Proliferation Contributing Factors

Background

Technical definitions for the 30 contributing factors for foodborne illness outbreaks are organized around the three types of contributing factors (contamination, proliferation, and survival). Staff from CDC, the Food and Drug Administration (FDA), and state health departments helped revise these contributing factors to show how foodborne illness outbreaks evolve.

Definitions

Proliferation contributing factors allow proliferation of etiologic agents. These factors relate to how the pathogen was able to increase in numbers and/or produce toxic products before the food was ingested. These factors are only for bacterial and fungal outbreaks.

P1 Allowing foods to remain out of temperature control for a prolonged period during food preparation

During food preparation, food was kept out of temperature control for a prolonged period that allowed pathogenic bacteria and/or fungi to multiply to an amount sufficient to cause illness or to produce toxins if toxigenic. Examples of this type of contributing factor include:

• Improper thawing (such as allowing frozen food to thaw at room temperature or leaving frozen foods in standing water for prolonged periods) allowed pathogens to multiply.
• Prolonged preparation time (such as prolonging preparation time by preparing too many foods at the same time) allowed pathogens to multiply.

P2 Allowing foods to remain out of temperature control for a prolonged period during food service or display

During food service or display, food was kept out of temperature control for a prolonged period that allowed pathogenic bacteria and/or fungi to multiply to an amount sufficient to cause illness or to produce toxins if toxigenic. Examples of this type of contributing factor include:

• Foods left out at ambient temperature for a prolonged time at a church supper.
• No time or temperature control measures on a buffet line.

P3 Inadequate cold holding temperature due to malfunctioning refrigeration equipment

Malfunctioning refrigeration equipment caused foods to be held at an inadequate cold holding temperature. Examples of this type of contributing factor include:

• Walk-in cooler malfunctioned causing inadequate cold holding temperature of food.
• A broken or torn door gasket caused air leakage in a reach-in refrigerator resulting in inadequate cold holding temperature of food.

P4 Inadequate cold holding temperature due to an improper practice

Inadequate cold holding temperature occurred due to an improper practice. Examples of this type of contributing factor include:

• Overloaded refrigerator resulting in poor air circulation.
• Inadequately iced salad bar.
• Time/Temperature Control for Safety (TCS) foods, such as tuna or egg salad, were stacked above the fill line of the cold holding wells in a deli cold holding unit.

P5 Inadequate hot holding temperature due to malfunctioning equipment

Malfunctioning hot-holding equipment caused foods to be held at an inadequate hot holding temperature. Examples of this type of contributing factor include:

• A steam table or crockpot broke and caused food to be held at inadequate hot holding temperatures.

P6 Inadequate hot holding temperature due to an improper practice

Inadequate hot holding temperature occurred due to an improper practice. Examples of this type of contributing factor include:

• A steam table or crockpot was not turned on or properly maintained and caused food to be held at inadequate hot holding temperatures.
• A crockpot being used to heat or reheat food was overloaded and caused food to be held at inadequate hot holding temperatures.

P7 Improper cooling of food

Foods were refrigerated in large quantities or stored in devices where the temperature was poorly controlled and allowed pathogens to multiply. Examples of this type of contributing factor include:

• Foods were refrigerated in large masses or as large volumes of foods in containers, which did not allow proper cooling.
• Foods were stored in containers with tight-fitting lids, pans were stacked on top of others, or crowded storage in a refrigerator, all of which led to inadequate air circulation during cooling process.

P8 Extended refrigeration of food for an unsafe amount of time, relative to the food product and pathogen

This situation is a concern for psychrotrophic pathogenic bacteria (e.g., Listeria monocytogenes, Clostridium botulinum type E, Yersinia enterocolitica, Aeromonas hydrophila) that can multiply over sufficient time at ordinary refrigerator temperatures and grow to an amount sufficient to cause illness or produce toxins if toxigenic (e.g., C. botulinum). Examples of this type of contributing factor include:

• Listeria growth after deli meat refrigeration for more than 7 days
• Kept containers of commercially prepared foods for several weeks after they were opened

P9 Inadequate reduced oxygen packaging (ROP) of food

Food was sealed using inadequate Reduced Oxygen Packaging (ROP) methods, which provided conditions conducive to growth of anaerobic or facultative bacteria in foods. ROP includes processing and packaging techniques that prevent the entry of oxygen into the container, such as vacuum packaging, modified or controlled atmosphere packaging, cook chill packaging, sous vide packaging, hermetically sealed containers (double seams/glass jar with lid), deep containers from which air is expressed, and products packed in oil. Examples of this type of contributing factor include:

• Inadequate process applied to vacuum-packed fish
• Insufficient process applied to salad in gas-flushed bag
• Ineffective hermetically seal on can
• Garlic packaged in oil with unsatisfactory process
• Lack of controlled atmosphere packaging of beef jerky

P10 Inadequate non-temperature dependent processes (e.g., acidification, water activity, fermentation) applied to a food to prevent pathogens from multiplying

Non-temperature-dependent processes (e.g., acidification, water activity, fermentation) failed and allowed pathogens to multiply to an amount sufficient to cause illness. This situation is a concern for growth of preformed heat-stable toxins or bacterial spores (e.g., Clostridium perfringens, Clostridium botulinum, Bacillus cereus, Staphylococcus aureus). Examples of this type of contributing factor include:

• Insufficient acidification (low concentration of acidic ingredients) in home canned foods
• Insufficiently low water activity (low concentration of salt) in smoked/salted fish
• Inadequate fermentation (starter culture failure or improper fermentation conditions) in processed meat or processed cheese

P11 Other situations that promoted or allowed microbial growth of toxic production (specify)

A factor that promoted growth, proliferation, amplification, or concentration of bacterial agents but that did not fit into any of the other defined categories; the factor should be specified in the 'Contributing Factors Comments' section.