Food Safety Magazine: Given the recent spate of foodborne illness outbreaks associated with Listeria monocytogenes contamination, and several recent food recalls and consumer advisories, this pathogen is once again in the spotlight. As an authority on Listeria monocytogenes, would you provide some background on the emergence of this pathogen as a health concern?
Catherine Donnelly: Food recalls as a result of Listeria monocytogenes contamination definitely have been on the increase in recent months, most notably the Pilgrim's Pride/Wampler Foods recall of 27.4 million pounds of ready-to-eat poultry products in October. The recall was the largest in U.S. history associated with Listeria contamination of meat products. I think the reason we are seeing more Listeria-related recalls is two-fold: First, there have been tremendous advances in disease surveillance made by the U.S. Centers for Disease Control and Preven-tion (CDC) through PulseNet and Food-Net, and second, there is more attention focused on this pathogen on the part of the regulatory agencies.
With regard to the former, we have an excellent surveillance system at work in the U.S., which has raised the bar for the way the industry has to manufacture food. With PulseNet, for example, you have a whole public health laboratory system that is actively sharing information on genetic fingerprints of strains that can be isolated in different parts of the country, which allows public health officials to get a jump on the sources of foodborne illness. With the national distribution of most food products, it used to be more difficult to rapidly track sources of outbreaks. Today, if CDC scientists start to see the same microbial strains appear in different regions of the country, it's a trigger that we could have a nationwide outbreak on our hands. We really are using Star Wars technologies in public health surveillance, and as such, the time it takes to understand that outbreaks are occurring has been greatly shortened. This is one of the explanations as to why recall activity is increasing.
In terms of regulatory attention to Listeria monocytogenes, the fact is that regulators are looking for it, food processing plants are looking for it, and once you start increasing the frequency of activities designed to detect a pathogen, you are going to find it more frequently and increased recalls will result.
In terms of the organism itself, Listeria is a very common pathogen that can be found almost anywhere in the environment. Despite its ubiquitous nature and the seemingly high number of recalls of late, Listeria-caused human illness rates are remaining fairly stable. Dr. Paul Mead of the CDC published a 1999 study that estimated that 76 million cases of foodborne illness occur per year in the U.S. This study specifically estimates that of those cases, there are about 2,500 cases of listeriosis annually. So, while recalls may be on the increase, this shows that the food industry is doing a really good job in keeping the number of Listeria-related cases either stable or on a decline.
The key reason for all of the regulatory focus on this organism is that it causes a higher rate of hospitalization than any other foodborne pathogen: 95% of the individuals who acquire listeriosis are hospitalized and this disease is the leading cause of death from a foodborne pathogen. The way I like to explain this concept to people is to say that even though there are only 2,500 cases of listeriosis per year in the U.S., those 2,500 cases result in about 500 deaths. Compare that to Salmonella, which is responsible for about 1.5 million cases of illness. Those same 1.5 million cases of salmonellosis result in about 500 deaths. This comparison really illustrates the fact that Listeria is a very deadly pathogen for the individuals it affects.
Food Safety Magazine: How far along is the food industry in assessing risk as it pertains to this pathogen? Do the control mechanisms used by industry address the risk assessments?
Donnelly: The Department of Health and Human Services (HHS), the U.S. Food and Drug Administration (FDA) and the U.S. Department of Agriculture (USDA) made identifying high risk foods for Listeria contamination really easy for us by publishing the joint Listeria Risk Assessment paper in 1999. A number of products were identified as high risk foods for Listeria contamination, including smoked seafood, ready-to-eat (RTE) meat and poultry products, soft cheeses, raw milk and Mexican-style cheese, especially products not commercially prepared.
Risk assessment is a good tool for the industry in its efforts to produce safe foods. A good example is the comparison of an RTE meat with a potato salad. Most commercially prepared potato salads in this country are manufactured using preservatives and inhibitor systems. They are very acidic products, and if you look at Listeria in a commercially prepared potato salad, it dies off over time. FDA presented some data earlier this year at the International Association of Food Protection (IAFP) meetings in San Diego, CA, showing the rapid die-off of Listeria in commercially prepared potato salad. This is an example of a food that simply does not support the growth of Listeria.
