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.

References

1. U.S. Department of Agriculture, Food Safety and Inspection Service (USDA-FSIS). "Boar's Head Provisions Co. Recalls Ready-to-Eat Liverwurst and Other Deli Meat Products Due to Possible Listeria Contamination." July 26, 2024. https://www.fsis.usda.gov/recalls-alerts/boars-head-provisions-co--recalls-ready-eat-liverwurst-and-other-deli-meat-products.
2. Centers for Disease Control and Prevention (CDC). "Investigation Update: Listeria Outbreak, Meats Sliced at Delis." September 25, 2024. https://www.cdc.gov/listeria/outbreaks/details-delimeats-7-24.html.
3. USDA-FSIS. "Boar's Head Provisions Co. Expands Recall for Ready-to-Eat Meat and Poultry Products Due to Possible Listeria Contamination." July 30, 2024. https://www.fsis.usda.gov/recalls-alerts/boars-head-provisions-co--expands-recall-ready-eat-meat-and-poultry-products-due.
4. USDA-FSIS. "Noncompliance Report, Establishment Number(s): M12612+P12612 from 06/01/2023 to 07/29/2024." https://www.fsis.usda.gov/sites/default/files/media_file/documents/Non-Compliance_Reports_112022-To-812024.pdf.
5. Malley, T.J.V., J. Butts, and M. Wiedmann. "Seek and Destroy Process: Listeria monocytogenes Process Controls in the Ready-to-Eat Meat and Poultry Industry." Journal of Food Protection 78 (2015): 436–445.
6. Butts, J.N. "Seek and Destroy: Best Practices for Controlling Environmental Pathogens." Food Quality & Safety. August 14, 2019. https://www.foodqualityandsafety.com/article/environmental-pathogens-best-practices-process-control/?singlepage=1.
7. U.S. Food and Drug Administration (FDA) Center for Food Safety and Applied Nutrition (CFSAN) and USDA-FSIS. "Quantitative Assessment of the Relative Risk to Public Health from Foodborne Listeria monocytogenes Among Selected Categories of Ready-to-Eat Foods." September 2003. https://www.fda.gov/media/77947/download.
8. Zhang, L., S.R. Moosekian, E.C. Todd, and E.T. Ryser. "Growth of Listeria monocytogenes in Different Retail Delicatessen Meats During Simulated Home Storage." Journal of Food Protection 75 (2012): 896–905.
9. Pouillot, R., K.C. Klontz, Y. Chen, et al. "Infectious Dose of Listeria monocytogenes in Outbreak Linked to Ice Cream, United States, 2015." Emerging Infectious Diseases 22 (2016): 2113–2119.
10. James, C., B.A. Onarinde, and S.J. James. "The Use and Performance of Household Refrigerators: A Review." Comprehensive Reviews in Food Science and Food Safety 16 (2017): 160–179.
11. Brown, L. G., E.R. Hoover, and B.V. Faw, et al. "Food Safety Practices Linked with Proper Refrigerator Temperatures in Retail Delis." Foodborne Pathogens and Disease 15 (2018): 300–307.
12. ComBase. "ComBase Predictor." 2024. https://combase.errc.ars.usda.gov/default.aspx.
13. Glass, K.A. and M.P. Doyle. "Fate of Listeria monocytogenes in processed meat-products during refrigerated storage." Applied Environmental Microbiology 55 (1989): 1565–1569.
14. USDA-FSIS. "FSIS Best Practices Guidance for Controlling Listeria monocytogenes (Lm) in Retail Delicatessens." June 2023. https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS-GD-2023-0004.pdf.
15. Mead, P. S., E.F. Dunne, L. Graves, et al. "Nationwide Outbreak of Listeriosis Due to Contaminated Meat." Epidemiology & Infection 134 (2006): 744–751.
16. CDC. "Outbreak of Listeriosis—Northeastern United States, 2002." Morbidity and Mortality Weekly Report 51 (2002): 950–951.
17. Gottlieb, S. L., E.C. Newbern, P.M. Griffin, et al. "Multistate Outbreak of Listeriosis Linked to Turkey Deli Meat and Subsequent Changes in US Regulatory Policy." Clinical Infectious Diseases 42 (2006): 29–36.
