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Reaction: The Science Behind Salad Safety

Here, Trevor Suslow, Ph.D., shares his reaction to the recent Consumer Reports article
Packaged Salad Can Contain High Levels of Bacteria.  Suslow is a cooperative extension research specialist in postharvest quality and safety in the Department of Plant Sciences at the University of California at Davis.

Yes, once again this type of bacterial testing activity has caused a flurry of concern and confusion. I support the notion that there is always room for improvement in food safety management and that FDA should increase the specificity of their guidance and regulations, where warranted and defensible, to include science-based standards and microbiological limits for fresh produce.

However, I feel it is grossly unfair to consumers to raise a specter of fear well beyond what is supported by available science and our everyday shared experiences. What I rely on for my personal confidence in regularly consuming lettuces, spring mix, and spinach salads is that there are billions and billions of servings of these items consumed every year in the U.S. alone and the predominant experience we have is of safe consumption.

No one wishes to dismiss the fact that such consumption likely results in sporadic cases of illness that aren’t known by the public health system and have caused multiple outbreaks and tragic consequences for individuals and families. Continued efforts by the industry, FDA, and consumer advocacy groups to elevate performance standards for prevention and process management along the whole food chain at a national level are certainly warranted.

Uniform and accepted microbiological standards, as stated in the Consumer Reports report (See Study Finds Bacteria in Packaged Greens, Feb. 3), are not available at this time. I believe the criteria that were chosen do not provide sufficient information, by themselves, to judge the sanitation performance or risk to consumers.

First let’s take care of one issue, from my perspective; a normal head of lettuce is colonized–not contaminated–with a diversity of microbiota, including diverse types of bacteria. Only a small fraction of the total normal bacteria on lettuce can be grown or cultured in the lab. The total numbers of bacteria on a leaf far exceed the number of a single group like the total coliforms that were a prime target in the survey. A smaller subset of total coliform bacteria are the fecal coliforms. We eat lots and lots of microbes all the time.

Second, total coliforms and fecal coliforms are defined by a set of culture-dependent lab criteria. This long-standing and convenient trait-based classification includes non-harmful E. coli and other related bacteria associated with fecal origin.

An estimate of the number of total coliforms generated by the lab tests also includes many other related bacteria that are part of the normal and expected group of plant colonizers. We are all exposed to plant-associated bacteria and consume them on a regular basis, often in large numbers like those reported in the survey.

Some that are not necessarily of fecal origin are recognized to be opportunistic pathogens, as a group, but the role of environmental isolates in causing human illness, as compared to the same taxonomic species from a hospital environment, is much less certain. Even here, illness with this group is more associated with problems that arise from inhalation or injection with non-sterile medical devices and equipment and other predisposing health factors.

However, I am certainly not a medical or public health expert and I am simplifying this quite a bit just to ensure that you are aware that a total coliform or fecal coliform doesn’t necessarily indicate fecal contamination in the plant world. Their numbers on a leaf or fruit do not relate well to risk of illness or true and serious pathogens being present. When one follows standard protocols, developed for dairy, meat, drinking water, and wastewater reclamation, for example, for enumerating total coliform populations from plants, one often gets high numbers of these plant colonizers. They are very tough to wash off and are not killed 100 percent even with the most elegant and sophisticated wash disinfection system.

It is certainly conceivable and has happened that contamination we should be concerned about would be present among these coliform bacteria, but it isn’t automatic. The normal level of “fecal coliforms” (I prefer and always use the alternate classification Thermotolerant Coliforms; grows at 42 to 44 degrees Celsius or 107 to 111 degrees Fahrenheit) is generally a subset of this and often varies more widely from head to head and leaf to leaf; here again this is not a strong predictor of pathogen presence or risk of illness to consumers.

The suitability of enterococci as strong indicators of recent fecal contamination or pathogen presence is not well established for plant products. This group has also been shown to have an environmental phase (growth in soil and sediments) which complicates the interpretation of their presence. While enterococci are generally considered better indicators of fecal contamination, their presence is simply not a perfect associative indicator for direct environmental contact with fecal matter or gross sanitation failures.

That the survey results found higher numbers of total coliform near the end of Use By Date is not at all surprising as there will always be some at the end of the most vigorous wash and sanitizer treatment. These survivors can grow (slowly) at typical refrigeration temperatures and certainly could multiply more quickly if exposed to warmer temperatures.

Growth would be expected especially if exposed to fluctuating temperatures that go from coldest to warmer to cold. Higher numbers are also consistent with the stage of decline of freshness and natural plant senescence, the inevitable process of quality loss that goes hand in hand with an increase in spoilage organisms.

The Consumer Reports study results may be consistent with widely held concerns for better cold-chain control, especially with packaged salads and other pre-cut or ready-to-eat fruits and vegetables, all the way to the home consumer. Have we seen high counts seasonally or wash procedures that aren’t optimal? Sure, but there is another possible explanation.  Because all the samples were taken from retail stores, the numbers of bacteria (not that fact that they were present) may tell us more about the temperature history of the product than provide clear evidence of poor sanitation.

