the likelihood of its your seafood to temperature abuse for each occurrence to an acceptable level) if it is process step. reasonably likely to occur. The preventive measures that can be applied for pathogenic Remember that you should consider the bacteria growth and toxin formation due to potential for time and temperature abuse in time and temperature abuse include: the absence of controls. You might already have controls in your process that minimize • Refrigeration of the product and the potential for time and temperature controlling refrigeration temperatures; abuse that could result in unsafe levels of • Proper icing of the product; pathogenic bacteria or toxins. This section and subsequent sections will help you • Controlling the amount of time that the determine whether those or other controls product is exposed to temperatures should be included in your Hazard Analysis that would permit pathogenic bacteria Critical Control Point (HACCP) plan. growth or toxin production; • Rapid cooling of the product;

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 213 • Ensuring that incoming fish the processor for culinary purposes (e.g., were handled properly during setting the batter or breading, or stabilizing refrigerated transportation from the the product shape), and are customarily previous processor, including: fully cooked by the consumer or end user. ° Controlling refrigeration temperatures Examples include: fish balls, shrimp egg rolls, during transit; shrimp and cheese stuffed ravioli, crab cakes, and breaded fish portions. Although the Proper icing during transit. ° exterior of these products may appear cooked, • Intended use the interior fish protein is not coagulated, and Except as noted, it is unlikely that the the products are not ready-to-eat. intended use will affect the significance of Other products contain a combination of the hazard. raw or partially cooked, and fully cooked FDA is not aware of any HACCP controls ingredients (e.g., seafood mixture of raw that exist internationally for the control oysters, cooked shrimp, and raw or cooked of pathogenic bacteria in fish and fishery octopus). Although the protein of some of products that are customarily fully cooked the fishery ingredients is coagulated, some is by the consumer or end user before not. As a result, many of these products are consumption, other than a rigorous sanitation not ready-to-eat. However, these combination regime as part of a prerequisite program products should be considered ready-to-eat or as part of HACCP itself. The Fish and if the raw or partially cooked ingredients are Fishery Products regulation, 21 CFR 123 customarily eaten without cooking by the (called the Seafood HACCP Regulation in consumer or end user. this guidance document) requires such a Note that the toxin produced by S. aureus regime. The proper application of sanitation is not destroyed by cooking or retorting. Its controls is essential because of the likelihood formation should, therefore, be prevented that pathogenic bacteria can be introduced in all fish and fishery products. However, as into fish and fishery products through previously mentioned, S. aureus does not poor handling practices by the aquaculture grow well in raw fish, unless the growth of producer, the fisherman, or the processor. competing spoilage organisms is inhibited (e.g., FDA is interested in information regarding any by salting or vacuum packaging). B. cereus also HACCP controls beyond sanitation that could produces a heat-stable toxin and forms heat- be necessary and practical for the control resistant spores that can survive cooking. of pathogenic bacteria in fish and fishery products that are customarily fully cooked by the consumer or end user. However, the agency makes no recommendations in this guidance document and has no specific expectations with regard to such controls in processors’ HACCP plans. The agency plans to develop Good Manufacturing Practice guidelines for harvest vessels and for aquaculture in an effort to minimize the likelihood that these operations will contribute pathogens to fish and fishery products. Some products are partially cooked by

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 214 IDENTIFY CRITICAL CONTROL POINTS. identify as a CCP each processing step at which you have identified this hazard as significant. You The following guidance will assist you in should control cumulative exposure of the product determining whether a processing step is a to time and temperatures that will permit growth critical control point (CCP) for pathogenic or toxin formation at these steps. bacteria growth and toxin formation as a result of Example: time and temperature abuse: A crabmeat processor identifies a series 1. If there is a cook step, pasteurization step, or of post-cook processing and storage retorting step later in your manufacturing process, steps (e.g., backing, picking, packing, you should, in most cases, identify that step as and refrigerated storage) as presenting the CCP. You would not usually need to identify a reasonable likelihood of pathogenic processing steps prior to cooking, pasteurization, bacteria growth and toxin formation. or retorting as CCPs for this hazard. The processor does not subject the product to a final pasteurization process and Example: recognizes that it might be consumed A cooked shrimp processor should set without further cooking. The processor the critical control point for pathogenic controls the temperature during bacteria growth and toxin formation as refrigerated storage and the time of a result of time and temperature abuse exposure to unrefrigerated conditions at the cook step. The processor would not during the processing steps. The processor need to identify each of the processing should identify each of the post-cook steps prior to cooking as CCPs. processing and storage steps as CCPs for Guidance for this pathogen control strategy this hazard. is contained in Chapter 16 (for cooking and This chapter provides the following four pasteurization) and the LACF Regulation, 21 control approaches, or control strategies, each CFR 113 (for retorting). relating to a separate potential CCP or a set However, there are two important limitations of CCPs: to this strategy: • “Control Strategy Example 1 - Transit • The cooking, pasteurizing, or retorting Control.” This control strategy should process must be sufficient to eliminate be applied to the control of transit at the most resistant pathogenic bacteria receipt of chilled (i.e., refrigerated, of public health concern that are iced, or held under chemical cooling reasonably likely to be present; media, such as gel packs, and not frozen) ready-to-eat fishery products; • Certain toxins (e.g., S. aureus and B. cereus toxins) are heat stable. Heat • “Control Strategy Example 2 - treatment, including retorting, might not Refrigerated Storage and Refrigerated eliminate the toxin once it is formed. Processing Control.” This control strategy should be applied to chilled In either case, time and temperature control (i.e., refrigerated, iced, and not would be necessary at the processing steps frozen) storage and refrigerated at which growth and toxin formation could (i.e., <40ºF (4.4ºC)) processing; occur. • “Control Strategy Example 3 - Cooling 2. If there is no cook step, pasteurization step, or After Cooking Control.” This control retorting step later in the process, you should strategy should be applied to a cooling