18. Currie, A., J.M. Farber, C. Nadon, et al. "Multi-Province Listeriosis Outbreak Linked to Contaminated Deli Meat Consumed Primarily in Institutional Settings, Canada, 2008." Foodborne Pathogens and Disease 12 (2015): 645–652.
19. Health Canada. "Policy on Listeria monocytogenes in Ready-to-Eat Foods." April 1, 2011. https://www.canada.ca/content/dam/hc-sc/migration/hc-sc/fn-an/alt_formats/pdf/legislation/pol/policy_listeria_monocytogenes_2011-eng.pdf.
20. Kaptchouang Tchatchouang, C.-D., J. Fri, M. De Santi, et al. "Listeriosis Outbreak in South Africa: A Comparative Analysis with Previously Reported Cases Worldwide." Microorganisms 8 (2020): 135.
21. Graves, L. M., S.B. Hunter, A.R. Ong, et al. "Microbiological Aspects of the Investigation that Traced the 1998 Outbreak of Listeriosis in the United States to Contaminated Hot Dogs and Establishment of Molecular Subtyping-Based Surveillance for Listeria monocytogenes in the PulseNet Network." Journal of Clinical Microbiology 43 (2005): 2350–2355.
22. Forbes. "The Long Climb Back." June 6, 2013. https://www.forbes.com/forbes/2003/0106/146.html.
23. De Valk, H. V. Vaillant, C. Jacquet, et al. "Two Consecutive Nationwide Outbreaks of Listeriosis in France, October 1999–February 2000." American Journal of Epidemiology 154 (2001): 944–50.
24. CDC. "Multistate Outbreak of Listeriosis—United States, 2000." Morbidity and Mortality Weekly Report 49 (2000): 1129–1130.
25. Sim, J., D. Hood, L. Finnie, et al. "Series of Incidents of Listeria monocytogenes Non-Invasive Febrile Gastroenteritis Involving Ready-to-Eat Meats." Letters in Applied Microbiology 35 (2002): 409–13.
26. Frye, D.M., R. Zweig, J. Sturgeon, et al. "An Outbreak of Febrile Gastroenteritis Associated With Delicatessen Meat Contaminated with Listeria monocytogenes." Clinical Infectious Diseases 35 (2002): 943–949.
27. Winter, C. H., S.O. Brockmann, S.R. Sonnentag, et al. "Prolonged Hospital and Community-Based Listeriosis Outbreak Caused by Ready-to-Eat Scalded Sausages. Journal of Hospital Infection 73 (2009): 121–128.
28. Delaune, E., T. Sokol, R. Ratard, et al. "Outbreak of Invasive Listeriosis Associated with the Consumption of Hog Head Cheese—Louisiana, 2010. Morbidity and Mortality Weekly Report 60 (2011): 401–405.
29. Hächler, H., G. Marti, P. Giannini, et al. "Outbreak of Listerosis Due to Imported Cooked Ham, Switzerland 2011." Eurosurveillance 18 (2013): 20469.
30. Gelbíčová, T., M. Zobaníková, Z. Tomáštíková, et al. "An Outbreak of Listeriosis Linked to Turkey Meat Products in the Czech Republic, 2012–2016." Epidemiolgy & Infection 146 (2018): 1407–1412.
31. Ruppitsch, W., R. Prager, S. Halbedel, et al. "Ongoing Outbreak of Invasive Listeriosis, Germany, 2012 to 2015." Eurosurveillance 20 (2015): 30094.
32. Kleta, S., J.A. Hammerl, R. Dieckmann, et al. "Molecular Tracing to Find Source of Protracted Invasive Listeriosis Outbreak, Southern Germany, 2012–2016." Emerging Infectious Diseases 23 (2017): 1680–1683.
33. Jensen, A. K., E.M. Nielsen, J.T. Björkman, et al. "Whole-Genome Sequencing Used to Investigate a Nationwide Outbreak of Listeriosis Caused by Ready-to-Eat Delicatessen Meat, Denmark, 2014." Clinical Infectious Diseases 63 (2016): 64–78.
