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:
- Reducing the amount of pathogens entering processing plants will reduce the pathogen burden entering such plants, rendering in-plant interventions more effective
- Reducing horizontal pathogen spread from infected animals during transport and lairage
- Reducing the pathogen burden in the environment (e.g., dust and pen surfaces) and wastewaters that potentially contaminate crops (e.g., leafy greens)
- 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:
- Animal management and transport practices
- Feed and water management
- 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.
Live Animal Interventions
Research into understanding how feeds and management practices affect animal production and the resident microbial populations of food animals has opened our eyes to many novel approaches that can be used in live animals to specifically target foodborne pathogenic bacteria. Plants contain many phytochemicals that can alter the microbial population of the gut, such as tannins, phenolics, and essential oils, which can be included in the diets of food animals. For example, brown seaweed has been shown to improve the fermentation efficiency characteristics and reduce the fecal shedding of STEC. Other studies in ruminants have found that citrus products, which contain essential oils such as limonene, can reduce both Salmonella and STEC shedding, but do not impact the shedding of Campylobacter in model ruminants. Organic acids (e.g., lactate, acetate, butyrate) have been widely shown to have antimicrobial activity against foodborne pathogens and have been used widely in post-harvest pathogen reduction strategies. These acids can be included in rations and are produced by the native (or introduced) gastrointestinal microbial fermentation.
Probiotic preparations are designed to harness the power of the microbial ecosystem of the gut to exclude pathogens and prevent colonization, and are one of the most exciting avenues to reduce foodborne pathogens in food animals. While probiotics have long been used to improve growth efficiency of food animals and to modulate immune responses, recent advances in understanding the microbial ecology of the gut (e.g., next-generation sequencing, or NGS) have dramatically expanded our knowledge about how specific microbes (or end products) alter microbial populations. Probiotics are a very broad category, and in animals the category of "direct-fed microbials" includes several specific product types: eubiotics (traditional live culture probiotics, which can encompass competitive exclusion cultures), postbiotics (fermentation end products and non-living cells), and prebiotics (nutrients that are not used by the host animal but can be utilized by the microbial population as "colonic food"). Increasingly, support for the use of probiotic-type approaches has been growing in the industry as more of these products are examined utilizing a metric of foodborne pathogen populations.
The microbial population of the gut engages in brutal chemical warfare to defeat competitors, not only producing acids like VFA, but also producing antimicrobial substances. Colicins and bacteriocins are antimicrobial proteins that kill or inhibit STEC or other foodborne pathogenic bacteria. Until recently, these proteins were too expensive for use; however, producing these proteins in new hosts (e.g., yeasts or plants) has led to production of these proteins in sufficient quantities for use in food animals. This is an exciting development that offers opportunities for the use of this novel, targeted antimicrobial peptide to improve food safety.
The closest product to a "silver bullet" to reduce foodborne pathogens is the use of sodium chlorate. Pathogens such as Salmonella and STEC can respire under anaerobic conditions by reducing nitrate to nitrite using the enzyme nitrate reductase. The intracellular enzyme nitrate reductase does not differentiate between nitrate and its analog, chlorate, which produces chlorite in the cytoplasm; chlorite accumulation kills bacteria. Chlorate treatment quickly reduces populations of both E. coli O157:H7 and Salmonella in swine, cattle, and sheep intestinal tracts. To date, the U.S. Food and Drug Administration (FDA) has not approved chlorate for use in food animals.
The immune system is a powerful pathogen reduction mechanism, and vaccination is widely used in the food animal industry to utilize this anti-pathogen reservoir to prevent diseases that impact animal health and production efficiency. If the power of the immune system could be focused and applied to address foodborne pathogenic bacterial populations, then pathogen populations could be reduced. Immunization has worked against pathogenic bacteria that cause diseases in food animals, such as E. coli strains that cause edema disease in swine and Salmonella in poultry. However, because foodborne pathogens do not often cause illness in food animals, challenges to eliciting immune responses to these foodborne pathogens have been significant. Therefore, novel vaccines have been developed that specifically target foodborne pathogenic bacteria, with some exciting results in reducing pathogens (especially Salmonella) in cattle and swine.
Pre-harvest interventions that reduce foodborne pathogenic bacteria in food animals hold the potential to reduce foodborne pathogen dissemination on farms, in the environment, and from entering the food chain (in meat, milk, water, and other crops). Yet, development of successful pre-harvest strategies does not eliminate the need for good sanitation and procedures in the processing plant and in the food preparation environment. The animal production industry is quite varied, with each species passing through several production phases (e.g., cow-calf, finishing, feeder slab), each of which has different goals and economic realities, incentives, and drivers that must be met.
Each producer is focused on economic sustainability, but is also committed to wholesome and safe animal-derived protein production, and pre-harvest food safety techniques could be implemented during each phase of animal-derived food production. Live animal interventions must be implemented along the production chain in a complementary fashion to reduce pathogens in a multiple-hurdle approach that complements the in-plant interventions that currently exist, as well as the future improvements that are anticipated. Combining the use of pathogen reduction interventions from the farm and in the plant means that food products leaving the processing facility will have a significant reduction in hazardous foodborne pathogens entering the post-harvest retail and commercial supply chain.
References
- 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.
Todd R. Callaway, Ph.D., is an Associate Professor in the Department of Animal and Dairy Science at the University of Georgia. He is a ruminant microbiologist who grew up on a small horse, dairy, and beef farm and received his B.S. and M.S. degrees from the University of Georgia and his Ph.D. in Microbiology from Cornell University. Dr. Callaway previously worked for USDA's Agricultural Research Service and served as a research microbiologist in the Food and Feed Safety Research Unit at the Southern Plains Agricultural Research Center in College Station, Texas. In his research, Dr. Callaway focuses on the intestinal microbiome and the impacts of diet on the microbial population and host susceptibility to pathogen colonization. He has published more than 200 refereed journal articles, more than 25 book chapters, and two books.
Alexander Stelzleni, Ph.D., is a Professor and Graduate Coordinator in the Department of Animal and Dairy Science at the University of Georgia. Dr. Stelzleni received his B.S. degree from Missouri State University and his M.S. from the University of Arkansas in Animal Science. While at the University of Arkansas, he also worked for Tyson Foods in quality assurance and food safety. He completed his Ph.D. in Animal Science–Meat Sciences in 2006 from the University of Florida. Dr. Stelzleni's areas of research interest focus on pre-and post-harvest methodologies that impact factors considered traits of value to the red meat industry and red meat animal producers.
Jeferson M. Lourenco, Ph.D., is an Assistant Professor in the Department of Animal and Dairy Science at the University of Georgia. He started his career managing commercial dairy and beef-producing farms in Brazil and accumulated almost a decade of experience in that role. After moving to the U.S., he pursued his M.S. degree and Ph.D. at the University of Georgia. He also holds a B.S. degree from the State University of Maringá and a D.V.M. from Unicesumar, both in Brazil. Dr. Lourenco has been working with microbiology applied to animal sciences, bioinformatics, and biostatistics utilizing several animal species (particularly cattle, chicken, and swine). His research relies heavily on metagenomic approaches. He is also interested in the biologically relevant metabolites (e.g., short-chain fatty acids) produced by microorganisms, which may have a significant impact on animal health and productivity.