Purchasing packaged salads or whole heads is a matter of personal choice. We do both in my family. I always wash loose leaf lettuces to remove any adhering soil. I never wash packaged salads. I do not support or believe that re-washing packaged salads should be a recommendation for the home consumer. A large and diverse panel of experts published a comprehensive article in 2007* detailing the scientific evidence for the lack of benefit and the greater risk of cross-contamination in the home.

If one chooses to take advantage of the convenience and diversity of greens available in sensible serving portions or as complete salad meals, it is always best to look at the Best if Consumed By dating and take notice of the display case arrangement. Bags should be vertical in a row, not laid one on top of the other in stacks. Clamshell containers are displayed in various stacking or slanted row patterns which allow generous space for airflow.

I always make it a habit to check the display temperature by hand. This isn’t perfect or necessarily an indication of safe or unsafe product but it is at least easy to tell if the air is really cool and the bags are very cool to the touch. Maybe our cell phones and smart-phones sho
uld come with an infrared di
gital thermometer function.

Comments regarding cold-chain management, product temperature at point of purchase (POP), and the role of the home consumer in handling of packaged salads have prompted additional requests for information. Two main questions regarding consumer recommendations emerged:

1.    Is post-purchase temperature equally relevant for quality and safety?
2.    Can consumers really judge if product has been temperature-compromised at POP?

Simple answers to the theme of Question #1 are not possible because exceptions to lower risk or higher risk can always be made and are equally valid. The most responsible answer is “It depends.” However, this is unsatisfactory, especially when trying to provide information consumers can use as an everyday rule of thumb.  So I will make a brief general attempt and hope any backlash is not too intense. To limit the scope of the response, I will stick with packaged salads for the most part.

Is post-purchase temperature equally relevant for quality and safety?

Temperature management and cumulative cold-chain history is predominantly a quality issue and determines a product’s visual, sensory, and nutritive keeping-potential. The FDA Food Code (2009) has identified Time/Temperature Control for Safety (TCS) limits, at or below 41F (5C), for certain value-added produce that must be applied to distribution, storage, and display. This includes cut leafy greens as well as fresh cut cantaloupe, pre-sliced or diced tomatoes.

These are designated as TCS foods due to recurring outbreaks AND the known growth potential of bacterial pathogens on the product.   The recognized low infectious dose of many pathogens may be sufficient to cause illness in highly susceptible individuals and growth on the product is not necessary to cause great harm. However, not all possible pathogens and variants of these pathogens, that may infrequently find their way onto or into product, are equally infectious to all individuals.

Proper post-purchase temperature management may and likely has kept a bacterial contaminant, such as Salmonella or pathogenic E. coli, below the threshold for illness for an individual consumer. Improper post-purchase temperature management may and likely has contributed to elevating these pathogens above an individual’s personal threshold and, by cross-contamination in serving, increased the chance of exposure in an individual portion from the same bag.

The absence of visual signs of improper temperature exposure, such as spoilage or decay, provides no assurance that significant growth of bacterial pathogens has not occurred. Recent research evidence suggests that the pre-consumption environment may increase the aggressiveness (lowering the threshold) by activating mechanisms for human infection.

In summary, with all best efforts at prevention and control, if pathogens are present in packaged salads the consumer is at risk of illness, possible long-term health effects, or death. Keeping packaged salads cold is essential to quality and may reduce risk to individual consumers though not likely all consumers of the same lot.

Can consumers really judge if product has been temperature-compromised at the Point of Purchase?

Yes and No. I’ll bet you knew that was coming. Realistically the Yes is very small and No the more sensible response. So to keep this answer simple for a change, let’s stick with the No side of the equation and talk briefly about a potential consumer-oriented solution that always crops up.

Time:Temperature Indicators or Integrators (TTI) have been around for a long time and used on many perishable products. The function of a TTI is to make improper and abusive temperature exposure, linked to known quality defect-inducing conditions, readily apparent by a simply visual inspection, usually a color change, color development (invisible to highly visible), or progressive loss of color bars on a small patch or tag. No equipment is needed and no special training is required for anyone to get the information.

There are many types and have been many improvements in accuracy and readability over the past 15 years. For the consumer, TTI’s affixed to a bag, clamshell, or other individualized purchase unit would be the relevant location. These have been used in the EU for many years, including on value-added produce.

There are many arguments for and against the value of TTI labeling which is beyond the details of this response; retailers in the U.S. have consistently argued against their use. Do TTI’s tell the consumer anything about product safety? Not really, apart from considerations for TCS in the answer to Question #1 above.

If the TTI validations, and therefore the rate of color-change, were adjusted to pathogen growth response rather than quality loss and shelf-life parameters it could be argued that a level of consumer protection had been achieved. Under the current boundaries at the low end of cold-chain performance, would safe product be destroyed? Highly likely. Could TTI’s help simplify a consumer’s POP decision about quality? I think so. Would the use of TTI complicate a retailer’s liability? I will let the experts answer that.

*Recommendations for Handling Fresh-cut Leafy Green Salads by Consumers and Retail Foodservice Operators. 2007. Food Protection Trends. 2: 892-898

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