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Trevor Suslow Of UC Davis Speaks Out: The Truth About Consumer Reports, Bacteria And Packaged Leafy Greens

First we received a press release from Consumers Union, titled Packaged Salad Can Contain High Levels of Bacteria:

Consumers Union Urges FDA to Set Performance Standards for Greens

YONKERS, NY — Consumer Reports’ latest tests of packaged leafy greens found bacteria that are common indicators of poor sanitation and fecal contamination, in some cases, at rather high levels. The story appears in the March 2010 issue of Consumer Reports and is also available free online at Consumers Union today also issued a report urging the U.S. Food and Drug Administration (FDA) to set safety standards for greens, available online at FDA food safety legislation pending in the Senate, and passed last summer by the House of Representatives, would require the FDA to create just such safety standards.

The tests, which were conducted with financial support from the Pew Health Group, assessed for several types of bacteria, including total coliforms and enterococcus — “indicator organisms” found in the human digestive tract and in the ambient environment that can signal inadequate sanitation and the potential for the presence of disease-causing organisms. While there are no existing federal standards for indicator bacteria in salad greens, there are standards for these bacteria in milk, beef, and drinking water. Several industry consultants suggest that an unacceptable level in leafy greens would be 10,000 or more colony forming units per gram (CFU/g) or comparable measure.

Consumer Reports found that 39 percent of samples exceeded this level for total coliform, and 23 percent for enterococcus. The tests did not find E. coli O157:H7, listeria monocytogenes or salmonella — sometimes deadly pathogens which can be found in greens, although it was not expected given the small sample size. The goal was to investigate other markers of poor sanitation that should be used in the food safety management of produce.

“Although these ‘indicator’ bacteria generally do not make healthy people sick, the tests show not enough is being done to assure the safety or cleanliness of leafy greens,” said Dr. Michael Hansen, senior scientist at Consumers Union, nonprofit publisher of Consumer Reports. “Levels of bacteria varied widely, even among different samples of the same brand. More research and effort is needed within the industry to better protect the public. In the meantime, consumers should buy packages of greens that are as far from the use-by date as possible.”

For its latest analysis, Consumer Reports had an outside lab test 208 containers of 16 brands of salad greens, sold in plastic clamshells or bags, bought last summer from stores in Connecticut, New Jersey, and New York. Among the findings:

• 39 percent of samples exceeded 10,000 CFUs (or another similar measure) per gram for total coliforms and 23 percent for enterococcus, the levels industry consultants deemed unacceptable.

• 2 percent of samples exceeded French and 5 percent Brazilian standards for fecal coliform bacteria.

• Many packages containing spinach, and packages which were one to five days from their use-by date, had higher bacterial levels. Packages six to eight days from their use-by date generally fared better.

• Whether the greens came in a clamshell or bag, included “baby” greens, or were organic made no difference in bacteria levels.

• Brands for which there were more than four samples, including national brands Dole, Earthbound Farm Organic, and Fresh Express, plus regional and store brands, had at least one package with relatively high levels of total coliforms or enterococcus.

“The Senate should act immediately to pass pending FDA food safety reform legislation that requires the agency to set performance standards as well as develop safety standards for the growing or processing of fresh produce,” said Hansen. “FDA should also formally declare that certain pathogenic bacteria — such as E. coli O157:H7, salmonella, and listeria — be considered adulterants when found in salad greens.” The Senate bill, S. 510, the FDA Food Safety Modernization Act, was voted unanimously out of committee in November. The House passed similar legislation last July.

Until packaged salad becomes cleaner, consumers’ best line of defense involves following these procedures in stores and kitchens:

• Buy packages far from their use-by date.

• Wash the greens even if the packages say “prewashed” or “triplewashed.” Rinsing won’t remove all bacteria but may remove residual soil.

• Prevent cross contamination of greens by keeping them away from raw meat and poultry.

The March 2010 edition of Consumer Reports contains an article drawing on the same research, titled Bagged Salad: How Clean?

It is important that the industry response to such publicity be science-based. So we thought presenting a more technical response written by Trevor Suslow, Ph.D.,Extension Research Specialist, Postharvest Quality and Safety at UC Davis, was appropriate:

Here is a somewhat brief response, relative to the complex issues involved in responsibly addressing your questions. I have prepared this more extensively than a brief reaction to the Consumer Reports article, Packaged Salad Can Contain High Levels of Bacteria, as yours is not the first or probably last e-mail or phone call for reaction to this study I have received.


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 CR report, 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% 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 C or 107 to 111 degrees F) 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 should come with an infrared digital thermometer function.

Hope this helps.

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

We think it does help.

First, it reminds the industry that we can still do better — and it points out that “the industry” is not just the grower or processor. In our travels, we visit a lot of retailers and we find many instances of improperly functioning display equipment or of incorrect stacking that might block air flow. Because of the way liability is apportioned in the United States, producers are primarily responsible for a food safety problem — even if it could have been prevented through a more effective cold chain. So this whole area does not get the attention it needs.

Second, it points out the lack of sophistication with which Consumers Union approaches the science. The presumption that the presence of these pathogens is always an indicator of fecal contamination is not true. As Dr. Suslow puts it: “…a total coliform or fecal coliform doesn’t necessarily indicate fecal contamination in the plant world.”

More importantly, Dr. Suslow points out: “Their numbers on a leaf or fruit do not relate well to risk of illness or true and serious pathogens being present.” This is very important. There are lots of things that can be measured. The key is to find the relevant ones.

Third, though Dr. Suslow’s knowledge of science in this realm is substantial, his common sense approach is far more useful than the doctrinaire approach that Consumers Union has adopted. Dr. Suslow points out that A) consumers have a choice as to whether they prefer to eat bulk produce or fresh-cut produce, B) he eats both, C) he does not feel a need to even wash bagged salad, and D) the overwhelming safety record on fresh-cuts, with billions and billions of servings consumed overwhelmingly without incident, speaks profoundly to the safety of these products.

In contrast, Consumers Union takes the following position in its conclusion of the article: “Consumers Union supports Senate Bill 510, the Food Safety Modernization Act, that would, among other things, require the Food and Drug Administration to set stronger produce safety standards. Those should include performance standards for indicators of fecal contamination, such as generic E. coli and enterococcus” is more an inclination than an analysis.

There is not the slightest indication that Consumers Union would think differently if the industry reduced the colonization of bacteria by, say 50%. There also is not the slightest indication that it would make any difference if the industry reduces food safety issues in the next 20 years to 10% of what they were in the previous 20 years.

There is certainly no evidence that Consumers Union has studied the cost of reducing the incidence of Thermotolerant Coliforms and has come to a conclusion that this expenditure of money is the best way to improve food safety in America.

The industry has worked very hard with The California Leafy Greens Marketing Agreement, The Center For Produce Safety, and other efforts to enhance safety. Each processor has itself made significant efforts. And more efforts are underway.

We would not want to say that we can’t still find better ways. We suspect we will.

But safety is not a free good and consumers will not be helped if we make the standards such that these items have to be grown and packed in an Intel-like “clean room” and so consumers cannot afford to enjoy the product.

There is no evidence that Consumers Union has any thought other than that every product should always be made safer — even if any safety improvement would be infinitesimal and the cost extravagant.

We thank Dr. Trevor Suslow for helping us understand the science behind this matter.

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