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 215 step when there is no significant In some cases, refrigerated cooked, ready- handling during the cooling and to-eat foods (e.g., lobster meat, pasteurized there is a need to control spore- crabmeat, smoked fish, and surimi-based forming pathogenic bacteria; analog products) are received by a secondary processor and held for sale without further • “Control Strategy Example 4 - handling. In other cases, these products Unrefrigerated Processing Control.” are received by a secondary processor and This control strategy should be used as ingredients in a ready-to-eat product applied to unrefrigerated (i.e., that will not be cooked or pasteurized by ≥40ºF (4.4ºC)) processing. that processor (e.g., seafood salad). In these Following is further guidance that may help cases, the receiving and storage steps by the you determine whether these processing secondary processor should be designated steps should be identified as CCPs for this as CCPs to control the hazard of pathogenic hazard. The guidance is divided into two bacteria growth. On the other hand, if types of finished products: cooked ready-to these ready-to-eat foods are received by the eat and raw ready-to-eat. secondary processor to be used in a product that will be cooked or pasteurized by that • Cooked, ready-to-eat products processor, the receiving and storage steps These products may be cooked by the before the cooking or pasteurization step processor, received by the processor already might not need to be designated as CCPs, cooked, or assembled by the processor from unless S. aureus or B. cereus toxin formation ready-to-eat components. They may appear is a significant hazard. Remember that these to the consumer or end user to be ready-to toxins are not likely to be inactivated by heat. eat products and may, therefore, be eaten without further cooking. Examples include: In still other cases, ready-to-eat foods are cooked crabmeat, lobster meat, and crayfish received by a secondary processor and meat; surimi-based analog products; seafood used as ingredients in a non-ready-to-eat salads; and hot-smoked fish. Note that product (e.g., cooked octopus used by the smoked fish is also covered in Chapter 13, processor as an ingredient in a seafood mix and cooking and pasteurization are covered that is customarily eaten after cooking by the in Chapter 16. consumer or end user). Again, the receiving and storage steps might not need to be Cooked, ready-to-eat products, especially designated as CCPs, unless S. aureus or B. assembled products, might develop pathogen cereus toxin formation is a significant hazard. hazards as a result of cross-contamination and growth. Contributing factors to this The need to establish a CCP at cooling after risk are manual handling steps, multiple cooking or pasteurization depends on: ingredients, unrefrigerated processing, and • The severity of the cooking (including multiple cooling steps. Cumulative exposure hot smoking) or pasteurization step; to time and temperature abuse after the • The extent to which the product cook step should be taken into consideration is handled between the end of the when establishing CCPs based on time and cooking or pasteurization step and temperature. the end of the cooling step. Spore-forming pathogenic bacteria may survive cooking or pasteurization processes that target vegetative pathogenic bacteria.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 216 For example, in foods that contain meat or Time and temperature controls may be rice, spores of C. perfringens and B. cereus needed at the following steps (CCPs): could be present, could survive the cooking • Receiving; process, and could grow and produce toxin in the product during cooling and subsequent • Thawing; handling. In fact, the heat from the cooking • Cooling after cooking; process might initiate growth of the surviving spores. In this case, a CCP may be needed • Processing after cooking: at product cooling. However, some cooking ° Slicing hot-smoked salmon; processes might be adequate to kill even the ° Mixing seafood salad; spores of C. perfringens and B. cereus. In this Picking crabmeat; case, a CCP at product cooling may not be ° necessary. • Packaging; When significant handling occurs after • In-process and finished product cooking or pasteurization, there is a risk refrigerated (not frozen) storage. that the product might be recontaminated Time and temperature controls will usually with pathogenic bacteria. Because many of not be needed at processing steps that meet the normally occurring spoilage organisms the following conditions: may have been eliminated by the cooking or pasteurization process and are no longer • Continuous, mechanical present to compete with the pathogenic processing steps that are brief: bacteria, rapid growth and toxin formation ° Mechanical size grading of cooked by the pathogenic bacteria are possible. It shrimp; is advisable to fully cool a product before ° Mechanical forming of surimi-based it is further handled, in order to minimize analog products; pathogenic bacteria growth and toxin Individual quick freezing; formation. When significant handling occurs ° after the heating process but before the • Processing steps that are brief and completion of the cooling process or when unlikely to contribute significantly to the cooked product comes into contact with the cumulative time and temperature equipment that was not heated along with exposure to unrefrigerated conditions: the product, time and temperature exposure ° Date code stamping; controls may need to start at that point. In ° Case packing; some processes, cooling is performed (1) • Processing steps where the product before any significant handling of the cooked is held in a frozen state: product; and (2) in the same container in which the product was cooked. Under ° Glazing; these conditions, cooling after cooking may ° Assembly of orders for distribution; not need to be identified as a CCP for this ° Frozen product storage; hazard. However, such a determination is dependent upon strict adherence to good • Processing steps where the sanitation practices to further minimize the product is held at temperatures risk of recontamination with pathogenic above 135°F (57.2°C): bacteria. ° Initial stage of cooling; ° Hot holding.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 217 • Raw, ready-to-eat products Time and temperature controls will usually These products are not heated during not be needed at processing steps that meet processing to a temperature that destroys the following conditions: pathogenic bacteria. They are often • Continuous, mechanical consumed without cooking. Examples processing steps that are brief: include: cold-smoked fish, raw oysters, Mechanical filleting; clams and mussels, and raw finfish (when ° the processor has knowledge or has reason • Processing steps that are brief and to know that the product will be consumed unlikely to contribute significantly to without a process sufficient to kill pathogens the cumulative time and temperature of public health concern or where the exposure to unrefrigerated conditions: processor represents, labels, or intends for ° Date code stamping; the product to be so consumed). ° Case packing; Like cooked, ready-to-eat products, raw • Processing steps where the product ready-to-eat products may contain pathogenic is held in a frozen state: bacteria as a result of near-shore harvest Assembly of orders for distribution; water contamination, poor aquaculture ° practices, or poor sanitary practices during ° Frozen storage. harvesting, transportation, or processing. • Time and temperature profile For example, oysters, especially those harvested during the warm weather Preparing a diagram that depicts the months, might contain V. vulnificus or maximum times and temperatures at which V. parahaemolyticus. Raw finfish might your product will be exposed at each contain V. parahaemolyticus, Salmonella processing step may help you determine spp., or L. monocytogenes. Some of these cumulative product exposure, especially if pathogenic bacteria (e.g., V. vulnificus, V. your product is cooked, ready-to-eat. This parahaemolyticus, and L. monocytogenes) are diagram can help you identify CCPs, as capable of growth in raw fish. well as critical limits, as will be discussed later. Figures 12-1 and 12-2 are examples Time and temperature controls may be needed of time and temperature profiles for two at the following processing steps (CCPs): different crabmeat processes. Although the • Receiving; figures show similar time and temperature profiles, they demonstrate how differences in • Processing: processing operations, especially with respect ° Thawing; to when significant handling occurs, can have ° Shucking; an impact on the location of CCPs and on the ° Portioning; critical limits at those CCPs. • Packaging; Figure 12-1 shows a time and temperature profile for a cooked crabmeat processor that • Raw material, in-process product, significantly handles product before it is and finished product refrigerated cooled to 50°F (10°C). As a result, a CCP is (not frozen) storage. likely to be needed at backing, picking, and packing.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 218 Figure 12-2 shows a time and temperature handling occurs. A more restrictive set of profile for a cooked crabmeat processor that critical limits is also likely for the product does not significantly handle product before depicted by Figure 12-1 than for that depicted it is cooled to 50°F (10°C). As a result, a CCP by Figure 12-2, because the former product is is not needed until the picking operation, handled while still warm. which is the first point at which significant

FIGURE 12-1: Internal Temperature Proﬁle — Blue Crabmeat Processing Partial Cooling Only After Cook With Signiﬁcant Handling Before Full Cooling

135˚F (57.2˚C)

Backing Begins Place in Cooler Picking Begins Packing Ends

80˚F (26.7˚C) 70˚F (21.1˚C)

50˚F (10˚C)

40˚F (4.4˚C)

1 HR. 2 HOURS MAX. MAX. 1 HR. MAX. FIGURE 12-2: Internal Temperature Proﬁle — Blue Crabmeat Processing Cooling After Cook in Original Container With No Signiﬁcant Handling During Cooling

135˚F (57.2˚C) Cooling in Original Container No Signiﬁcant Handling Picking Begins Packing Ends 80˚F (26.7˚C) 70˚F (21.1˚C)

50˚F (10˚C)

40˚F (4.4˚C)

5 HOURS MAX.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 219 DEVELOP A CONTROL STRATEGY. OR • For products delivered under ice: The following guidance provides examples of four ° Product is completely surrounded by ice control strategies for pathogenic bacteria growth at the time of delivery; and toxin formation. It may be necessary to select OR more than one control strategy in order to fully control the hazard, depending upon the nature of • For products delivered under chemical your operation. You may select a control strategy cooling media, such as gel packs: that is different from those which are suggested, ° There is an adequate quantity of cooling provided it complies with the requirements of the media that remain frozen to have applicable food safety laws and regulations. maintained the product at an internal temperature of 40°F (4.4°C) or below The following are examples of control strategies throughout transit; included in this chapter: AND MAY APPLY TO MAY APPLY TO The internal temperature of the product CONTROL STRATEGY PRIMARY SECONDARY ° PROCESSOR PROCESSOR at the time of delivery is 40°F (4.4°C) or Transit control  below; Refrigerated storage and   OR refrigerated processing control • For products delivered refrigerated (not frozen) with a transit time (including all Cooling after cooking   control time outside a controlled temperature Unrefrigerated processing   environment) of 4 hours or less (optional control control strategy): ° Time of transit does not exceed 4 hours; • CONTROL STRATEGY EXAMPLE 1 - TRANSIT AND CONTROL (FOR REFRIGERATED (NOT FROZEN) COOKED, READY-TO-EAT OR RAW, READY-TO ° Internal temperature of the product at EAT FISHERY PRODUCTS TO BE STORED OR the time of delivery does not exceed PROCESSED WITHOUT FURTHER COOKING) 40°F (4.4°C). It may be necessary to select more than one Note: Processors receiving product with transit times of 4 hours or less may elect to use one of the controls described for longer transit control strategy in order to fully control the times instead. hazard, depending upon the nature of your operation. Establish Monitoring Procedures.

