Mitigating The Risk Of Salmonella In Food

Gary C. Smith, Colorado State University

Dorland’s Illustrated Medical Dictionary defines “Salmonella” as follows: “A genus of gram-negative, facultatively anaerobic bacteria of the family Enterobacteriaceae; the genus is separated into species (N=3) or serotypes (more than 1,500) on the basis of antigens (O, Vi, or H, where O is somatic, Vi is capsular, and H is flagellar). The genus contains pathogenic species causing enteric fevers, septicemias, and gastroenteritis; the most frequent clinical manifestation is food poisoning. 

Salmonella is Everywhere

Salmonella species are widely distributed in lower animals, frequently producing disease.”¹ From a food plant sanitation standpoint, Michael Cramer adds these details about Salmonella: “It is an intestinal bacterium often found in the fecal material of birds, livestock, pests, and pets, but – in truth – it is ubiquitous in the environment (especially in the soil). There are more than 2,200 serotypes, and all are known to cause disease in humans. 

Salmonella is an Adulterant at Any Level in RTE Food

The disease is called Salmonellosis, with symptoms including nausea, headache, abdominal pain, vomiting, and non-bloody diarrhea.”² CDC says, “Eating food contaminated with feces is the most common way that people become infected with Salmonella; it can be spread by people through cross-contamination and improper hand-hygiene.”^3,4 Matthew Taylor identifies Salmonella enterica (non-typhoidal) as the major culprit in food; it is considered “infectious” in raw foods at 1 CFU per gram and is categorized as an “adulterant” if present at any level in ready-to-eat (RTE) food.⁵

Salmonella spp. is the Deadliest Foodborne Illness

Characterization of “Foodborne Illnesses In The United States Per Year: CY 2011”, showed Salmonella spp. ranked second to Norovirus in “Estimated Number of Episodes” at 1,027,561, but first in “Deaths” at 378. It was third to Listeria monocytogenes and Toxoplasma gondii in “Case Fatality Rate” at 0.0368 (1 in 2,700), which is comparable to that of Escherichia coli 0157:H7 (0.0317; 1 in 3,150). So, it’s the second “most likely to make you sick,” first in “most likely to kill you,” and third “most likely to kill you once you get it,” among the most common foodborne pathogens.⁶

Foodborne Illnesses due to Salmonella Cost the U.S. Economy $3.7 Billion Annually

Economic Research Service (of USDA) determined the cost of 15 major pathogens in the U.S. that are collectively responsible for 95% of the foodborne illnesses and deaths for which CDC can identify a pathogen cause.⁷ Conclusions were that, each year, foodborne illnesses cost the economy more than $15.6 billion, cause 8.9 million cases, send 53,245 persons to hospitals, and take the lives of 2,377.⁷ Number 1 among those 15 pathogens is non-typhoidal Salmonella at a cost of $3.7 billion.⁷

Salmonella episodes have not decreased over time; it was estimated at 1.03 million in 2011,⁷ then 1.20 million⁴ to 1.35 million⁸ in 2022. Foodborne illness outbreaks increased from 8-16% from 2017 to 2019⁹, then 26% more in 2020.¹⁰ FY 2020 outbreaks by pathogen were 50% Salmonella; FY 2020 by product were 42% beef, 17% chicken, and 8% FDA-regulated foods.¹⁰

Some Recommend We “Attack Comprehensively” to Fight Salmonella in Food

To control Salmonella, we could act comprehensively or at delineated junctures in the supply-chains; whatever is the approach, those in production and processing sectors, regulators, and consumers will be better informed via whole genome sequencing.¹¹

Some have recommended that we Attack Comprehensively: 

 

1. Salmonella can be reduced through on-farm strategies, hygienic slaughter practices, and processing techniques.¹²

1. Sweden has virtually eliminated Salmonella in store-bought chicken by using microbiological testing at multiple key production points, inspection of clean-up protocols, banning shipments from producers that are not Salmonella-free, etc.¹³

1. Vaccination of broiler/layer flocks, stronger hygienic practices, vermin control, quarantine procedures, biosecurity measures, and comprehensive microbial testing programs for carcasses.¹⁴