On the other hand, RTE deli meats or any RTE meat product are shown to be of higher risk in terms of Listeria contamination. Unless these products are formulated with chemical barriers to Listeria growth (and today, some of these products are being formulated with that control in place), there's nothing to stop the growth of Listeria on that type of product. This is in part because the organism has adapted in its ability to grow, albeit slowly, at refrigeration temperatures. If you look at RTE meat products, you will find that they all carry a fairly long shelf-life. The combination of a product that supports the growth of the organism coupled with extended storage at refrigeration temperatures really speaks to why these products are assessed at a higher risk level.
The main control mechanism that the food industry has in place for protecting products like RTE meat and poultry from Listeria contamination is to clean and sanitize to eliminate the pathogen and then to conduct environmental testing and monitoring to verify that sanitation efforts have been successful. In reality, there are really good and high-profile food companies that are using every scientific and sanitation resource available to them, but even in the best situations, Listeria is a very difficult pathogen to control from an environmental perspective. We know that Listeria establishes niches in food processing plant environments and unless there is absolutely rigorously focused sanitation, that organism can persist for months or years within food plant environments.
The other reality is that most food processing plants in the U.S. were not designed with control of this pathogen in mind. For example, the location of drains, if there are drains at all, may have been placed in an undesirable high-traffic floor area where cross-contamination can easily occur. One of the responses to the Listeria crisis in the mid-1980s in the dairy industry was major plant redesign activities, including redesign of floors so they could be washed and sanitized effectively, redesign of drains so they could be effectively cleaned and sanitized, and increased protection of the filling equipment from air contamination.
The difficulty in being able to control Listeria simply through sanitation really speaks to the need for the development of other terminal processes or process interventions to eliminate the pathogen in high-risk food products.

Food Safety Magazine: What is the status of government, industry or academic research initiatives or rules with regard to Listeria monocytogenes?
Donnelly: I think that the real frustration for the food industry is the whole notion of zero tolerance in terms of the U.S. regulatory policy. Try as companies might to reduce the incidence of Listeria in the plant, they have to operate under this zero tolerance policy, which offers no incentive for the company to go in and test finished product to make sure it is in compliance. This is because, with zero tolerance at work, if you find Listeria you've got to withhold your own product. To address this challenge, most food manufacturers try to manage the plant environment, correctly assuming that if the environment is being properly managed then the risk of Listeria exposure of product is substantially reduced. But again, even the most rigorous sanitation efforts may not prevent this pathogen from establishing itself somewhere in the plant.
Other countries have adopted a risk-based system to deal with Listeria, where officials take regulatory action against products at highest risk. Canada, for instance, has identified four risk categories, and those products placed in the highest risk category are foods that can support the growth of Listeria to high levels and have been linked to a foodborne disease outbreak. In those particular foods, you are allowed zero Listeria in 25 grams. Foods that don't support the growth of Listeria and haven't been involved in an outbreak are placed in the lowest risk category, where there are tolerance limits for Listeria monocytogenes up to 100 per gram. This risk-based approach makes sense from a public health perspective because it allows you to focus regulatory resources on food products assessed with the highest risk.
Countries outside of the U.S. have adopted tolerance limits because they understand that while the risk of Listeria monocytogenes contamination can be reduced, it is unlikely that the presence of this organism is going to be eliminated. However, I also think that it is important to remember that most of the cases of listeriosis reported in the U.S. are sporadic cases; they are not related to outbreaks. With respect to this recent outbreak reported in the Northeast, for example, there are seven patients that have died to date, but when you consider that the other 493 deaths from listeriosis that are estimated to occur this year aren't related to this specific outbreak, you can see that outbreaks actually account for a small percentage of cases that occur. Even so, there are many ongoing discussions and workshops between industry, government and academic concerns to address the zero tolerance approach that is the current policy in the U.S.