Set Critical Limits. » What Will Be Monitored? • For fish or fishery products delivered • For products delivered refrigerated (not refrigerated (not frozen): frozen): ° All lots received are accompanied by ° The internal temperature of the product transportation records that show that the throughout transportation; product was held at or below an ambient OR or internal temperature of 40°F (4.4°C) throughout transit. Note that allowance ° The ambient temperature within the for routine refrigeration defrost cycles truck or other carrier throughout may be necessary; transportation;

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 220 OR OR • For products delivered under ice: • For products delivered under chemical ° The adequacy of ice surrounding the cooling media, such as gel packs: product at the time of delivery; ° Make visual observations of the adequacy and frozen state of the cooling OR media in a representative number of • For products held under chemical cooling containers (e.g., cartons and totes) from media, such as gel packs: throughout the shipment at delivery; The quantity and frozen status of cooling ° AND media at the time of delivery; ° Use a temperature-indicating device (e.g., AND a thermometer) to determine internal ° The internal temperature of a product temperatures in a representative representative number of product units at number of product containers from time of delivery; throughout the shipment at delivery; OR OR • For products delivered refrigerated (not • For products delivered refrigerated (not frozen) with a transit time of 4 hours or less: frozen) with a transit time of 4 hours or less: ° The date and time product was ° Review carrier records to determine the removed from a controlled temperature date and time product was removed from environment before shipment and the a controlled temperature environment date and time delivered; before shipment and the date and time AND delivered; ° The internal temperature of a AND representative number of product ° Use a temperature-indicating device (e.g., containers (e.g., cartons and totes) at the a thermometer) to determine internal time of delivery. product temperatures in a representative number of product containers (e.g., » How Will Monitoring Be Done? cartons and totes) randomly selected • For products delivered refrigerated (not from throughout the shipment, at frozen): delivery. Measure a minimum of 12 ° Use a continuous temperature-recording product containers, unless there are device (e.g., a recording thermometer) fewer than 12 products in a lot, in which for internal product temperature or case measure all of the containers. Lots ambient air temperature monitoring that show a high level of temperature during transit; variability may require a larger sample OR size. • For products delivered under ice: » How Often Will Monitoring Be Done (Frequency)? ° Make visual observations of the • Every lot received. adequacy of ice in a representative number of containers (e.g., cartons and » Who Will Do the Monitoring? totes) from throughout the shipment at • For continuous temperature-recording delivery; devices:

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 221 ° Monitoring is performed by the device AND itself. The visual check of the data Take the following corrective action to regain control generated by the device, to ensure that over the operation after a critical limit deviation: the critical limits have consistently been met, may be performed by any person • Discontinue use of the supplier or carrier who has an understanding of the nature until evidence is obtained that the identified of the controls; transportation- handling practices have been improved. OR • For other checks: Establish a Recordkeeping System. ° Any person who has an understanding of • Receiving records showing: the nature of the controls. ° The results of continuous temperature monitoring, including: Establish Corrective Action Procedures. • Printouts, charts, or readings from Take the following corrective action to a product temperature-recording devices; involved in a critical limit deviation: AND • Chill and hold the affected product until an evaluation of the total time and temperature • Visual check of recorded data; exposure is performed (a product with OR cumulative exposures that exceed the critical The results of ice checks, including: limits recommended in “Control Strategy ° Example 4 - Processing Controls” should be • The number of containers (e.g., cooked or diverted to a use in which the cartons and totes) examined and critical limit is not applicable (e.g., divert the sufficiency of ice for each; crabmeat to a stuffed flounder operation), AND after giving consideration to the fact that any S. aureus or B. cereus toxin that may be • The number of containers (e.g., present may not be inactivated by heat, or cartons and totes) in the lot; destroyed or diverted to a non-food use); OR OR ° The results of chemical media checks, • Cook the product, after giving consideration including: to the fact that any S. aureus or B. cereus • The number of containers (e.g., toxin that may be present may not be cartons and totes) examined and the inactivated by heat; frozen status of the media for each; OR AND • Divert the product to a use in which the • The number of units in the lot; critical limit is not applicable (e.g., divert crabmeat to a stuffed flounder operation), AND/OR after giving consideration to the fact that ° The results of internal product any S. aureus or B. cereus toxin that may be temperature monitoring, including: present may not be inactivated by heat; • The number of containers (e.g., OR cartons and totes) examined • Reject the lot. and the internal temperatures observed for each;

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 222 AND kinks. The device should be checked to ensure that it is operational; • The number of containers (e.g., cartons and totes) in the lot; AND AND • Calibrate the temperature-indicating device against a known accurate reference device • Date and time product was (e.g., a NIST-traceable thermometer) at initially removed from a controlled least once a year or more frequently if temperature environment and recommended by the device manufacturer. date and time product was Optimal calibration frequency is dependent delivered, when applicable. upon the type, condition, past performance, and conditions of use of the device. Establish Verification Procedures. Consistent temperature variations away from • Before a temperature-indicating device (e.g., the actual value (drift) found during checks a thermometer) is put into service, check and/or calibration may show a need for more the accuracy of the device to verify that the frequent calibration or the need to replace factory calibration has not been affected. the device (perhaps with a more durable This check can be accomplished by: device). Calibration should be performed at ° Immersing the sensor in an ice slurry a minimum of two temperatures that bracket (32°F (0°C)) if the device will be used at the temperature range at which it is used; or near refrigeration temperature; AND OR • Check the accuracy of temperature-recording ° Comparing the temperature reading on devices that are used for monitoring transit the device to the reading on a known conditions upon receipt of each lot. The accurate reference device (e.g., a accuracy of the device can be checked thermometer traceable to standards of by comparing the temperature reading on the National Institute of Standards and the device with the reading on a known Technology (NIST)) under conditions that accurate reference device (e.g., a NIST- are similar to how it will be used (e.g., traceable thermometer) under conditions that product internal temperature) within the are similar to how it will be used (e.g., air temperature range at which it will be temperature) within the temperature range at used; which it will be used; AND AND • Once in service, check the temperature- • When visual checks of ice or cooling media indicating device daily before the beginning of are used, periodically measure internal operations. Less frequent accuracy checks may temperatures of fish to ensure that the ice be appropriate if they are recommended by or cooling media are sufficient to maintain the instrument manufacturer and if the history product temperatures at 40°F (4.4°C) or less; of use of the instrument in your facility has AND shown that the instrument consistently remains • Review monitoring, corrective action, accurate for a longer period of time. In addition and verification records within 1 week of to checking that the device is accurate by one preparation to ensure they are complete and of the methods described above, this process any critical limit deviations that occurred should include a visual examination of the were appropriately addressed. sensor and any attached wires for damage or

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 223 CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse Abuse Temperature and Time of aResult as botulinum) Clostridium Than (Other Toxin and Formation Growth 12:CHAPTER Bacteria Pathogenic TABLE 12-1

CONTROL STRATEGY EXAMPLE 1 - TRANSIT CONTROL

This table is an example of a portion of a HACCP plan using “Control Strategy Example 1 - Transit Control.” This example illustrates how a processor receiving pasteurized crabmeat can control pathogenic bacteria growth and toxin formation as a result of time and temperature abuse during transit. It is provided for illustrative purposes only. It may be necessary to select more than one control strategy in order to fully control the hazard, depending upon the nature of your operation.

Pathogenic bacteria growth and toxin formation may be only one of several significant hazards for this product. Refer to Tables 3-3 and 3-4 (Chapter 3) for other potential hazards (e.g., environmental chemical contaminants and pesticides, pathogen survival through cooking and pasteurization, and metal fragments).

Example Only See Text for Full Recommendations

(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)

CRITICAL LIMITS MONITORING CRITICAL SIGNIFICANT FOR EACH CORRECTIVE CONTROL RECORDS VERIFICATION HAZARD(S) PREVENTIVE ACTION(S) POINT WHAT HOW FREQUENCY WHO MEASURE

Receiving Pathogenic All lots received Temperature Digital time and Continuous, Receiving Reject the Data Check pasteurized bacteria growth are of truck temperature with visual employee shipment logger printout accuracy of the crabmeat and toxin accompanied refrigerated data logger review and temperature 224 formation by truck compartment evaluation of Discontinue use data logger records that temperature of the upon show monitoring supplier or receipt of each temperature records for each carrier until lot was maintained shipment evidence is at or below obtained that Review 40°F the identifi ed monitoring, transportation- corrective handling action, and practices have verification been improved records within 1 week of preparation • CONTROL STRATEGY EXAMPLE 2 - REFRIGERATED • For raw material, in-process product, or STORAGE AND REFRIGERATED PROCESSING finished product stored under ice: CONTROL ° The product is completely and It may be necessary to select more than one continuously surrounded by ice control strategy in order to fully control the throughout the storage time. hazard, depending upon the nature of your operation. Establish Monitoring Procedures.

