Consumers expect and rightfully demand a plentiful supply of affordable, safe, and wholesome red meat. Concerns about the safety of meat have been important to the industry, the public, and the government since the implementation of the Pure Food and Drug Act of 1906. Unfortunately, despite the effort expended in controlling foodborne illnesses in the U.S., foodborne pathogens cost the GDP more than $17.6 billion each year in direct and indirect costs.¹

One of the most notable improvements to food safety is the implementation of Hazard Analysis and Critical Control Points (HACCP), which has been globally adopted as a method to systematically improve food safety. The implementation of other procedures, such as "test and hold" for ground beef prior to shipment to consumers, has significantly improved consumer safety. As a result of these systematic improvements in the food supply chain driven by industry and government actions, the U.S. food supply is safer than ever before.

While the number of foodborne bacterial illness cases and outbreaks impacting consumers has been reduced, too many foodborne illnesses still occur. Most foodborne pathogenic bacterial reduction processes have focused on reducing pathogen loads in processing plants. Processing plants do an excellent job of reducing pathogen levels on carcasses during the processing and retail phases of animal-derived food production, and many new interventions have been implemented in recent years on the post-harvest side of the continuum.

Fecal foodborne pathogen shedding by the live animal is correlated with levels of carcass contamination; therefore, if the pathogen burden entering the processing facility in and on food animals can be reduced, then pathogen reduction strategies in the plant can be more effective in controlling the pathogen load in finished products. Furthermore, foodborne pathogenic bacteria are not only transmitted to humans through animal-derived foods and can reach humans via drinking water, or on irrigated vegetables, and can be transmitted via dust or other vehicles. Recent years have also witnessed an increasing frequency of illnesses in schoolchildren who have visited petting zoos or open farms. Thus, developing strategies to reduce foodborne pathogens in live animals can have impacts in more than just the food chain.

Foodborne pathogenic bacteria [e.g., Salmonella, Campylobacter, Listeria, and Shiga toxin-producing Escherichia coli (STEC) O157:H7 and associated serotypes] are commonly found in the gut of food animals, as well as in on-farm production environments (e.g., manure, water, migratory birds, rodents). Many of these foodborne pathogenic bacteria do not cause detectable illnesses in food animals, and so are nearly invisible members of the gut microbial populations found in the on-farm production environment where animals are produced. For example, STEC is a cluster of pathogenic bacteria that cause bloody diarrhea in humans. These bacteria do not cause any illnesses in cattle, but they can cause profound kidney damage in humans, especially in children under seven years of age. While STEC-related illnesses have been often associated with consumption of undercooked ground beef or via contaminated produce, pathogen transmission to humans can occur through contaminated drinking or recreational water, contact with cattle, pen surface contamination, and through human-to-human contact. Due to the profound impacts on both children and adults, seven STEC strains were declared as adulterants in ground beef (but not in intact beef products). As a consequence of this declaration, the U.S. beef industry invested heavily in research on food safety improvements, which has resulted in a significant decrease in the number of human STEC illnesses.

Most foodborne pathogenic bacteria behave similarly to "typical" bacteria in the gut of food animals, which has led researchers to mine ecological concepts to develop strategies to reduce pathogen entry to the food chain at the processing plant and beyond. The logic behind investing resources in developing pre-harvest intervention strategies is demonstrated through the following:

1. Reducing the amount of pathogens entering processing plants will reduce the pathogen burden entering such plants, rendering in-plant interventions more effective
2. Reducing horizontal pathogen spread from infected animals during transport and lairage
3. Reducing the pathogen burden in the environment (e.g., dust and pen surfaces) and wastewaters that potentially contaminate crops (e.g., leafy greens)
4. Reducing the risk to those in direct contact with animals (e.g., petting zoos and open farms).

To control pathogens in the live animal, several potential reduction strategies have been developed for use on-farm in live animals. These approaches can be grouped loosely into broad categories:

1. Animal management and transport practices
2. Feed and water management
3. Live animal treatments.

While some of these pathogen reduction strategies are available today, many remain to be developed in the near future and are weapons to help secure the safety and integrity of the food supply from farm-to-fork.

Animal Management and Transport Practices

Good animal management is critical to the production of healthy and efficient food animals, and is often referred to as "Good Agricultural Practices" (GAP). No typical management procedures directly affect colonization or shedding of any foodborne pathogens; yet, impacts from bad animal care and management (e.g., stress, animal health, and water run-off) can impact pathogen shedding and recirculation/colonization of pathogens within a pen or herd. Good animal management techniques, production hygiene, stress-reducing handling practices, and overall good animal husbandry play an important role in food animal production and should be followed. For example, STEC and Salmonella excretion in cattle is highest in the late spring through late summer; this seasonality is reflected in the "summer peak" of illnesses in humans. Seasonality may require specific interventions to be utilized more during peak shedding season; however, at present, the seasonal use of interventions is not recommended.