1. Sweden, Finland, Norway, and Denmark – for poultry and swine – require strict, on-farm biosecurity measures, cleaning and disinfection of animal housing, extensive microbiological testing for Salmonellain animals and feed, culling of infected breeding animals, and separate handling of Salmonella-positive flocks or herds at slaughter.¹⁵

1. Food and Agriculture Organization of the United Nations and the World Health Organization concluded that there is no single control measure that allows for the prevention of Salmonella in poultry, but it likely will require multiple intervention steps to reach the greatest impact in the broiler production chain.¹⁶

1. Many experts on the subject agree that “Farm-to-fork” technological applications or interventions are needed to control Salmonella in meat and poultry production.^17,18,19,20

1. FDA’s “Key Recommendations” for control of Salmonella in fruits and vegetables are:

    

   1. Follow FSMA Produce Safety Rules; 
   1. Enact Good Agricultural Practices;
   1. Implement sanitation practices and sampling plans; Ensure science-based preventive measures; and 
   1. Employ pre-harvest and post-harvest microbiological testing of food, water, and the physical environment.²¹    

Others Recommend We “Focus On Preharvest Solutions”

In a “delineated juncture in the supply-chain” approach, some Focus On Preharvest Solutions: 

 

1. Fruits and vegetables can be contaminated by wildlife (e.g., feral hogs, deer, ducks, mice); manure used as fertilizer; wind-dust and water from nearby livestock; and H-2A field workers.^{22,23,24,25,26,27}Farm animals can be contaminated by wildlife (e.g., geese, starlings, deer, raccoons); manure used as fertilizer; feed containing feces; contaminated water; allowing animals to “free-range;” and “No Antibiotics Ever” chickens.^{22,23,28,29,30,31} Improving the conditions in which plants and animals live to mitigate the risk of contamination are best delineated by FDA’s “Key Recommendations”²¹, EFSA’s “Epidemiological Indicators,”³¹ and a Texas A&M University “Salmonella Prevalence” paper.³²

1. Preharvest intervention strategies such as Salmonella vaccines should be used in the egg-laying and broiler-producing industries.³³ Salmonella in pork products can be reduced through on-farm strategies.¹² Microbiological testing at multiple key production points – starting at the hatchery and ending after transportation to the processing plant – will lessen Salmonella presence in poultry products.¹³ Pathogens can enter and become disseminated at any point in the live production chain from when the egg is laid to when it’s hatched, during the growing period, and, due to stress, during transportation from the grower farm to the processing facility; prevalence of Salmonella at the processing plant can be greater than 90%.¹⁸ FSIS-USDA is in the midst of a comprehensive effort to reduce Salmonella in poultry products; a key component is encouraging preharvest controls to reduce Salmonella coming into the slaughterhouse.^34,35 Salmonella infections in broiler-breeder chicken flocks and breeder pig herds can be transmitted to chicks and piglets, underscoring the need for efficient control measures – like vaccines – earlier in the production chain.³⁶ The National Advisory Committee on Microbiological Criteria for Foods recommended improved poultry vaccines for pathogenic microorganisms.³⁷ Poultry operations could reduce risks to consumers by vaccinating broiler-breeder flocks against Salmonella, strong hygiene practices, quarantine procedures, and biosecurity protocols.¹⁴ The Pew Charitable Trust called for on-farm exposure-reduction strategies to tackle foodborne illnesses focused on use of probiotics and vaccines as on-farm interventions after finding that those interventions were most effective at reducing livestock exposure to Salmonella.³⁸ USDA scientists have proven efficacy for addition of sodium chlorate to the feed and water of livestock to kill SalmonellaTyphimurium.³⁸ At slaughterhouses in the United Kingdom and Australia, visual inspection of individual cattle’s “hide condition” (based on presence of soil and feces) may necessitate washing them prior to processing.³¹ Plants throughout the European Union require microbiological testing on-farm from cattle herds one month prior to slaughter.³¹ Four consumer groups have petitioned USDA to reduce or eliminate Salmonella on meat/poultry by “requiring slaughterhouses to adopt science-based tools to prevent animals from being infected by these bacteria on the farm, including by vaccinating live poultry and monitoring farms for the presence of dangerous bacteria.”¹⁷  

What Does it Mean to “Attack at the Harvest/Processing Level”?