Set Critical Limits. » What Will Be Monitored? • For refrigerated (not frozen) storage or • For refrigerated storage or processing: processing of the raw material, in-process ° The ambient air temperature of the product, or finished product: cooler or refrigerated processing room; ° The product is held at a cooler ambient OR air temperature of 40°F (4.4°C) or • For storage under ice: below. Note that allowance for routine refrigeration defrost cycles may be ° The adequacy of ice surrounding the necessary. On the other hand, minor product. variations in cooler temperature » How Will Monitoring Be Done? measurements can be avoided • For refrigerated storage or processing: by submerging the sensor for the temperature-recording device (e.g., a ° Use a continuous temperature-recording recording thermometer) in a liquid that device (e.g., a recording thermometer); mimics the characteristics of the product. OR Also note that critical limits during • For storage under ice: refrigerated storage and refrigerated Make visual observations of the processing that specify a cumulative ° adequacy of ice in a representative time and temperature of exposure to number of containers (e.g., cartons and temperatures above 40°F (4.4°C) are not totes) from throughout the cooler. ordinarily suitable to control the hazard because of the difficulty in tracking » How Often Will Monitoring Be Done (Frequency)? the specific products and the specific • For continuous temperature recording cumulative temperature exposures devices: that those products experience. The cumulative exposure for each product ° Continuous monitoring by the device would need to be determined prior to itself, with a visual check of the recorded shipping. If you chose this approach, data at least once per day; the critical limit for cumulative exposure OR to temperatures above 40°F (4.4°C) • For storage under ice: should include time during transit, Sufficient frequency to ensure the critical refrigerated storage, and refrigerated and ° limit is met. unrefrigerated processing; OR

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 225 » Who Will Do the Monitoring? OR • For continuous temperature-recording • Destroy the product; devices: OR ° Monitoring is performed by the device • Divert the product to a non-food use. itself. The visual check of the data generated by the device, to ensure that AND the critical limits have consistently been Take the following corrective actions to regain control met, may be performed by any person over the operation after a critical limit deviation: who has an understanding of the nature • Prevent further deterioration of the product: of the controls; ° Add ice to the product; OR OR • For other checks: ° Move some or all of the product in the ° Any person who has an understanding of malfunctioning cooler to another cooler; the nature of the controls. OR Establish Corrective Action Procedures. ° Freeze the product; Take the following corrective action to a product AND involved in a critical limit deviation: • Address the root cause: • Chill and hold the affected product ° Make repairs or adjustments to the until an evaluation of the total time and malfunctioning cooler; temperature exposure is performed. A product with cumulative exposures that OR exceed the critical limits recommended in ° Make adjustments to the ice application “Control Strategy Example 4 - Unrefrigerated operations. Processing Controls,” should be cooked or diverted to a use in which the critical limit Establish a Recordkeeping System. is not applicable (e.g., divert crabmeat to • For refrigerated storage: a stuffed flounder operation), after giving Printouts, charts, or readings from consideration to the fact that any S. aureus ° continuous temperature-recording devices; or B. cereus toxin that may be present may not be inactivated by heat, or destroyed or AND diverted to a non-food use; ° Record of visual checks of recorded data; OR OR • Cook the product, after giving consideration • For storage under ice: to the fact that any S. aureus or B. cereus The results of ice checks: toxin that may be present may not be ° inactivated by heat; • The number of containers (e.g., cartons and totes) examined and OR the sufficiency of ice for each; • Divert the product to a use in which the critical limit is not applicable (e.g., divert AND crabmeat to a stuffed flounder operation), • The approximate number after giving consideration to the fact that of containers (e.g., cartons any S. aureus or B. cereus toxin that may be and totes) in the cooler. present may not be inactivated by heat;

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 226 Establish Verification Procedures. Consistent temperature variations away from • Before a temperature-recording device (e.g., the actual value (drift) found during checks a recording thermometer) is put into service, and/or calibration may show a need for more check the accuracy of the device to verify frequent calibration or the need to replace that the factory calibration has not been the device (perhaps with a more durable affected. This check can be accomplished by: device). Calibration should be performed at a minimum of two temperatures that bracket Immersing the sensor in an ice slurry ° the temperature range at which it is used; (32°F (0°C)) if the device will be used at or near refrigeration temperature; AND OR • When visual checks of ice are used, periodically measure internal temperatures Comparing the temperature reading ° of fish to ensure that the ice is sufficient to on the device with the reading on a maintain product temperatures at 40°F (4°C) known accurate reference device (e.g., or less; a NIST-traceable thermometer) under conditions that are similar to how it will AND be used (e.g., air temperature) within • Review monitoring, corrective action, the temperature range at which it will be and verification records within 1 week of used; preparation to ensure they are complete and AND any critical limit deviations that occurred were appropriately addressed. • Once in service, check the temperature- recording device daily before the beginning of operations. Less frequent accuracy checks may be appropriate if they are recommended by the instrument manufacturer and the history of use of the instrument in your facility has shown that the instrument consistently remains accurate for a longer period of time. In addition to checking that the device is accurate by one of the methods described above, this process should include a visual examination of the sensor and any attached wires for damage or kinks. The device should be checked to ensure that it is operational and, where applicable, has sufficient ink and paper; AND • Calibrate the temperature-recording device against a known accurate reference device (e.g., a NIST-traceable thermometer) at least once a year or more frequently if recommended by the device manufacturer. Optimal calibration frequency is dependent upon the type, condition, past performance, and conditions of use of the device.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 227 CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse Abuse Temperature and Time of aResult as botulinum) Clostridium Than (Other Toxin and Formation Growth 12:CHAPTER Bacteria Pathogenic TABLE 12-2

CONTROL STRATEGY EXAMPLE 2 - REFRIGERATED STORAGE AND REFRIGERATED PROCESSING CONTROL (ICING MODEL)

This table is an example of a portion of a HACCP plan using “Control Strategy Example 2 - Refrigerated Storage and Refrigerated Processing Control (Icing Model).” This example illustrates how a blue crabmeat processor can control pathogenic bacteria growth and toxin formation as a result of time and temperature abuse during icing. It is provided for illustrative purposes only. It may be necessary to select more than one control strategy in order to fully control the hazard, depending upon the nature of your operation.

Example Only See Text for Full Recommendations

(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)

MONITORING CRITICAL LIMITS CRITICAL SIGNIFICANT FOR EACH CORRECTIVE CONTROL RECORDS VERIFICATION HAZARD(S) PREVENTIVE ACTION(S) POINT WHAT HOW FREQUENCY WHO 228 MEASURE

Finished Pathogenic Finished Adequacy of ice Visual Each case Production Re-ice the Ice storage Check internal product cooler bacteria growth product observation immediately employee product record temperature of and toxin containers before iced crabmeat formation completely shipping Hold and weekly surrounded evaluate with ice based on Review total time and monitoring, temperature corrective exposure action, and verification records within 1 week of preparation CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse Abuse Temperature and Time of aResult as botulinum) Clostridium Than (Other Toxin and Formation Growth 12:CHAPTER Bacteria Pathogenic TABLE 12-3

CONTROL STRATEGY EXAMPLE 2 - REFRIGERATED STORAGE AND REFRIGERATED PROCESSING CONTROL (REFRIGERATION MODEL)

This table is an example of a portion of a HACCP plan using “Control Strategy Example 2 - Refrigerated Storage and Refrigerated Processing Control (Refrigeration Model).” This example illustrates how a blue crabmeat processor can control pathogenic bacteria growth and toxin formation as a result of time and temperature abuse during refrigerated storage. It is provided for illustrative purposes only.

