By the time you read this, you have almost certainly heard about the Listeria monocytogenes outbreak associated with Boar's Head ready-to-eat (RTE) deli meats. While the first illness was identified in late May 2024, the scope of the outbreak was not recognized until July.¹ As of this writing, at least ten deaths among the 61 people who were sickened (of whom at least 60 required hospitalization) have occurred. More cases remain possible, given the long incubation period for listeriosis and the potential for consumers to have recalled product in their refrigerator or freezer beyond the marked sell-by dates, some of which extended into October 2024.²

Investigation by the Centers for Disease Control and Prevention (CDC) found that outbreak cases (vs. controls) were significantly more likely to have eaten liverwurst, with 19 cases specifically reporting Boar's Head brand. The outbreak strain was found in an unopened Boar's Head liverwurst product obtained from a retail store in Maryland. Boar's Head expanded its recall beyond liverwurst to include 71 other RTE deli meats produced between May 10 and July 29 at the same facility as the liverwurst, totaling more than 7 million pounds of product.³

This outbreak once again emphasizes that multiple measures are needed to reduce the risk of listeriosis associated with RTE foods: controlling contamination at the source, rigorous temperature control, and formulating foods to prevent growth during storage. The latter is the focus of this article.

FSIS Inspection Reports Reveal Sanitation Failures

The U.S. Department of Agriculture's Food Safety and Inspection Service (USDA-FSIS) inspection reports detailed unsanitary conditions at the Boar's Head processing plant in Jarratt, Virginia.⁴ Inspectors documented numerous problems in the years prior to the outbreak, including findings such as insects, leaky pipes, puddles of blood, mold on walls, and residual meat on a variety of food contact surfaces. The non-compliance reports do not mention swab tests for Listeria. Given the plant's history of repeated sanitation failures, it may have been inevitable that L. monocytogenes established itself in the facility and evaded detection, therefore preventing corrective actions to eliminate it from the equipment and environment.^5,6

The Problem of L. monocytogenes in RTE Meat Products

A 2003 risk assessment by the U.S. Food and Drug Administration (FDA) and USDA-FSIS concluded that deli meats sliced at retail caused more foodborne listeriosis cases than any other RTE food.⁷ In addition to the fact that they are a frequently consumed food, their high risk is due to factors related to both the food formulation and pathogen growth characteristics.

Deli meats have high moisture content and near-neutral pH values, facilitating L. monocytogenes growth. The high salt content of many deli meats and their requirement for refrigerated storage may provide L. monocytogenes with a competitive advantage over other microorganisms, as the pathogen exhibits relatively high salt tolerance and, perhaps most importantly, can grow at refrigeration temperatures.

While risk assessments suggest that a relatively high dose of L. monocytogenes is required to cause illness, the long shelf life of deli meats provides more time for the organism to grow to higher levels.^8,9 Exacerbating these problems is the fact that consumers and delis do not always maintain their refrigerators at recommended temperatures,^10,11 and temperatures just slightly above 3 °C (37.4 °F) support more rapid growth of L. monocytogenes than lower temperatures, as illustrated in Figure 1.^8,12,13

Pathogens present in RTE meat and poultry raw ingredients will be killed during a cook step; however, L. monocytogenes can persist in the post-lethality processing and packaging environment.⁵ For example, a full chub of meat may be fully cooked in a bag, and after cooking will be cut in half or sliced before final packaging, exposing the surface of the cooked meat product to potential recontamination from the processing and packaging environment. Deli meats face even higher risks of contamination if they are sliced and packaged in retail stores, where cleaning and sanitation practices are frequently less consistent and can spread contamination to multiple foods handled on the same slicers or tables throughout the day. USDA-FSIS estimates that slicing and packaging at retail accounts for 83 percent of deli meat-associated listeriosis illnesses.¹⁴