In a “delineated juncture in the supply chain” approach, some Attack At The Harvest/Processing Level: 

 

1. Fruits and vegetables generally eaten raw (e.g., peaches, grapes, melons, leafy greens, onions) are usually given chlorine (or other disinfectant) washes, but because there is no “kill-step” in their harvesting/processing scheme, periodic microbiological testing is a “Key Recommendation” of FDA.²¹Shell eggs are routinely given warm-water washes that can include formaldehyde, hydrogen peroxide, peracetic acid, or ozone, or subjected to ultraviolet light (at 253.7 nm).¹⁹  

1. Microbiological testing of beef carcasses prior to dehiding, of lymph nodes at evisceration, and of carcasses pre-chilling and post-chilling is required in the European Union.³¹ Salmonella are found in the lymph nodes of cattle^32,39 and market hogs^40,41 at slaughter; some beef processors presently extract three to six of the major peripheral lymph nodes (popliteal, subiliac, superficial cervical, axillary, coxal, iliofemoral) from beef trimmings during fabrication.³² Processing has traditionally been viewed as the last line of defense for safeguarding consumers from foodborne disease but, in truth, growers should be sending animals to the processor with the lowest possible levels of Salmonella.³³ Once chickens are delivered, processing plants can leverage interventions like lactic acid sprays and chilling techniques to further reduce Salmonella growth and spread.²⁰ Intervention technologies for poultry carcasses include ozone (gas or aqueous solutions, often pressurized to penetrate feather follicles), cold atmospheric plasma, ultraviolet light, and advanced oxidation process.¹⁹ Pathogen control in pork slaughter facilities is effected by use of 185°F water under pressure; plus antimicrobial chemicals (lactic acid, acetic acid, peroxyacetic acid, acidified sodium chlorate) that are hand-applied or in spray cabinets; knife hygiene; and “sanitary dressing procedures.”⁴² A novel process, Refrigerated Instantaneous Temperature Cycling (RITC) eliminates microbiological risk in raw meat products.⁴³ Novel techniques such as use of bacteriophages and high pressure processing (HPP) are being explored as interventions against pathogens in pork.¹² Arresting the growth of microorganisms before they take hold on product can be achieved by using antimicrobials or inhibitors (acetates; diacetates; preservatives like benzoates, sorbates, vinegar, or lemon juice), via vacuum packaging or modified atmosphere packaging.⁴⁴ New data, published in Poultry Science, shows that faster slaughter line-speed for chickens does not increase the risk of Salmonella contamination.⁴⁵ One problem that neither FSIS-USDA nor processors has solved is “enteric fluid” (i.e., non-visible fecal material); it contaminates poultry carcasses post-defeathering and pork carcasses post de-hairing with pathogens.⁴⁶ It has reached the point that growers must incorporate preharvest interventions that will lower the bacterial pathogen load on the animals arriving at the packing plant; otherwise attack at the harvest level will not sufficiently mitigate the public health risk.⁴⁷

Can We Depend on Regulatory Oversight to Protect Against Salmonella?

In a “delineated juncture in the supply-chain” approach, some Depend On Regulatory Oversight. 

 

1. After more than a century of reacting to incidents/outbreaks of foodborne pathogenesis, FDA shifted its focus to preventing them; the U.S. Congress, reacting to the Peanut Corporation of America Salmonelladebacle, passed FSMA. FSMA requires that companies implement “Best Practices” to prevent hazards in manufacturing processes; but FDA does not have the authority to conduct microbial testing, on farms, of plants, animals, water, and the environment.^27,48  

1. Salmonella is introduced on farms/ranches and in feedlots/finishing-facilities, but FSIS has no authority over how flocks or herds are managed.²⁰ At the harvest level, FSIS has historically tried to regulate Salmonella contamination on meat and poultry carcasses using Pathogen Reduction Performance Standards (those have been modified several times and are used now as a categorization/public-notification system).^49,50 Between 1996 and 2022, E. coli O157:H7 and other STECs were declared “Adulterants” (thereby not regulated via Performance Standards), while FSIS tweaked the Performance Standards for Salmonella, issued Guidance documents regarding Salmonella, and contemplated making Salmonella an adulterant.^{13,17,20,34,35,49,51,52,53,54,55,56,57,58,59,60}

Which Salmonellae Should be Targeted in Food?