Example Only See Text for Full Recommendations

(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)

MONITORING CRITICAL LIMITS CRITICAL SIGNIFICANT FOR EACH CORRECTIVE CONTROL RECORDS VERIFICATION HAZARD(S) PREVENTIVE ACTION(S) POINT WHAT HOW FREQUENCY WHO MEASURE 229

Finished Pathogenic Cooler Cooler Digital time and Continuous, Production Move to Data Check the product cooler bacteria growth maintained temperature temperature with visual employee alternate cooler logger printout data logger for and toxin at or below data logger check of and/or add ice accuracy and formation 40°F recorded data Record or visual damage and to once per day Hold and checks ensure that it evaluate based is operational on total time before putting and into operation; temperature check it exposure daily, at the beginning of operations; and calibrate it once per year

Review monitoring, corrective action, and verification records within 1 week of preparation • CONTROL STRATEGY EXAMPLE 3 - COOLING OR AFTER COOKING CONTROL • Use appropriate instruments (e.g., a It may be necessary to select more than one temperature-indicating device, such as a control strategy in order to fully control the hazard, thermometer, a continuous temperature- depending upon the nature of your operation. recording device, such as a time and temperature data logger, a scale) and/or Set Critical Limits. visual observations as necessary to measure • The product is cooled from 135°F (57.2°C) to the critical factors of the process that affect 70°F (21.1°C) within 2 hours; the rate of cooling, as established by a cooling rate study. AND • The product is further cooled from 135°F Example: (57.2°C) to 40°F (4.4°C) within an additional A crayfish processor identifies cooling 4 hours; after the cook step as a CCP for pathogenic bacteria growth and toxin OR formation. The processor establishes a • The minimum or maximum values for the cooling critical limit of no more than critical factors of the process that affect the 2 hours from 135°F (57.2°C) to 70°F rate of cooling, as established by a cooling (21.1°C) and no more than 4 more rate study (e.g., product internal temperature hours from 70°F (21.1°C) to 40°F at the start of cooling, cooler temperature, (4.4°C). The processor uses marked quantity of ice, quantity or size of the batches of cooked product to monitor product being cooled, product formulation, the cooling process. The time that the configuration of the product in the cooler). marked batch is removed from the cooker is monitored visually, and the Establish Monitoring Procedures. internal temperature of the product in that batch 2 hours after cooking and 4 » What Will Be Monitored? more hours after cooking is monitored • The length of the cooling cycle and the with a dial thermometer. internal temperature of the product; Example: OR Another crayfish processor has similarly • The critical factors of the process that affect identified cooling after cooking as the rate of cooling, as established by a a CCP and has established the same cooling rate study. critical limit. The processor uses a digital time and temperature data logger » How Will Monitoring Be Done? to monitor the cooling rate of the cooked • Clock; product. AND Example: • Use a temperature-indicating device (e.g., a Another crayfish processor has similarly thermometer) and visual check on time of identified cooling after cooking as a CCP. cooling; This processor has performed a cooling rate study that determined that a cooling OR rate of no more than 2 hours from 135°F • Use a continuous temperature-recording device (57.2°C) to 70°F (21.1°C) and no more (e.g., time and temperature data logger); than 4 more hours from 70°F (21.1°C) to 40°F (4.4°C) can be achieved as long as

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 230 certain conditions are met in the cooling Establish Corrective Action Procedures. process. The study determined that the following critical limits must be met: Take the following corrective action to a product a cooler temperature of no more than involved in a critical limit deviation: 60°F (15.6°C) during the first 2 hours of • Recook the product, after giving cooling and no more than 40°F (4.4°C) consideration to the fact that any S. aureus during the remainder of cooling; and toxin that may be present may not be no more than 1,000 pounds of crayfish inactivated by heat; in the cooler. The processor monitors OR the cooler temperature with a recording • Divert the product to a use in which the thermometer and monitors the weight of critical limit is not applicable (e.g., divert the product at receiving with a scale. crabmeat to a stuffed flounder operation), » How Often Will Monitoring Be Done (Frequency)? after giving consideration to the fact that any • For temperature-indicating devices: B. cereus toxin that may be present may not be inactivated by heat; ° At least every 2 hours; OR OR • Destroy the product; • For temperature-recording devices: ° At least every 2 hours a device is placed OR in the product. It provides continuous • Divert the product to a non-food use. monitoring, which is visually checked at AND the end of the cooling period; Take the following corrective actions to regain control OR over the operation after a critical limit deviation: • For critical aspects of the cooling process: • Prevent further deterioration of the product: ° As often as necessary to ensure control Add ice to the product; of the process. ° AND » Who Will Do the Monitoring? • Address the root cause: • For temperature-recording devices: ° Make repairs or adjustments to the ° Monitoring is performed by the device malfunctioning cooler; itself. The visual check of the data OR generated by the device, to ensure that the critical limits have consistently been • Make adjustments to the ice application met, may be performed by any person operation. who has an understanding of the nature of the controls; Establish a Recordkeeping System. • For temperature-indicating devices: OR Cooling records showing the internal • For other checks: ° temperature of the product, and the ° Any person who has an understanding of length of time between the end of the the nature of the controls. cooking (or the time that the product internal temperature falls below 135°F (57.2°C)), and the time that the measurement was made;

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 231 OR (e.g., product internal temperature) • For temperature-recording devices: within the temperature range at which it will be used; ° Record of continuous temperature monitoring; AND AND • Once in service, check the temperature- indicating device or temperature-recording Record of visual checks of recorded data; ° device daily before the beginning of OR operations. Less frequent accuracy checks may • For the critical factors of the process that be appropriate if they are recommended by affect the rate of cooling, as established by a the instrument manufacturer and the history cooling rate study: of use of the instrument in your facility has ° Appropriate records (e.g., processing shown that the instrument consistently remains record showing the results of the time accurate for a longer period of time. In addition and temperature checks and/or volume to checking that the device is accurate by one of product in cooler). of the methods described above, this process should include a visual examination of the Establish Verification Procedures. sensor and any attached wires for damage or kinks. The device should be checked to ensure • Before a temperature-indicating device (e.g., that it is operational; a thermometer) or temperature- recording device (e.g., a time and temperature data AND logger) is put into service, check the • Calibrate the temperature-indicating device accuracy of the device to verify that the or temperature-recording device against a factory calibration has not been affected. known accurate reference device (e.g., a This check can be accomplished by: NIST-traceable thermometer) at least once a ° Immersing the sensor in an ice slurry year or more frequently if recommended by (32°F (0°C)) if the device will be used at the device manufacturer. Optimal calibration or near refrigeration temperature; frequency is dependent upon the type, condition, past performance, and conditions OR of use of the device. Consistent temperature ° Immersing the sensor in boiling water variations away from the actual value (drift) (212°F (100°C)) if the device will be used found during checks and/or calibration may at or near the boiling point. Note that show a need for more frequent calibration or the temperature should be adjusted to the need to replace the device (perhaps with compensate for altitude, when necessary; a more durable device). Devices subjected to OR high temperatures for extended periods of time may require more frequent calibration. Doing a combination of the above if ° Calibration should be performed at a the device will be used at or near room minimum of two temperatures that bracket temperature; the temperature range at which it is used; OR AND Comparing the temperature reading on ° • Review monitoring, corrective action, the device with the reading on a known and verification records within 1 week of accurate reference device (e.g., a NIST- preparation to ensure they are complete and traceable thermometer) under conditions any critical limit deviations that occurred that are similar to how it will be used were appropriately addressed.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 232 CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse Abuse Temperature and Time of aResult as botulinum) Clostridium Than (Other Toxin and Formation Growth 12:CHAPTER Bacteria Pathogenic TABLE 12-4

CONTROL STRATEGY EXAMPLE 3 - COOLING AFTER COOKING CONTROL

This table is an example of a portion of a HACCP plan using “Control Strategy Example 3 - Cooling After Cooking Control.” This example illustrates how a dungeness crabmeat processor can control pathogenic bacteria growth and toxin formation as a result of time and temperature abuse during cooling after cooking. In this case, the product is fully cooled, i.e., to 40°F (4.4°C), after cooking before significant handling. It is provided for illustrative purposes only. It may be necessary to select more than one control strategy in order to fully control the hazard, depending upon the nature of your operation.