History of Listeriosis Outbreaks in RTE Meat and Poultry Products

As shown in Table 1, numerous L. monocytogenes outbreaks attributable to RTE meat products have occurred around the world over the past three decades. While massive, the recent Boar's Head deli meat recall is dwarfed by the Bil Mar Foods recall of RTE meat products in 1998, in which 35 million pounds of deli meats were recalled after an associated Listeria outbreak, ultimately resulting in 108 illnesses, 14 deaths, and four miscarriages/stillbirths.¹⁵ This tragedy motivated research and U.S. regulatory approval for the use of antilisterial agents (two organic acid salts—lactate and diacetate) in RTE meats to reduce the risk of growth to high levels. However, before these antimicrobials were in widespread use, another outbreak in 2002 attributed to sliced deli turkey produced by Pilgrim's Pride resulted in 54 cases of listeriosis, eight deaths, and three stillbirths/miscarriages.^16,17

Large listeriosis outbreaks linked to RTE meat products are not unique to the U.S. In 2008, contaminated deli meats produced by Canada-based Maple Leaf Foods were implicated in 57 cases of illness and caused 24 deaths.¹⁸ In response, Canada joined the U.S. in approving and encouraging the use of antimicrobials in RTE meats.¹⁹ However, the most notorious listeriosis outbreak associated with RTE meat products was the 2017–2019 outbreak associated with Tiger Brands polony in South Africa. More than 1,000 cases were identified, with 50 percent of the cases associated with pregnancies and 216 deaths reported.²⁰ It is unknown if South Africa encourages its manufacturers to modify their formulations to include growth inhibitors.

As a result of the large U.S. listeriosis outbreaks associated with RTE meat products from 1998–2002, a flurry of research efforts and regulatory initiatives began to identify strategies to prevent such events from occurring in the future. While relatively few large listeriosis outbreaks associated with RTE meat products have occurred in North America in the past decade, small, sporadic outbreaks continue to occur.^49,50

USDA-FSIS Listeria Rule Recognizes Formulation Control for Safety

In 2003, USDA-FSIS published its Listeria Rule (9 CFR part 430), outlining how producers of RTE meats should reduce the risk of L. monocytogenes in such products.⁵¹ Guidelines for recommended ways to meet the requirements of this rule have been issued, most recently in 2014.⁵²

Table 2 outlines the three Listeria Rule alternatives that establishments can choose to utilize in their Hazard Analysis and Critical Control Points (HACCP) plan. Alternative 3 (Alt. 3) relies on enhanced sanitation and environmental monitoring alone to control L. monocytogenes. Alternative 2a (Alt. 2a) requires establishments to utilize a post-lethality treatment on RTE products, while Alternative 2b (Alt. 2b) requires product reformulation with an antimicrobial growth inhibitor—a step that an interagency risk assessment concluded would reduce the number of predicted illnesses associated with products prepared or sliced at the retail deli by approximately 96 percent.^{14, 53} Finally, Alternative 1 (Alt. 1) requires the use of both a post-lethality treatment (e.g., flash pasteurization or high-pressure processing) and the reformulation of a product to include an antimicrobial growth inhibitor.⁵²

While establishments that use Alt. 1 and Alt. 2 are also required to maintain and verify sanitation in their environment, establishments choosing Alt. 3 for RTE deli meats must complete more frequent verification testing of food contact surfaces and are subject to more intense verification activity by FSIS.⁵²

The "belt-and-suspenders" approach of Alt. 1 and Alt. 2 are used by many North American manufacturers of RTE products. The use of multiple hurdles for Listeria control likely accounts for the reduced number of listeriosis cases and recalls attributable to RTE meats produced in the U.S., despite increasingly sensitive and enhanced surveillance.⁵⁴

When choosing to use an antimicrobial under Alt. 1 or Alt. 2, establishments must validate that their reformulation results in no greater than a 2-log increase of L. monocytogenes during the shelf life of the product. Validation includes both the scientific or technical support for the intervention (via processing guidelines, performance standards, challenge studies, or other means enumerated in the Listeria Rule), as well as demonstrating its efficacy in practice via an in-plant demonstration.⁵²

While the guidelines do not specify a required temperature for validation studies, shelf life is known to be shorter at higher incubation temperatures. A more stringent approach is to follow the National Advisory Committee on Microbiological Criteria for Foods (NACMCF) guidelines, which limit growth to more than a 1-log increase in L. monocytogenes numbers over 1.25 times shelf life, ideally at both 4 °C and 7 °C (39.2 °F and 44.6 °F).⁵⁵ Canada limits growth to no more than a 1-log increase when stored at 7 °C, while New Zealand recognizes growth as no greater than a 0.5 log increase.^{56, 57}

Validated Synthetic Antilisterial Antimicrobials for Use in RTE Meats

Even with the most rigorous environmental control program, L. monocytogenes can occasionally find its way onto RTE meats. As a result, many manufacturers have opted to reformulate their foods to comply with Alt. 2b to supplement good manufacturing practices and better protect the consumer. In the years following the 1998–2002 listeriosis outbreaks, a variety of synthetic antimicrobials were shown to be effective in controlling L. monocytogenes in RTE meat products and have been approved for use in RTE meats, as illustrated in Table 3.