Most foodborne pathogenic bacteria live a fecal-oral lifecycle, meaning proper sanitation of facilities and disposal of manure are important for interrupting pathogen transmission within facilities. Animal density may also play a role in the horizontal spread and recirculation of foodborne pathogenic bacteria within pens or herds. Densely packed animals have an increased chance of co-contamination via spread through fecal-oral pathways. Cattle manure is a good source of nutrients to fertilize crops, is often used after composting, and can also be sprayed onto (or injected as a slurry into) fields where crops and forages are grown, posing a potential risk to crops that are fertilized or irrigated with manure.

Manure can harbor foodborne pathogenic bacteria for long periods (in excess of 100 days, in some cases) in organic materials, serving as an important source of foodborne pathogen contamination that may be later spread by rainfall events or flushing alleyways with water. Manure-borne pathogens can enter surface or groundwater and can contaminate drinking water, wells, ponds, or irrigation water supplies. Retention ponds and catch basins are used to limit manure run-off in many animal production systems and allow producers to recycle waste as fertilizer for crops and forages, but the creation of this sustainability improvement may have inadvertently created a reservoir or source for foodborne pathogenic bacteria. Muddy pen conditions have been linked to increased pathogen populations compared to dry pen surfaces. Furthermore, the amount of solar radiation reaching the pen surface is correlated with foodborne pathogen populations due to the bactericidal effect of UV light.

On-farm biosecurity is a GAP that impacts animal health and welfare and can reduce the spread of transmissible animal diseases, including illnesses contracted from foodborne pathogenic bacteria. Typically, producers limit animal exchange between farms and use animal grouping systems to prevent disease transmission. The use of closed herds is a common biosecurity procedure and prevents the spread of pathogens between farms. Furthermore, limiting visitors and controlling rodents and other pests are a critical facet of biosecurity because many rodents and birds (including migratory birds) can serve as pathogen vectors between pens, between farms, and even across large distances.

Humans understand stress intuitively, yet we have limitations in our ability to understand what is stressful to food animals. Long-term stress may depress immune function in cattle, making them more susceptible to colonization with a variety of pathogens on farms, but the short-term effects of stress from weaning, handling, or transport on immune status are impactful and may play a large role in colonization with foodborne pathogens. It is clear that stresses of transport and mixing impact the gastrointestinal microbial population and foodborne pathogenic bacterial colonization of food animals. Handling and transport between farms, to sale barns, and to processing plants cause multiple simultaneous and sequential stresses, which can impact animal welfare, meat quality, and the microbial population and carriage of foodborne pathogenic bacteria, as well as increase pathogen spread due to physical contact or fecal contamination.

In cattle, trailer washing has been shown to have a limited impact on the transmission of foodborne pathogens, but it is a GAP. The length of transport time has been linked with increased risk of pathogen shedding. Many animals are exposed to common environmental stressors, heat stress, and cold stress, all of which can negatively affect animal health, productivity, and pathogen shedding. Interestingly, periods of extreme temperature have been linked in cattle to "high event periods" of STEC shedding and a large number of subsequent positive carcasses in the processing facility.

Managing food animals throughout their lifecycle is a complex issue that includes many elements outside of "animal production," such as environmental impacts, sustainability, profitability, animal welfare, and, increasingly, food safety. No one system of food animal production is "best," and management strategies vary geographically and with production goals. Coupling the best practices for biosecurity and animal production can reduce some of the horizontal spread and recirculation on and between individual farms, thereby reducing pathogen burden at the processing facility, which can allow other strategies that are utilized closer to the consumer to be more effective.

Cattle Water and Feed Management

Rations of food animals are typically controlled by humans and can profoundly impact the health and productivity of animals by altering the native gastrointestinal microbial population, including foodborne pathogen populations. Fasting animals, especially cattle, can lead to reduced gastrointestinal fermentation, which is correlated with the increased survival of many pathogenic bacteria that can be found in the gut. The area of diet composition is currently under investigation for its role in pathogen carriage in food animals. Feeding distillers grains to cattle has shown to increase shedding of STEC. Steam flaking of corn increases STEC shedding in cattle compared to cracked corn, suggesting that the availability of starch in the hindgut may play a role with this pathogen.

Furthermore, cattle that are fed a higher-quality forage tend to have lower STEC shedding than do grain-fed cattle, but lower-quality forage feeding increases STEC shedding. Collectively, data demonstrates that end products of feedstuff fermentation (e.g., volatile fatty acids or VFA), as well as some secondary compounds in forages, play important roles in foodborne pathogen populations and prevalence in the gut. This has prompted the use of other organic acids or VFA to alter the gastrointestinal microbial population and resultant fermentation and to reduce pathogen populations in the gut.

References

1. U.S. Department of Agriculture, Economic Research Service. "Cost Estimates of Foodborne Illnesses." March 4, 2022. https://www.ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses.aspx.