Example Only See Text for Full Recommendations

(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)

CRITICAL LIMITS MONITORING CRITICAL SIGNIFICANT FOR EACH CORRECTIVE CONTROL RECORDS VERIFICATION HAZARD(S) PREVENTIVE ACTION(S) POINT WHAT HOW FREQUENCY WHO MEASURE

Cooked crab Pathogenic Crabs cooled Length of Clock Start marked Production Destroy product Production Check the dial cooler bacteria growth from 135°F to cooling cycle batch supervisor record thermometer 233 and toxin 70°F in 2 hours Make for accuracy formation and 70°F to Approximately adjustment and damage 40°F in 4 more every 2 hours or repairs to and to ensure hours during cooking cooler that it is operational before putting Cooked Dial into operation; crab internal thermometer in check it temperature marked batches daily, at the of cooked crabs beginning of operations; and calibrate it once per year

Review monitoring, corrective action, and verification records within 1 week of preparation

Note: Control during unrefrigerated processing is covered under “Control Strategy Example 4 - Unrefrigerated Processing Control.” Note: Control is necessary at this step because the processor has not established that the cook step is adequate to kill the spores of C. perfringens or B. cereus • CONTROL STRATEGY EXAMPLE 4 - OR UNREFRIGERATED PROCESSING CONTROL • CRITICAL LIMIT 3: It may be necessary to select more than one ° The product is held at internal control strategy in order to fully control the temperatures below 50°F (10°C) hazard, depending upon the nature of your throughout processing, operation. OR Set Critical Limits. ° Alternatively, the product is held at The following recommended critical limits are ambient air temperatures below 50°F intended to keep the pathogenic bacteria of (10°C) throughout processing. greatest concern in fish and fishery products For cooked, ready-to-eat products: from reaching the rapid growth phase (i.e., Note: The critical limits for cooked, ready-to-eat products are keep them in the lag phase) as a result of time intended to begin at the completion of cooling or at the time that the and temperature exposure during processing. product is first significantly handled after cooking, whichever occurs You may also wish to reference Table A-2 first. (Appendix 4), which provides cumulative time • CRITICAL LIMIT 1: and temperature combinations for the pathogenic ° If at any time the product is held at bacteria individually. internal temperatures above 80°F For raw, ready-to-eat products: (26.7°C), exposure time (i.e., time at internal temperatures above 50°F (10°C) • CRITICAL LIMIT 1: but below 135ºF (57.2ºC)) should be ° If at any time the product is held at limited to 1 hour (3 hours if S. aureus is internal temperatures above 70°F the only pathogen of concern), (21.1°C), exposure time (i.e., time at internal temperatures above 50°F (10°C) OR but below 135ºF (57.2ºC)) should be ° Alternatively, if at any time the product limited to 2 hours (3 hours if S. aureus is is held at internal temperatures above the only pathogen of concern), 80°F (26.7°C), exposure time (i.e., time at internal temperatures above 50°F (10°C) OR but below 135ºF (57.2ºC)) should be ° Alternatively, exposure time (i.e., time at limited to 4 hours, as long as no more internal temperatures above 50°F (10°C) than 1 of those hours is above 70°F but below 135ºF (57.2ºC)) should be (21.1°C); limited to 4 hours, as long as no more than 2 of those hours are between 70°F OR (21.1°C) and 135ºF (57.2ºC); • CRITICAL LIMIT 2: OR ° If at any time the product is held at internal temperatures above 70°F • CRITICAL LIMIT 2: (21.1°C) but never above 80°F (26.7°C), ° If at any time the product is held at exposure time at internal temperatures internal temperatures above 50°F (10°C) above 50°F (10°C) should be limited to but never above 70°F (21.1°C), exposure 2 hours (3 hours if S. aureus is the only time at internal temperatures above 50°F pathogen of concern), (10°C) should be limited to 5 hours (12 hours if S. aureus is the only pathogen of concern);

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 234 OR Example: ° Alternatively, if the product is never A crabmeat processor using a retort process held at internal temperatures above identifies a series of post-cook processing 80°F (26.7°C), exposure times at internal steps (e.g., backing, picking, and packing) temperatures above 50°F (10°C) should as CCPs for pathogenic bacteria growth be limited to 4 hours, as long as no more and toxin formation. Initial cooling takes than 2 of those hours are above 70°F place in the cooking crates and then the (21.1°C); product is first handled at temperatures of around 120°F (48.9°C). The processor sets a OR critical limit of maximum cumulative time • CRITICAL LIMIT 3: of exposure of 4 hours at product internal ° If at any time the product is held at temperatures above 50°F (10°C), no more internal temperatures above 50°F (10°C) than 1 of which is above 70°F (21.1°). This but never above 70°F (21.1°C), exposure critical limit is selected because the crabs time at internal temperatures above 50°F are handled while still warm (e.g., above (10°C) should be limited to 5 hours (12 80°F (26.7°C)). Cooling that takes place hours if S. aureus is the only pathogen of after the product is handled is included in concern); the limit. OR Example: Another crabmeat processor using a retort • CRITICAL LIMIT 4: process also identifies a series of post-cook ° The product is held at internal processing steps (e.g., backing, picking, temperatures below 50°F (10°C) and packing) as CCPs. However, this throughout processing, product is cooled fully before handling, OR and ice is used on the product during processing to control time and temperature Alternatively, the product is held at ° abuse. The processor sets a critical limit of ambient air temperatures below 50°F a maximum product internal temperature (10°C) throughout processing. of 50°F (10°C) at all times. Specifying a Note: The preceding recommended critical limits do not address time of exposure is not necessary in this internal product temperatures between 40°F (4.4°C), the case, because it is not reasonably likely recommended maximum storage temperature for refrigerated fish and fishery products, and 50°F (10°C). The recommended that the product would be held long critical limits do not address such temperatures because growth of enough that significant pathogen growth foodborne pathogenic bacteria is very slow at these temperatures could occur at this temperature (e.g., 2 to and the time necessary for significant growth is longer than would be reasonably likely to occur in most fish and fishery product processing 21 days, depending upon the pathogen). steps. However, if you have processing steps that occur at these temperatures that approach the maximum cumulative exposure times listed in Table A-2 (Appendix 4) for the pathogenic bacteria of concern in your product, you should consider development of a critical limit for control at these temperatures. The cumulative time and temperature critical limits above (other than the last critical limit for raw, ready-to-eat and cooked, ready-to-eat fish and fishery products) are depicted in table format below:

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 235 TABLE 12-5

CUMULATIVE TIME AND TEMPERATURE CRITICAL LIMITS

THEN THE CUMULATIVE EXPOSURE TIME AT INTERNAL WHEN THE PRODUCT INTERNAL TEMPERATURES ABOVE 50°F (10°C) IN HOURS IS1… TEMPERATURE RANGE IN ºF (ºC) IS… 1 2 3 5 12

RAW, READY TO EAT >503 X X2 (>10) Alternatively, >50 to ≤ 70 X (>10 to ≤ 21.1)

Plus X >70 (>21.1)

Alternatively, X >50 to ≤ 70 (>10 to ≤ 21.1) Plus X >70 (>21.1) >50 to ≤ 70 X X2 (>10 to ≤21.1)

COOKED, READY TO EAT >504 X X2 (>10) Alternatively, X >50 to ≤ 70 (>10 to ≤ 21.1) Plus X >704 (>21.1) >50 to ≤ 80 X X2 (>10 to ≤ 26.7) Alternatively, X >50 to ≤ 70 (>10 to ≤ 21.1) Plus X >70 to <80 (>21.1 to <26.7) Alternatively, X >50 to ≤ 70 (>10 to ≤ 21.1) Plus X >70 to <80 (>21.1 to <26.7) >50 to ≤ 70 X X2 (>10 to ≤ 21.1)

1. Time at temperatures of 135ºF (57.2ºC) and above is not counted. 2. Where S. aureus is the only pathogen of public health significance. 3. Temperature may exceed 70ºF (21.1ºC). 4. Temperature may exceed 80ºF (26.7ºC).