Antimicrobial agents added to the final product formulation are meant to be effective over the course of the shelf life; therefore, they are classified as ingredients and not processing aids. In order to be used in processed meats, antimicrobial agents must be generally recognized as safe by FDA or be included on USDA's Safe and Suitable Ingredients list, and they must be listed on the ingredient label.⁶⁷

Does Consumer Demand for Clean Labels Drive RTE Meat Product Manufacturers to Try to Control L. monocytogenes Without Antimicrobials?

Consumer demand for cleaner labels on food products has meant that some food manufacturers have tried to eliminate synthetic ("chemical-sounding") ingredients to increase appeal to consumers.^68,69 Perhaps because of such a commitment to clean-label ideals, the products manufactured in Boar's Head's Jarret facility relied upon Alt. 3 (no post-lethality treatment or antimicrobial agent or process, just sanitation) for Listeria control in its RTE products.⁷⁰ A breakdown in sanitation and ineffective control of the source of contamination in a facility manufacturing RTE meats, along with the ability of the product to support Listeria growth, are common threads in the Bil Mar, Pilgrim's Pride, Maple Leaf, and Tiger Brand outbreaks. Had their products been formulated with a microbial growth inhibitor, the outbreak likelihood may have been reduced.^14,71

Clean-Label Antimicrobials for Use in RTE Meat Products in the U.S.

Despite evidence of their ability to control L. monocytogenes and other pathogens in RTE meat products, the presence of antimicrobial ingredients (such as those listed in the first column of Table 4) in foods might discourage consumers because of their overtly "chemical" names.

However, in more recent years, a variety of clean-label antimicrobials have been developed and demonstrated to be effective in controlling L. monocytogenes in RTE meat products.^72,73 Many of these clean-label antimicrobials are natural versions of the chemicals that have already been shown to be effective in RTE meats (Table 4). In some cases—especially for some proprietary products—clean-label antimicrobials are combinations of such agents.⁷⁴

As mentioned earlier, a 2013 U.S. interagency risk assessment of L. monocytogenes in retail delis predicted that the use of a growth inhibitor in a retail deli product reduced the relative risk of listeriosis per serving by approximately 96 percent, which the report concluded "almost completely eliminated" the listeriosis risk.^14,53

Despite such compelling promise, barriers exist for the use of growth inhibitors/antimicrobials in RTE meat products, even when they are clean-label ingredients. First, clean-label ingredients are often more expensive than their conventional counterparts. Second, the exact active ingredients and proportions are often guarded as "trade secrets" or "proprietary," making the utilization of past challenge studies, microbial modeling, or other validations difficult to apply. Due to the variation in type and concentration of active ingredients, each growth inhibitor considered for use should be validated for its efficacy in specific substrates. Another challenge is lot-to-lot variability in levels of active compounds in some clean-label alternatives, which can influence effectiveness. Even though an ingredient may inhibit growth, differences in meat matrix may affect overall efficacy (Figure 2). Finally, some clean-label ingredients, by virtue of usage at relatively higher levels and including more than just the active compounds, may negatively impact the color, aroma, or taste of the final product.

Modes of Action of Synthetic and Clean-Label Antimicrobials

Various modes of action have been proposed for antimicrobials. Weak organic acids (e.g., acetic and lactic acid, which are also components of some clean-label antimicrobials) disrupt cellular membranes, acidify the cytoplasm, and inhibit metabolic activity.⁷⁵ This activity is driven by the ability of organic acids to cross the plasma membrane in an undissociated state; upon entering the cellular environment, dissociation occurs, and the ions cannot cross the cellular membrane, affecting cellular processes and internal pH.⁷⁵ Organic acids are often used in their buffered forms (to reduce the effect on pH; e.g., sodium or potassium lactate and sodium acetate) and combined with NaCl in RTE meats.