34. Dahl, V., L. Sundqvist, I. Hedenström, et al. "A Nationwide Outbreak of Listeriosis Associated with Cold-Cuts, Sweden 2013–2014." Infection Ecology & Epidemiology 7 (2017): 1324232.
35. Lachmann, R., S. Halbedel, M. Adler, et al. "Nationwide Outbreak of Invasive Listeriosis Associated with Consumption of Meat Products in Health Care Facilities, Germany, 2014–2019." Clinical Microbiology and Infection 27 (2021): 1035.e1.
36. Duranti, A., M. Sabbatucci, G. Blasi, et al. "A Severe Outbreak of Listeriosis in Central Italy with a Rare Pulsotype Associated with Processed Pork Products." Journal of Medical Microbiology 67 (2018): 1351–1360.
37. Pietzka, A., F. Allerberger, A. Murer, et al. "Whole Genome Sequencing Based Surveillance of L. monocytogenes for Early Detection and Investigations of Listeriosis Outbreaks." Frontiers in Public Health 7 (2019).
38. Thomas, J., N. Govender, K.M. McCarthy, et al. "Outbreak of Listeriosis in South Africa Associated with Processed Meat." The New England Journal of Medicine 382 (2020): 632–643.
39. Hobbs, J.L., C. Lee, B. Thompson, et al. "Two Listeria monocytogenes Outbreaks in a Cancer Centre: Onsite Food Premises and Their Potential Health Risk to Patients." BMC Public Health 23 (2023): 1443.
40. USDA-FSIS. "Listeria monocytogenes Illness Outbreak Associated with Ready-to-Eat, Country-Cured Ham, 2017–2018." After-Action Review Report 2018-16. May 13, 2020. https://www.fsis.usda.gov/sites/default/files/media_file/2020-11/Listeria%20monocytogenes%20Illness%20Outbreak%20Associated%20with%20Ready-to-Eat%2C%20Country-Cured%20Ham%2C%202017%E2%80%932018.pdf.
41. USDA-FSIS. "Listeria monocytogenes Outbreak Linked to Pork Patty Products Outbreak Investigation." After-Action Review Report 2019-02. https://www.fsis.usda.gov/sites/default/files/media_file/2021-11/Listeria-monocytogenes-Outbreak-Linked-to-Pork-Patty-Products-2019-02_0.pdf.
42. Halbedel, S., H. Wilking, A. Holzer, et al. "Large Nationwide Outbreak of Invasive Listeriosis Associated with Blood Sausage, Germany, 2018–2019. Emerging & Infectious Diseases 26 (2020): 1456–1464.
43. Fernández-Martínez, N.F., R. Ruiz-Montero, E. Briones, et al. "Listeriosis Outbreak Caused by Contaminated Stuffed Pork, Andalusia, Spain, July to October 2019." Eurosurveillance 27 (2022).
44. CDC. "2019 Outbreak of Listeria Infections Linked to Deli-Sliced Meats and Cheeses." September 26, 2019. https://archive.cdc.gov/#/details?url=https://www.cdc.gov/listeria/outbreaks/deliproducts-04-19/index.html.
45. CDC. "2020 Outbreak of Listeria Infections Linked to Deli Meats." January 28, 2021. https://archive.cdc.gov/#/details?url=https://www.cdc.gov/listeria/outbreaks/delimeat-10-20/index.html.
46. CDC. "2021 Outbreak of Listeria Infections Linked to Packaged Salad Mixes—Investigation updates." September 10, 2021. https://archive.cdc.gov/#/details?archive_url=https://archive.cdc.gov/www_cdc_gov/listeria/outbreaks/precooked-chicken-07-21/details.html.
47. CDC. "Listeria Outbreak Linked to Deli Meat and Cheese—November 2022." March 29, 2023. https://www.cdc.gov/listeria/outbreaks/deli-meat-and-cheese-11-22.html.