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 236 Establish Monitoring Procedures. • Make visual observations of length of exposure to unrefrigerated conditions (i.e., » What Will Be Monitored? >40ºF (4.4ºC)) using a clock. • The length of time of product exposure to Example: unrefrigerated conditions (i.e., above 40°F A crabmeat processor identifies a (4.4°C)); series of processing steps (e.g., backing, ° The product internal temperature during picking, and packing) as CCPs for the exposure period; pathogenic bacteria growth. The processor OR establishes a critical limit of no more than 1 cumulative hour of exposure to The ambient temperature of the ° unrefrigerated temperature during these processing area; processing steps (Critical Limit 1). The OR processor uses marked product containers • The length of time only of product exposure to monitor the progress of the product to unrefrigerated conditions (i.e., >40°F through the three processing steps. The (4.4°C)), for critical limit 1 (raw, ready-to-eat time that the marked container is removed and cooked, ready-to-eat); from and returned to refrigeration is monitored using a clock. OR • The internal temperature only of the Example: product, when internal temperatures are held Another crabmeat processor with identical below 50°F (10°C) or above 135°F (57.2°C) CCPs establishes a more complex set of throughout processing for critical limit 3 critical limits: no more than 4 cumulative for raw, ready-to-eat or critical limit 4 for hours with product internal temperatures cooked, ready-to-eat; above 50°F (10°C), with no more than 1 of those hours above 70°F (21.1°C) OR (Critical Limit 1 Alternative). This • The ambient air temperature only, when processor also uses marked containers ambient air temperature is held below 50°F to monitor the progress of the product (10°C) throughout processing for critical limit through the process. However, in addition 3 for raw, ready-to-eat or critical limit 4 for to monitoring time using a clock, the cooked, ready-to-eat. processor also monitors product internal temperature for the marked containers How Will Monitoring Be Done? » using a thermometer. This monitoring • For product internal temperature or ambient technique provides the processor more air temperature: flexibility in processing but requires more ° Use a temperature-indicating device (e.g., monitoring effort. a thermometer); Example: OR A lobster meat processor identifies the • For ambient air temperature: meat removal process as a CCP for pathogenic bacteria growth. The operation Use a continuous temperature-recording ° is performed under near-refrigeration device (e.g., a recording thermometer); conditions (<50°F (10°C)) (Critical Limit AND/OR 4 Alternative). The processor monitors ambient air temperature with a digital data logger.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 237 » How Often Will Monitoring Be Done (Frequency)? • Divert the product to a use in which the • For continuous temperature-recording critical limit is not applicable (e.g., divert devices: crabmeat to a stuffed flounder operation), after giving consideration to the fact that Continuous monitoring during processing ° any S. aureus or B. cereus toxin that may be is accomplished by the device itself, with present may not be inactivated by heat; a visual check of the recorded data at least once per day; OR OR • Destroy the product; • For temperature-indicating devices and OR clocks: • Divert the product to a non-food use. ° At least every 2 hours; AND OR Take the following corrective actions to regain control ° Every batch. over the operation after a critical limit deviation: » Who Will Do the Monitoring? • Add ice to the product; • For continuous temperature recording OR devices: • Return the affected product to the cooler; ° Monitoring is performed by the device AND itself. The visual check of the data • Modify the process as needed to reduce the generated by the device, to ensure that time and temperature exposure. the critical limits have consistently been met, may be performed by any person who has an understanding of the nature Establish a Recordkeeping System. of the controls; • Processing records showing the results of time and/or temperature exposure measurements. OR • For temperature-indicating devices and Establish Verification Procedures. clocks: • Before a temperature-indicating device (e.g., ° Any person who has an understanding of a thermometer) or temperature-recording the nature of the controls. device (e.g., a recording thermometer) is put into service, check the accuracy of the Establish Corrective Action Procedures. device to verify that the factory calibration Take the following corrective action to a product has not been affected. This check can be involved in a critical limit deviation: accomplished by: • Chill and hold the affected product until an ° Immersing the sensor in an ice slurry evaluation of the total time and temperature (32°F (0°C)) if the device will be used at exposure is performed; or near refrigeration temperature; OR OR • Cook the product, after giving consideration ° Immersing the sensor in boiling water to the fact that any S. aureus or B. cereus (212°F (100°C)) if the device will be used toxin that may be present may not be at or near the boiling point. Note that inactivated by heat; the temperature should be adjusted to compensate for altitude, when necessary; OR

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 238 OR or the need to replace the device (perhaps ° Doing a combination of the above if with a more durable device). Calibration the device will be used at or near room should be performed at a minimum of two temperature; temperatures that bracket the temperature range at which it is used; OR AND ° Comparing the temperature reading on the device with the reading on a known • Where appropriate to the critical limit, by accurate reference device (e.g., a NIST- using a study that establishes the relationship traceable thermometer) under conditions between exposure time and product that are similar to how it will be used temperature; (e.g., air temperature and product internal AND temperature) within the temperature • Review monitoring, corrective action, range at which it will be used; and verification records within 1 week of AND preparation to ensure they are complete and • Once in service, check the temperature- any critical limit deviations that occurred indicating device or temperature-recording were appropriately addressed. device daily before the beginning of operations. Less frequent accuracy checks may be appropriate if they are recommended by the instrument manufacturer and the history of use of the instrument in your facility has shown that the instrument consistently remains accurate for a longer period of time. In addition to checking that the device is accurate by one of the methods described above, this process should include a visual examination of the sensor and any attached wires for damage or kinks. The device should be checked to ensure that it is operational and, where applicable, has sufficient ink and paper; AND • Calibrate the temperature-indicating device or temperature-recording device against a known accurate reference device (e.g., a NIST-traceable thermometer) at least once a year or more frequently if recommended by the device manufacturer. Optimal calibration frequency is dependent upon the type, condition, past performance, and conditions of use of the device. Consistent temperature variations away from the actual value (drift) found during checks and/or calibration may show a need for more frequent calibration

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 239 CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse Abuse Temperature and Time of aResult as botulinum) Clostridium Than (Other Toxin and Formation Growth 12:CHAPTER Bacteria Pathogenic TABLE 12-6

CONTROL STRATEGY EXAMPLE 4 - UNREFRIGERATED PROCESSING CONTROL

This table is an example of a portion of a HACCP plan using “Control Strategy Example 4 - Unrefrigerated Processing Control.” This example illustrates how a blue crabmeat processor that handles the crabs at the beginning of backing while still hot can control pathogenic bacteria growth and toxin formation as a result of time and temperature abuse during unrefrigerated processing. It is provided for illustrative purposes only. It may be necessary to select more than one control strategy in order to fully control the hazard, depending upon the nature of your operation.

Example Only See Text for Full Recommendations

(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)

CRITICAL LIMITS MONITORING CRITICAL SIGNIFICANT FOR EACH CORRECTIVE CONTROL RECORDS VERIFICATION HAZARD(S) PREVENTIVE ACTION(S) POINT WHAT HOW FREQUENCY WHO MEASURE Backing, Pathogenic Exposure time The length of Visual Start marked Production Immediately Production Check the dial in-process bacteria growth (i.e., time time of product observation container supervisor ice product or record thermometer for 240 cooler, picking, and toxin at internal exposure to of marked approximately move to cooler accuracy and and packing formation temperatures unrefrigerated containers every 2 hours damage and to above 50°F conditions (i.e., using a clock during backing, Hold and ensure that it but below above 40°F) in-process evaluate is operational 135ºF) during cooler, picking, based on before putting backing, in- and packing total time and into operation; The product Dial process cooler, temperature check it daily, at internal thermometer picking, and exposure the beginning of temperature packing should operations; and during the be limited to 4 calibrate it once exposure hours, as long per year period as no more than 1 of those Review hours is above monitoring, 70°F verification, and corrective action records within 1 week of preparation