While cultured sugars and vinegars are the most frequently used clean-label alternatives, other solutions are available but are not as well validated. Antimicrobial peptides, such as the bacteriocin nisin produced by Lactobacillus lactis, enhances the efficacy against L. monocytogenes in bologna when applied with other organic acids.^76,77 Numerous plant-derived extracts including pomegranate peel, olive leaf, onion, thyme, clove, and lemongrass presumably act on bacteria by causing leakage of cellular contents, dissipation of ATP, and nucleic acid synthesis inhibition, mainly driven by the presence of hydroxyl groups.⁷⁸

Antimicrobial agents added to RTE meats, whether conventional or clean label, are best utilized when applied as part of the hurdle concept. Combining synthetic or clean-label antimicrobials with different preservation factors (or hurdles), such as low water activity, temperature control during storage, acidulation, or salt, can further extend the product shelf life by enhancing pathogen inhibition.⁷⁹

While nitrite levels used at levels within regulatory limits are not listeriostatic by themselves, the compound potentiates the antimicrobial activity of other synthetic and clean-label antimicrobials, as well as serving as a potent inhibitor against Clostridium botulinum and C. perfringens.^61,62,80-83 The demand for "natural" ingredients has led to an increased use of cultured celery (juice or powder) as a nitrite source. Research has demonstrated that L. monocytogenes inhibition is maintained as long as nitrite concentrations are equal (Figure 3).^81,84 The magnitude of nitrite-antimicrobial synergism is still being elucidated. Glass et al. (2008)⁶² determined that a minimum 30-ppm nitrite enhances L. monocytogenes inhibition by lactate-diacetate, and the effect increases with higher concentrations.

Antimicrobial selection is dependent on several factors, including desired labeling (natural or conventional ingredients), antimicrobial delivery method (powder or liquid), target organisms of control, and impact on the product itself. USDA's Safe and Suitable Ingredients List enumerates those ingredients currently approved for use (USDA-FSIS Directive 7120.1), describing the substance itself, the intended use of the product, the amount, and any labeling requirements.⁶⁷ Additionally, USDA has established guidelines for new technology notifications as emerging antimicrobial technologies are discovered.⁸⁵

Although growth of certain microbial spoilage bacteria can be inhibitory to L. monocytogenes due to acid production and competition for nutrients, they are not reliable as an intervention strategy due to their sporadic nature. There are some concerns that use of antimicrobials could "cover up spoilage," resulting in a greater likelihood that a consumer will eat an unsafe product. However, many meat spoilage microbes are more resistant to commercial growth inhibitors than L. monocytogenes and, therefore, require high levels of growth inhibitors to be affected.⁸⁶ The optimal system for safe foods with long shelf life is formulating products to inhibit Listeria and rigorous cleaning and sanitation to control spoilage.

Conclusions

The relative rarity of large U.S. listeriosis outbreaks associated with RTE meats in the last 20 years appears to have ended, coinciding at a high point of success for the preservative-free movement. The use of clean-label antimicrobial agents in RTE meat products might reduce or prevent future listeriosis outbreaks (and associated deaths, hospitalizations, associated costs, product recalls, and erosion of company reputations) while maintaining consumer confidence.

That being said, the catalyst for this article was the tragic Listeria outbreak in Boar's Head products. During the writing process, a new Listeria recall was executed for RTE meat and poultry products produced by BrucePac of Oklahoma.^87,88 At publication, this recall involved 11.8 million pounds of product, some of which was supplied to schools.⁸⁷ The recall was initiated after routine product testing of RTE chicken was found positive for L. monocytogenes.⁸⁷ A survey of ingredient lists of recalled products found that antimicrobial ingredients were included in some, but not all, of the chicken formulations.⁸⁸ While no illnesses have been reported to date, this recall, occurring so soon after the Boar's Head outbreak, reaffirms the persistent threat posed by Listeria in RTE meat and poultry products.

Acknowledgments

The authors would like to thank Kathleen O'Donnell, Dawn Pickett, and Robin Kalinowski for reviewing a draft of this manuscript.

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