There's a lot of active Listeria research being conducted by industry, government, trade associations and academic research centers. One of the key research questions is: Are all strains of Listeria monocytogenes equally virulent? There's not a lot of good scientific information available as yet to give us a good answer to this question. One of the exciting breakthroughs announced earlier this year was from Dr. Pascale Cossart of the Pasteur Institute. At the American Society for Microbiology (ASM) annual meeting in May 2002, she reported that the Listeria monocytogenes genome has been sequenced. With this development, researchers can actually probe certain genes to find out whether the genes are present in all strains of Listeria monocytogenes, or whether there are only certain strains that show high virulence and can be linked to certain outbreaks. They also can study whether certain Listeria strains possess genes that are different from strains that seem to persist environmentally or that don't have as great an impact on human illness.
Another one of the researchable questions we need to get a handle on is, What's the infectious dose of Listeria? Despite 20 years of very focused attention on this organism, we still aren't really any closer to an answer. And, at the same time, we're trying to get a handle on infectious dose; in other words, what susceptible populations are emerging? We know that individuals with compromised immune systems are susceptible to Listeria. There now is some suggestion that diabetics are susceptible to listeriosis, and we know that there is an epidemic of diabetes in our society. For those individuals in these immunocompromised states, no one can conclusively answer the question of what level of risk is incurred. In the future, I think we will answer this question, but for now, the problem is that to get a handle on this you have to work backwards, and in the majority of cases of listeriosis, the lag time between the ingestion of the product and the onset of symptoms can be fairly lengthy. This makes identifying the suspected food source and figuring out what levels of the pathogen were in that product kind of difficult.

Food Safety Magazine: Have there been any developments in screening/detection tools or technologies for Listeria monocytogenes that have proved useful to the food industry?
Donnelly: The food industry really has every available screening and detection technology that you're going to want to employ in the detection, identification and characterization of Listeria monocytogenes. Of course, the rapid and automated microbiological methods have helped industry tremendously. When we're talking about screening and detection tools for Listeria, we're essentially talking about a focus on environmental monitoring and verification in the food plant. Of course, depending on the level of expertise in the food company and how the facility is designed for production, most testing is not advised within the plant environment simply because you have to run positive controls in your testing and you really don't want to introduce that pathogen into your environment.
Since so many laboratory facilities are located off-site, food companies will take environmental samples and ship them to companies that will handle the analysis. I would say that advances in sampling methods for environmental hygiene monitoring and verification purposes have helped the industry a great deal. So much progress has been made in sampling techniques that a food company can get very reliable results using standardized procedures. These advances range from the use of sterile sponges, swabs and paddles for product contact surface collection, to the use of Petrifilm (3M Co.) as a sanitation verification method.
With regard to the identification and characterization of Listeria monocytogenes, there are two techniques that are widely incorporated in various diagnostic test kits and automated systems: enzyme-linked immunosorbent assay (ELISA) and polymerase chain reaction (PCR). The very rapid ELISA-based test kits are used as screening procedures to detect high levels of Listeria within 24-48 hours. It should be understood, however, that low levels of Listeria can escape detection and go on to grow on food products if the ELISA is the only screening procedure used. With PCR technology, the microbiologist doesn't have the same downside, because PCR can amplify even a nonviable cell. In addition, most of the PCR methods include some type of enrichment step so that you can differentiate between viable and nonviable cells, and thus detect with greater sensitivity low levels of Listeria.

The real-time PCR technology is very exciting, because it is very definitive and it substantially reduces the time for confirmation that you need. If you are an RTE meat producer and you're operating on test-and-hold, you'd like to get results back as soon as possible so you know whether or not you've got to withhold product. The advantages that PCR offers also are being recognized by the federal government, which is now starting to include rapid PCR screening methods in some of its regulatory procedures. Ironically, the U.S. Department of Defense is supporting a lot of research on real-time PCR for monitoring of the food supply for bioterrorist threats. If one could say that anything positive could have come out of September 11, I think we could say that this renewed focus on how we achieve a safer food supply through use of some of these technologies could be viewed as a good outcome.