Note: Control during refrigerated storage is covered under “Control Strategy Example 2 - Refrigerated Storage and Refrigerated Processing Control. Note: This critical limit is necessary because the crabs are handled at internal temperatures above 80°F during backing BIBLIOGRAPHY. • Gecan, J. S., R. Bandler, and W. F. Staruskiewcz. 1994. Fresh and frozen We have placed the following references on shrimp: a profile of filth, microbiological display in the Division of Dockets Management, contamination, and decomposition. J. Food Food and Drug Administration, 5630 Fishers Lane, Prot. 57:154158. rm. 1061, Rockville, MD 20852. You may see • Hood, M. A., G. E. Ness, G. E. Rodrick, and them at that location between 9 a.m. and 4 p.m., N. J. Blake. April 1983. Effects of storage Monday through Friday. As of March 29, 2011, on microbial loads of two commercially FDA had verified the Web site address for the important shellfish species, Crassostrea references it makes available as hyperlinks from virginica and Mercenaria campechiensis. the Internet copy of this guidance, but FDA is not Appl. Environ. Microbiol. 45:1221−1228. responsible for any subsequent changes to Non- • Huss, H. H., 1993. Assurance of seafood FDA Web site references after March 29, 2011. quality. FAO fisheries technical paper, no. • Ahmed, F. E. (ed.). 1991. Seafood safety. 334. FAO, Rome, Italy. 169p. National Academy Press, Washington, DC. • Huss, H. H. (ed.). 1993. Quality and quality • Baek, S-Y., S-Y. Lim, D-H. Lee, K-H. Min, changes in fresh fish. FAO fisheries technical and C-M. Kim. 2000. Incidence and paper, no. 346. FAO, Rome, Italy. characterization of Listeria monocytogenes • Huss, H. H. 1997. Control of indigenous from domestic and imported foods in Korea. pathogenic bacteria in seafood. Food J. Food Prot. 63:186−189. Control. 8:91−98. • Buchanan, R. L., and L. A. Klawitter. 1992. • Jemmi, T., and A. Keusch. 1992. Behavior of Effectiveness of Carnobacterium piscicola Listeria monocytogenes during processing LK5 for controlling the growth of Listeria and storage of experimentally contaminated monocytogenes Scott A in refrigerated foods. hot-smoked trout. Int. J. Food Microbiol. J. Food Safety 12:219−236. 15:339−346. • Duffes, F., C. Corre, F. Leroi, X. Dousset, • Huss, H. H., A. Reilly, and P. K. Ben and P. Boyaval. 1999. Inhibition of Listeria Embarek. 2000. Prevention and control monocytogenes by in situ produced and of hazards in seafood. Food Control. semipurified bacteriocins onCarnobacterium 11:149−156. spp. on vacuum-packed, refrigerated cold- • Jørgensen, L. V., and H. H. Huss. 1998. smoked salmon. J. Food Prot. 62:1394−1403. Prevalence and growth of Listeria • Farber, J. M. 1991. Listeria monocytogenes in fish monocytogenes in naturally contaminated products. J. Food Prot. 54(12):922−924, 934. seafood. Int. J. Food Microbiol. 42:127−131. • Food and Agriculture Organization and • Leung, C. K., Y. W. Huang, and M. World Health Organization. 2005. Risk A. Harrison. 1992. Fate of Listeria assessment of Vibrio cholerae 01 and 0139 monocytogenes and Aeromonas hydrophila in warm-water shrimp in international trade. on packaged channel catfish fillets stored at Microbiological risk assessment series no. 9. 4 C. J. Food Prot. 55:728−730. FAO, Rome, Italy. • Morris, G. J., and R. E. Black. 1985. Cholera • Food and Agriculture Organization and and other vibrioses in the United States. New World Health Organization. 2005. Risk Engl. J. Med. 12:343−350. assessment of Vibrio vulnificus in raw • Nielsen, H.-J. S., and P. Zeuthen. 1984. oysters: interpretative summary and technical Growth of pathogenic bacteria in sliced report. Microbiological risk assessment series vacuum-packed bologna-type sausage no. 8. FAO, Rome, Italy, FAO.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 241 as influenced by temperature and gas • Rosso, L., S. Bajard, J. P. Flandrois, C. permeability of packaging film. Food Microb. Lahellec, J. Fournaud, and P. Veit. 1996. 1:229−243. Differential growth of Listeria monocytogenes • Palumbo, S. A. 1986. Is refrigeration enough at 4 and 8°C: consequences for the shelf life to restrain foodbourne pathogens? J. Food of chilled products. 59:944−949. Prot. 49: 1003−1009. • Satoshi, I., A. Nakama, Y. Arai, Y. Kokubo, T. • Peixotto, S. S., G. Finne, M. O. Hanna, and Maruyama, A. Saito, T. Yoshida, M. Terao, S. C. Vanderzant. 1979. Presence, growth and Yamamoto, and S. Kumagai. 2000. Prevalence survival of Yersinia entercolitica in oysters, and contamination levels of Listeria shrimp and crab. J. Food Prot. 42:974−981. monoocytogenes in retail foods in Japan. Int. J. Food Microb. 59:73−77. • Peterson, M. E., G. A. Pelroy, R. N. Paranjpye, F. T. Poysky, J. S. Almond, and M. W. Eklund. • Son, N. T., and G. H. Fleet. December 1980. 1993. Parameters for control of Listeria Behavior of pathogenic bacteria in the oyster, monocytogenes in smoked fishery products: Crassostrea commercialis, during depuration, sodium chloride and packaging method. J relaying and storage. Appl. Environ. Food Prot. 56:938−943. Microbiol. 40(6):994−1002. • Philips, F. A., and T. Peeler. December 1972. • U.S. Food and Drug Administration. Bacteriological survey of the blue crab Foodborne pathogenic microorganisms industry. Appl. Microbiol. 24(6):958−966. and natural toxins handbook. In The bad bug book. http://www.fda.gov/ • Rahmati, T., and R. Labbe. 2007. Incidence Food/FoodSafety/FoodborneIllness/ and enterotoxigenicity of Clostridium rneIllnessFoodbornePathogensNaturalToxins/ perfringens and Bacillus cereus from retail BadBugBook/default.htm. seafood. IAFP Annual Meeting. P128. • U.S. Food and Drug Administration. 2009. • Refrigerated Foods and Microbiological Food code. Department of Health and Criteria Committee of the National Food Human Services, Public Health Service, FDA, Processors Association. 1988. Factors Center for Food Safety and Applied Nutrition, to be considered in establishing good College Park, MD. http://www.fda.gov/Food/ manufacturing practices for the production FoodSafety/RetailFoodProtection/FoodCode/ of refrigerated foods. Dairy and Food Sanit. FoodCode2009/default.htm. 8:288−291. • U.S. Food and Drug Administration. • Rivituso, C. P. and Snyder, O. P. 1981. 2005. Quantitative risk assessment on the Bacterial growth at foodservice operating public health impact of pathogenic Vibrio temperatures. J. Food Prot. 44:770−775. parahaemolyticus in raw oysters. Department • Rodríguez, Ó., V. Losada, S. P. Aubourg, of Health and Human Services, Public and J. Barros-Velázquez. 2004. Enhanced Health Service, FDA, Center for Food Safety shelf-life of chilled European hake and Applied Nutrition, College Park, MD. (Merluccius merluccius) stored in slurry http://www.fda.gov/Food/ScienceResearch/ ice as determined by sensory analysis and ResearchAreas/RiskAssessmentSafetyAssessment/ assessment of microbiological activity. Food ucm050421.htm Res. Int’l. 37(8):749−757. • U.S. Food and Drug Administration and U.S. • Rosso, L., J. R. Lobry, J. P. Flandrois. 1993 Department of Agriculture. 2003. Quantitative An unexpected correlation between cardinal assessment of the relative risk to public health temperature of microbial growth highlighted from foodborne Listeria monocytogenes among by a new mode. J. Theor. Biol. 162:447−463. selected categories of ready-to-eat foods.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 242 http://www.fda.gov/Food/ScienceResearch/ ResearchAreas/RiskAssessmentSafetyAssessment/ ucm183966.htm. • Wallace, B. J., J. J. Guzewich, M. Cambridge, and S. Altekruse. 1999. Seafood-associated disease outbreaks in New York, 1980-1994. Amer. J. Prev. Med. 17:48−54. • Ward, D. R, and C. R. Hackney (ed.). 1991. Microbiology of marine food products. Van Nostrand Reinhold, New York, NY. • Wentz, B. A., A. P. Duran, A. Swartzentruber, A. H. Schwab, F. D. McClure, D. Archer, and R. B. Read, Jr. 1985. Microbiological quality of crabmeat during processing. J. Food Prot. 48:44−49. • Wong, H.-C., M.-C. Chen, S.-H. Liu, and D. P. Lin. 1999. Incidence of highly genetically diversified Vibrio parahaemolyticus in seafood imported from Asian countries. Int. J. Food Microbiol. 52:181−188.

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 243 NOTES:

CHAPTER 12: Pathogenic Bacteria Growth and Toxin Formation (Other Than Clostridium botulinum) as a Result of Time and Temperature Abuse 244