Chief among concerns about Salmonella Performance Standards and/or designation of Salmonella as an adulterant is, which Salmonellae? All >2,500 serotypes? At least with E. coli O157:H7 and the other STECs, we knew which bad actors to target; FSIS didn’t use generic E. coli for Performance Standards or call them adulterants – that would have resulted in almost everything being adulterated.⁶¹ Martin Wiedmann (Cornell University) said, “Today, all Salmonella serotypes are treated the same in FSIS regulations – if you’re above a certain percentage, you’re published in the ‘bad actor list’ (i.e., the categorization system of the 2008 Salmonella Initiative).”⁴⁹ He believes that FSIS should focus on serotypes that are more likely to cause human disease, for example, Salmonella Newport for beef, Salmonella Enteritidis for eggs, and SalmonellaHeidelberg for chickens.⁴⁹ 

FSIS Outbreak Data List serotypes of 2017, 2018, 2019 were⁹: 

 

• Blockley

• Enteritidis

• Newport

• Rissen

• Schwarzengrund

• Reading

• Typhimurium

• Infantis 

In the Marler-Clarke LLP petition asking FSIS to declare 31 serotypes as adulterants in meat and poultry, it called out Hadar, Heidelberg, Newport, Typhimurium, Dublin, Enteritidis, and Infantis.⁵⁵

Personal Responsibility Plays A Role in Salmonella Illnesses

While there are thousands of strains of Salmonella, only about a hundred make people sick, and most illnesses are individual events related to human error.²⁰ The courts have weighed in on the personal responsibility issue by holding an executive of a company accountable; the “Park Doctrine” was used to impose a 28-year prison sentence on the owner of Peanut Corporation of America™️.⁶² And an Arizona federal court jury attributed 30% of a fault to Foster Farms™️, and 70% to family members for their preparation of some chicken that caused brain injury to a 5-year-old child.⁶³  

Consumer Education Can Help Reduce Illnesses From Salmonella

So, in a “delineated juncture in the supply-chain” approach, some Pursue Consumer Education.  CDC, in 2015, issued “Tips For Avoiding Salmonella While Preparing Foods.”⁶⁴ CDC, in 2019, warned people, “You can get sick from Salmonella simply by touching poultry or the birds’ environment.”⁶⁵  

At retail, 1 of 5¹⁸ to 1 of 25²⁰ of packages of chicken are contaminated with Salmonella; USDA provides detailed suggestions of how not to spread dangerous bacteria around the kitchen, about hand-washing hygiene, and use of food thermometers.⁶⁶ Mindy Brashears (USDA) and Frank Yiannis (FDA) jointly developed educational programs on mishandling of foods and ways to avoid bacterial food poisoning.⁶⁷  

Many say that creation of more food regulations is not likely to achieve reductions in Salmonellosis and that FSIS should instead commit to substantial resources toward consumer education and teaching home cooks (through social media, internet marketing, TV ads, etc.) how to properly store, handle, and prepare poultry products.⁵⁷ Sandra Eskin (FSIS) said, “We are not sure people cook poultry thoroughly enough to kill pathogenic bacteria; since 1998, Salmonella outbreaks and ∼200 illnesses have been linked to breaded chicken products.²⁰  Too many people are ‘warming up’, rather than ‘fully baking’, not-ready-to-eat (NRTE) frozen, raw, breaded, and stuffed chicken products like Chicken Cordon Bleu and Chicken Kiev.”²⁰ CDC recently determined that “ingrained habits” (i.e., ignoring food safety cooking instructions on packages) and “socio-economic challenges” (i.e., not having access to a conventional oven and instead using microwaves, air fryers, or toasters) are disproportionately responsible for Salmonella incidents/outbreaks.⁶⁸    

Are Salmonella Performance Standards Effective?