While I think there have been amazing advances in our detection capabilities for Listeria, all the way now to real-time PCR methods, the problem is that the methods can be expensive. For most manufacturers who are dealing with low margins, we have to ask whether these are the most practical approaches and the best use of resources? Most people in the industry would rather get away from testing and go to the interventions that are going to help control this pathogen and reduce its incidence. For example, Kraft Foods has published information looking at reformulation of hot dogs using a preservative system that very effectively controls growth of Listeria, because they know that this is going to have a measurable impact on public health. Also, there's a lot of discussion about the use of electronic pasteurization as a terminal intervention in the package step to eliminate not only Listeria but other pathogens.
Food Safety Magazine: Let's talk about these developments in intervention and control technologies for Listeria monocytogenes. What is available to the food industry?
Donnelly: If you are looking at any kind of food product that is going to undergo refrigerated storage, the more you do up front to reduce those initial loads is going to dictate how many organisms you're ultimately going to end up with on a given product. This is why food companies are looking with high interest at developments in intervention technologies, especially in terms of reducing Listeria counts.
First, there are many interventions used as part of the sanitation program in food companies that have a direct impact on reducing the incidence of Listeria monocytogenes. Some of the procedures used today are drastically different from how we operated 10 years ago. These include the use of advanced chemical sanitizers to clean and sanitize surfaces and the rotation of those chemical sanitizers so that you're not giving organisms a chance to develop resistance over time. For companies that manufacture RTE foods, there now is a fairly elaborate protocol for employee gowning, making sure employees are wearing boots that can be more easily cleaned and sanitized, making sure that areas involving food production are segregated from raw areas, and making sure that personnel don't cross between raw and cooked product sides. The use of foot baths, foaming sanitizers and handwashing systems have been incorporated to a great degree, as well. So, the sophistication with which we clean and sanitize food plants has improved dramatically in a relatively short period of time.
Another intervention strategy is one that is focused on making changes within the products themselves. In other words, industry is looking at how to build food safety into the products with reformulation. I mentioned Kraft Foods, for instance, which has developed a potassium lactate and sodium diacetate preservative system that, when used in the formulation of products like hot dogs, really creates a good chemical barrier to the growth of Listeria. This kind of intervention strategy--good environmental controls, employee practices and the lethal heat treatment of these products coupled with the formulation of product with chemical barriers--is going to substantially reduce the processor's risk of Listeria contamination.
Again, electronic pasteurization, especially when done in the package, affords a tremendous food safety tool, especially with some of the RTE meat products for which we know that Listeria control is a huge problem. Although electronic pasteurization is not a substitute for sanitation or other food safety interventions, it is another one of those tools that's going to add a margin of safety. If you're starting with high-quality ingredients and you're protecting your product throughout its manufacture, then this is a final step to assure that everything you've done right will render a very safe, quality finished product. For example, most of the products implicated in listeriosis problems don't have detectable off-odor or quality problems as indicators. The notable exception to this is the 1994 chocolate milk foodborne illness outbreak linked to Listeria that occurred in Illinois, where complaints about off-flavor led health inspectors to hone in on that product. For the most part, however, in the case of refrigerated, ready-to-eat foods that are refrigerated over an extended period, you usually don't have any visible quality parameters that would alert you to the fact that Listeria might be present. So again, especially if done in package, electronic pasteurization is that final step that assures product safety.
Ultimately, consumers are going to have to decide whether it is worth paying more for products treated by electronic pasteurization, knowing that you've got this added assurance of food safety. I think that the current test marketing of irradiated beef is showing that, yes, some consumers are certainly willing to pay for that added margin of safety. I think you will see a tremendous increase in the use of this technology. In fact, my local Price Chopper supermarket just did a press conference introducing irradiated ground beef. And many other supermarkets and foodservice operations have decided to offer consumers the opportunity to decide for themselves.