48. CDC. "Listeria Outbreak Linked to Meats Sliced at Delis." September 25, 2024. https://www.cdc.gov/listeria/outbreaks/delimeats-7-24.html?CDC_AAref_Val=https://www.cdc.gov/listeria/outbreaks/delimeats-7-24/index.html.
49. Farber, J.M., M. Zwietering, M. Wiedmann, et al. "Alternative Approaches to the Risk Management of Listeria monocytogenes in Low Risk Foods." Food Control 123 (2021): 107601.
50. Samelis, J., W. Bedale, and K. Glass. "Incidence, Behavior, and Control of Listeria monocytogenes in Meat Products." Listeria, Listeriosis, and Food Safety. 4th Ed. CRC Press.
51. USDA-FSIS. "Control of Listeria monocytogenes in Post-Lethality Exposed Ready-to-Eat Products." https://www.govinfo.gov/content/pkg/CFR-2016-title9-vol2/pdf/CFR-2016-title9-vol2-sec430-4.pdf.
52. USDA-FSIS. "Service Guideline: Controlling Listeria monocytogenes in Post-Lethality Exposed Ready-to-Eat Meat and Poultry Products." January 2014. https://www.fsis.usda.gov/guidelines/2014-0001.
53. Interagency Retail Listeria monocytogenes Risk Assessment Workgroup. "Interagency Risk Assessment: Listeria monocytogenes in Retail Delicatessens—Technical Report." September 2013. https://www.fda.gov/media/87042/download.
54. Datta, A. and L. Burall. "Current Trends in Foodborne Human Listeriosis." Food Safety 6 (2018): 1–6.
55. National Advisory Committee on Microbiological Criteria for Foods (NACMCF). "Parameters for Determining Inoculated Pack/Challenge Study Protocols." Journal of Food Protection 73 (2010): 140–202.
56. Health Canada. "Validation of Ready-to-Eat Foods for Changing the Classification of a Category 1 Into a Category 2A or 2B Food in Relation to Health Canada's Policy on Listeria monocytogenes in Ready-to-Eat Foods (2011)." November 29, 2012. https://www.canada.ca/content/dam/hc-sc/migration/hc-sc/fn-an/alt_formats/pdf/legislation/pol/listeria_monocytogenes-validation-eng.pdf.
57. New Zealand Ministry for Primary Industries. "Guidance for the Control of Listeria monocytogenes in Ready-to-Eat Foods Part 1: Listeria Management and Glossary." February 13, 2017. https://www.mpi.govt.nz/dmsdocument/16300-Guidance-for-the-Control-of-Listeria-monocytogenes-in-Ready-to-eat-Foods-Part-1-Listeria-Management-and-Glossary.
58. Devlieghere, F., A.H. Geeraerd, K.J. Versyck, et al. "Growth of Listeria monocytogenes in Modified Atmosphere Packed Cooked Meat Products: A Predictive Model." Food Microbiology 18 (2001): 53–66.
59. Blom, H., E. Nerbrink, R. Dainty, et al. "Addition of 2.5% Lactate and 0.25% Acetate Controls Growth of Listeria monocytogenes in Vacuum-Packed, Sensory-Acceptable Servelat Sausage and Cooked Ham Stored at 4 Degrees C." International Journal of Food Microbiology 38 (1997): 71–76.
60. Barmpalia, I.M., K.P. Koutsoumanis, I. Geornaras, et al. "Effect of Antimicrobials as Ingredients of Pork Bologna for Listeria monocytogenes Control During Storage at 4 or 10 Degrees C." Food Microbiology 22 (2005): 205–211.
61. Glass, K.A., D.A. Granberg, A.L. Smith, et al. "Inhibition of Listeria monocytogenes by Sodium Diacetate and Sodium Lactate on Wieners and Cooked Bratwurst." Journal of Food Protection 65 (2002): 116–123.
62. Glass, K., L.M. McDonnell, C. Sawyer, and J. Claus. "Minimum Nitrite Levels Required to Control Listeria monocytogenes on Ready-to-Eat Poultry Products Manufactured with Lactate and Diacetate." July 31, 2008. https://meatpoultryfoundation.org/namif/wp-content/uploads/05-226.pdf.