So, what’s happening now? FSIS seems to have lost faith in Salmonella Performance Standards, and so have some in the processing sector. Just 2.5 years ago, FSIS announced, “We have implemented SalmonellaPerformance Standards for poultry and that has worked… Salmonella on poultry dropped from 24%, to 9%; so, Performance Standards have been proposed for Campylobacter on poultry and Salmonella on beef, and will soon be proposed for pork.”⁵⁶  

But now FSIS says, “We’re not moving the needle in regards to reducing Salmonella illnesses as measured by ‘Healthy People 2030’ goals.”³⁴ And, USDA continues to tighten its Performance Standards, and processors thus far have successfully responded; now though, producers must incorporate Preharvest Interventions to lessen the bacterial pathogen load. Otherwise, the Harvest Interventions won’t be sufficient for the processor to achieve the Performance Standard.⁴⁷  

FSIS Plans to Declare Salmonella an Adulterant in Certain NRTE Chicken Products

On August 1, 2022, FSIS announced plans to declare Salmonella an “adulterant” in NRTE breaded and stuffed raw chicken products; FSIS proposed a quantitative standard of 1 colony forming unit (CFU) of Salmonella per gram for these products.²⁰  

Sandra Eskin (FSIS) pointed out that the 1 CFU/gram was just a proposal and USDA will seek public comment via its publication (in October) in the Federal Register as to whether the standards should be more or less strict (e.g., zero tolerance or one based on specific serotypes).²⁰  

Mindy Brashears (formerly with FSIS) says, “Not all Salmonellae are the same; without three pieces of information (Genus: Salmonella; Serotype: Typhimurium; Pathogenicity: Highly Pathogenic) there are information gaps – and the decisions made may be misinformed.”⁶⁹ We now have capability to count Salmonella CFUs (Biomerieux™️ GENE-UP® QUANT SALMONELLA)^70,71 and identify Salmonellaserovars.⁷² Food Safety Net Services (FSNS) offers the BAX® System SalQuant™ method.           

In October 2022, FSIS proposed a regulatory framework to control Salmonella contamination in poultry products and reduce foodborne illnesses attributed to such products.⁷³ Discussion is underway regarding FSIS deciding to designate Salmonella as an adulterant in NRTE breaded and stuffed raw chicken products, and a Public Hearing is scheduled for November 3, 2022 to discuss the adulterant issue plus a three-component proposed framework.⁷⁴ Components of the framework are: 

 

• Requiring that incoming flocks be tested for Salmonella before entering a processing establishment. 

• Enhancing establishment process-control monitoring and FSIS verification. 

• Implementing an enforceable final product standard for Salmonella.^69,73,74  

FSIS announced on October 9, 2022 that “it is also completing a risk profile for pathogenic Salmonella subtypes in poultry and is collaborating on quantitative risk assessments for Salmonella in chicken and turkey that will address key risk management questions associated with this framework.⁷⁵  

At the November 3 Public Hearing: 

 

1. National Chicken Council supported “changes in food safety regulations that are based on science and data that will positively impact public health.”⁷⁶  

1. FSIS pledged to help small-scale processors – with funding, logistics, scientific advice, and personnel as they adapt to the proposed Salmonella rules and framework.⁷⁷ 

1. An industry food-safety consultant testified that, “We need to go upstream starting at incubation to enact Preharvest interventions, and we need to determine the pathogenicity of Salmonella serotypes to know which bad actors to target.⁶¹  

1. “Data gaps” were mentioned multiple times; data are needed on Salmonella quantification and pathogenicity to the impact of specific mitigation strategies and monitoring on actual public health metrics.⁷⁸

The Public Comment Period ended on November 16, 2022.  Since then, FSIS has adjusted/expanded its original proposal to declare Salmonella an adulterant in breaded stuffed raw chicken products in the following manner: If the raw chicken intended to be breaded and stuffed exceeds 1 CFU per gram of Salmonella, it cannot be used to make the breaded and stuffed end product. The chicken component represented by the sampled lot can be diverted to a use other than breaded stuffed raw chicken products.^79,80

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