Some other non-thermal processing intervention technologies also look promising. High pressure processing (HPP) is one emerging non-thermal technology that, according to available information, is effective against Listeria and other pathogens on the food products themselves. There's been a lot of good research done in this area, such as studies on cheese products where you don't want to heat treat the milk. HPP is a good technology that eliminates the need for heat treatment. Another non-thermal intervention is the use of ozone as a sanitizer, which can be a very effective in reducing Listeria levels. We've done some work with ozone in our laboratory looking at whether we can decontaminate apples using an ozone wash system. We've found that it is effective as a strategy that leads to the reduction of the load of organisms, though not a panacea. As with many intervention strategies, a multi-hurdle approach provides more assurance.
In general, we know that thermal treatments/pasteurization of foods is effective against Listeria. We also know that the greatest risk of Listeria growth is through process contamination. So, with any of these technologies, it is going to be very important that the intervention is applied in final package, because just like pasteurized milk, if you don't protect that product from recontamination after thermalization, you've got a huge problem on your hands. This also is true of the non-thermal intervention strategies. It's going to be essential that after you've used electronic pasteurization, conventional pasteurization, high pressure processing or some other non-thermal intervention, you must also be careful to protect that product from further recontamination.
Food Safety Magazine: What are some of the challenges posed by Listeria that the industry will continue to face? What do you think are the next steps that can be taken by stakeholders to help reduce Listeria contamination rates or levels in food processing and foodservice operations?

Donnelly: One of the challenges is the critical issue of time and temperature in the control of Listeria. We know that Listeria can grow even at ideal refrigeration temperatures, and once you start elevating refrigeration temperatures beyond 45F, you have rampant growth of the pathogen. The 1999 Listeria Risk Assessment highlighted the fact that both home refrigeration and retail refrigeration do not function perfectly. Audits International (EcoSure) was a contractor to FDA in the Listeria Risk Assessment, and it found that 26% of home refrigerators were operating at temperatures above 45F, and an even higher percentage at retail. This indicates that we could do a lot to improve the cold chain and thereby improve our efforts against Listeria.
Again, there have been tremendous advances in disease surveillance that have been made by the CDC through the PulseNet and FoodNet systems. These excellent surveillance efforts are going to continue, as they should, in order to protect public health. I think the food industry has to understand that just as the use of technology for disease surveillance has drastically changed, we, too, need to employ the very best strategies to get control of pathogens like Listeria. It is important for the food industry to look at advances in technology, and at improving employee training and education. We need to take a closer look at the way the Hazard Analysis & Critical Control Points (HACCP) system is being employed in certain food manufacturing facilities and question the idea that attending a one-day HACCP certification course will make someone fully cognizant of microbiology and microbiological control. Many food company employees are attending these one-day HACCP certification courses, but there is just no substitute for companies producing large amounts of food to have that in-house microbiologist or someone that understands the microorganisms that they are trying to deal with. That one-day HACCP certification might be creating a false sense of security and knowledge.
We also need to do a better job of educating consumers about Listeria. Increasingly, we see a lot of government-issued advisories for high risk consumers, especially in the RTE food area, but at some level, people are still going to eat salads and consume raw vegetables and other products in which some level of Listeria can reside and pose some risk to certain individuals. We're never going to live in a Listeria-free environment, and so those consumers who are at greatest risk should be provided information about the foods that pose a significant health risk with the suggestion that they might want to alter their dietary practices for a time, say during chemotherapy treatments or pregnancy.
Finally, I would note that, based on information gathered through FoodNet, the incidence of listeriosis in the human population is on the decline. In the 1999 Listeria Risk Assessment, President Clinton called for a reduction in the cases of listeriosis to an incidence level of .25 cases per 100,000 population, and we're about there. I think that the food industry gets a lot of credit for the very significant reduction in the number of cases of listeriosis. It wasn't too long ago when we had about eight cases per million people, and now we're down to about 2.5 in a million. When you think about the mortality rate of the organism, all of these cooperative efforts of industry, government and academia are saving lives, and that's really where the rubber hits the road.