63. Chibeu, A., L. Agius, A. Gao, et al. "Efficacy of Bacteriophage LISTEX^TM P100 Combined with Chemical Antimicrobials in Reducing Listeria monocytogenes in Cooked Turkey and Roast Beef." International Journal of Food Microbiology 167 (2013): 208–214.
64. Glass, K., D. Preston, and J. Veesenmeyer. "Inhibition of Listeria monocytogenes in Turkey and Pork-Beef Bologna by Combinations of Sorbate, Benzoate, and Propionate." Journal of Food Protection 70 (2007): 214–217.
65. Glass, K.A., L.M. McDonnell, R.C. Rassel, and K.L. Zierke. "Controlling Listeria monocytogenes on Sliced Ham and Turkey Products Using Benzoate, Propionate, and Sorbate." Journal of Food Protection 70 (2007): 2306–2312.
66. Glass, K.A., L.M. McDonnell, R. VonTayson, B. Wanless, and M. Badvela. "Inhibition of Listeria monocytogenes by Propionic Acid-Based Ingredients in Cured Deli-Style Turkey." Journal of Food Protection 76 (2013): 2074–2078.
67. USDA-FSIS. "Safe and Suitable Ingredients Used in the Production of Meat, Poultry, and Egg Products, Revision 59." August 7, 2024. https://www.fsis.usda.gov/policy/fsis-directives/7120.1.
68. Nunes, K. "Clean Label Goes Mainstream." Food Business News. February 27, 2015. http://www.foodbusinessnews.net/Opinion/Keith-Nunes/Clean-label-goes-mainstream.aspx.
69. Labs, W. "Antimicrobials for Clean Labels." Food Engineering. October 16, 2017. https://www.foodengineeringmag.com/articles/97005-antimicrobials-for-clean-labels.
70. Beach, C. "Lawmakers Want to Know Why USDA, Boar's Head Did Not Take Action to Avoid Listeria Outbreak." Food Safety News. September 30, 2024. https://www.foodsafetynews.com/2024/09/lawmakers-want-to-know-why-usda-boars-head-did-not-take-action-to-avoid-listeria-outbreak/.
71. Pradhan, A.K., R. Ivanek, Y.T. Grohn, et al. "Quantitative Risk Assessment for Listeria monocytogenes in Selected Categories of Deli Meats: Impact of Lactate and Diacetate on Listeriosis Cases and Deaths." Journal of Food Protection 72 (2009): 978–989.
72. Bodie, A.R., C.A. O'Bryan, E.G. Olson, and S.C. Ricke. "Natural Antimicrobials for Listeria monocytogenes in Ready-to-Eat Meats: Current Challenges and Future Prospects." Microorganisms 11 (2023): 1301.
73. McDonnell, L.M., K.A. Glass, and J.J. Sindelar. "Identifying Ingredients that Delay Outgrowth of Listeria monocytogenes in Natural, Organic, and Clean-Label Ready-to-Eat Meat and Poultry Products." Journal of Food Protection 76 (2013): 1366–1376.
74. Golden, M., B. Wanless, A. Anagnostou, and P. Buckley. "Inhibition of Listeria monocytogenes in Cured Deli-Style Turkey Formulated with Commercial Blends of Propionate, Diacetate, Lactate, and Acetate-Based Antimicrobials." Journal of Food Protection 78 (2015): 267.
75. Brul, S. and P. Coote. "Preservative Agents in Foods—Mode of Action and Microbial Resistance Mechanisms." International Journal of Food Microbiology 50 (1999): 1–17.
76. Theron, M.M. and J.F.R. Lues. "Organic Acids and Meat Preservation: A Review." Food Reviews International 23 (2007): 141–158.
77. Samelis, J., G.K. Bedie, J.N. Sofos, K.E. Belk, J.A. Scanga, G.C. Smith. "Combinations of Nisin with Organic Acids or Salts to Control Listeria monocytogenes on Sliced Pork Bologna Stored at 4 Degrees C in Vacuum Packages." LWT Food Science and Technology 38 (2005): 21–28.
78. Santiesteban-López, N.A., J.A. Gómez-Salazar, E.M. Santos, et al. "Natural Antimicrobials: A Clean Label Strategy to Improve the Shelf Life and Safety of Reformulated Meat Products." Foods 11 (2022).
79. Leistner, L. and L.G.M. Gorris. "Food Preservation by Hurdle Technology." Trends in Food Science and Technology 6 (1995): 41–46.
80. Duffy, L.L., P.B. Vanderlinde, and F.H. Grau. "Growth of Listeria monocytogenes on Vacuum-Packed Cooked Meats: Effects of pH, A_w, Nitrite and Ascorbate." International Journal of Food Microbiology 23 (1994): 377–390.
81. Golden, M.C., L.M. McDonnell, V. Sheehan, J.J. Sindelar, and K.A. Glass. "Inhibition of Listeria monocytogenes in Deli-Style Turkey Breast Formulated with Cultured Celery Powder and/or Cultured Sugar-Vinegar Blend During Storage at 4 Degrees C." Journal of Food Protection 77 (2014): 1787–1793.
82. Seman, D.L., A.C. Borger, J.D. Meyer, P.A. Hall, and A.L. Milkowski. "Modeling the Growth of Listeria monocytogenes in Cured Ready-to-Eat Processed Meat Products by Manipulation of Sodium Chloride, Sodium Diacetate, Potassium Lactate, and Product Moisture Content." Journal of Food Protection 65 (2002): 651–658.
83. Seman, D.L., S.C. Quickert, A.C Borger, and J.D. Meyer. "Inhibition of Listeria monocytogenes Growth in Cured Ready-to-Eat Meat Products by Use of Sodium Benzoate and Sodium Diacetate." Journal of Food Protection 71 (2008): 1386–1392.
84. Horsch, A.M., J.G. Sebranek, J.S. Dickson, et al. "The Effect of pH and Nitrite Concentration on the Antimicrobial Impact of Celery Juice Concentrate Compared with Conventional Sodium Nitrite on Listeria monocytogenes." Meat Science 96 (2014): 400–407.
85. USDA-FSIS. "FSIS Compliance Guideline Procedures for New Technology Notifications and Protocols." April 2015. https://www.fsis.usda.gov/guidelines/2015-0012.
86. Weyker, R.E., K.A. Glass, A.L. Milkowski, D. Seman, and J.J. Sindelar. "Controlling Listeria monocytogenes and Leuconostoc mesenteroides in Uncured Deli-Style Turkey Breast Using a Clean Label Antimicrobial." Journal of Food Science 81 (2016): M672–M683.
87. USDA-FSIS. "BrucePac Recalls Ready-to-Eat Meat and Poultry Products Due to Possible Listeria Contamination." Current as of October 9, 2024. https://www.fsis.usda.gov/recalls-alerts/brucepac-recalls-ready-eat-meat-and-poultry-products-due-possible-listeria.
88. USDA-FSIS. "Distribution List for Recall 028-2024: BrucePac Recalls Ready-to-Eat Meat and Poultry Products Due to possible Listeria Contamination." Updated on October 29, 2024. https://www.fsis.usda.gov/sites/default/files/food_label_pdf/2024-10/Recall-028-2024-Labels.pdf.

Kathleen Glass, Ph.D. is Associate Director and Distinguished Scientist for the Food Research Institute (FRI) at the University of Wisconsin–Madison. In this capacity, she works with the food industry and regulatory agencies to evaluate microbial food safety risks, and design and conduct microbial food challenge studies to identify critical control limits for production.

Wendy Bedale, Ph.D. is a scientist serving as the Science Writer for the Food Research Institute at the University of Wisconsin–Madison. She researches literature to answer food safety questions for the food industry and writes reviews on a wide variety of food-related topics.

Daniel Unruh, Ph.D. is an Assistant Professor in the Department of Animal Science at Iowa State University. His research focuses on reduction and elimination of pathogenic and spoilage microorganisms in ready-to-eat and fresh meats. Previously, Dr. Unruh worked in the food ingredient industry, overseeing projects evaluating the efficacy of antimicrobials in various food systems.