Preharvest Food Safety

Food safety remains a global public health and agricultural priority. Since 1998, major funding programs and national initiatives have been developed and implemented within the United States and elsewhere. The emphasis of these programs has often been variable depending on the emerging new pathogen or outbreak, the changes in technology and method development, or funding mechanisms. Even terminology has been debated, i.e., farm-to-fork or plate-to-table, preharvest to postharvest. What remains constant is that accomplishments can be cited, yet the solutions for food safety issues remain elusive and changing. The reasons remain multifactorial, both from a scientific and from a strategic perspective. Scientifically, food safety is a complex issue that involves multiple and diverse food production practices, wide food distribution patterns, various and distinct consumers with assorted behaviors, and evolving foodborne pathogens and contaminants. Foodborne illnesses and outbreaks can be caused by not only microbial pathogens, but also by viruses, parasites, chemical agents, and toxins. Foodborne pathogens do not recognize specific barriers as humans, animals, and environments interact and as more food products are distributed globally. In addition to international travel, there has been an increase in world trade, and the United States continues to increase the importation of food products. In 2009, imports of various products such as grains and grain products, fruits and vegetables, nuts, and fish and shellfish were 17%, or 358 pounds, per capita (http://ers.usda.gov/topics/international-markets-trade/us-agricultural-trade/import-share-of-consumption.aspx). Importation can increase the access to new and familiar foods year-round but also can increase the possibility of introductions of additional food contaminants and pathogens.

Foodborne illness associated with fresh fruits and vegetables and growing and harvesting practices that impact the microbial safety of produce have been under the scrutiny of federal and state regulators for over 40 years. In 1998 the Food and Drug Administration published the Guide to Minimize Microbial Food Safety Hazards for Fruits and Vegetables (GMMFSH) in response to the U.S. President’s Food Safety Initiative, which launched, among other programs, the “Fight Bac” campaign. This GMMFSH guideline was created based on outbreak investigations that identified fresh produce as “an area of concern” ( 1 ) and summarized the then-current body of research and understanding of the risk factors associated with agricultural practices and how they could impact contamination of fresh produce with human pathogens. At the time, the GMMFSH guidelines did not address practices for risk elimination, supply chain, or environmental contaminants; however, they clearly identified the foundation for future research and new federal policies (the Food Safety Modernization Act [FSMA] and the Produce Safety Rule signed into law in 2011, which are currently impacting the farm to fork continuum). Twenty years after the development of these guidelines it is evident that previously identified sources of contamination linked to agronomic practices continue to be implicated in many of the more than 140 produce-related outbreaks investigated by federal and state agencies ( 2 ).

In addition to the need for food to be nutritious, abundant, and available, the term “food security” implies the requirement for food to be safe from health hazards and, at the same time, meet people’s food preferences. It is important that considerations about the safety of food begin prior to harvest because some potential food safety hazards introduced at the farm (e.g., chemical residues) cannot be mitigated by subsequent postharvest food processing steps. Also, some people have preferences for consuming food that has not been through postharvest processing (e.g., raw or lightly cooked foods) even though those foods may be unsafe because of microbiological hazards originating from the farm.

The goal of preharvest broiler food safety is to minimize opportunities for the introduction, persistence, and transmission of foodborne pathogens (mostly Salmonella and Campylobacter) in the bird flock. Current intervention strategies to combat foodborne pathogens in preharvest broiler production target Salmonella and Campylobacter in general, or more specifically target certain serotypes that are most frequently associated with human disease.

Eggs are one of the basic components of our food system. Their easy availability and being an inexpensive source of proteins make them attractive to consumers. The average annual consumption of eggs is around 250 eggs per capita in the United States, and according to statistical data, in 2013 the average per unit consumption was 252.6 eggs per person ( 1 ). Shell eggs can either be sold directly to consumers or be further processed and added as an ingredient in other food products. Due to the markets where eggs are sold, be it directly to consumers, as an ingredient in other food products, or as a processed product such as dried egg powder, liquid egg, etc., it is appropriate to decontaminate eggs to prevent foodborne illnesses. In most egg recipes half-cooked eggs are used, thus allowing certain pathogenic bacteria such as Salmonella, Campylobacter, and Clostridium perfringens to survive the low-temperature cooking. As a result, emphasis should be put on the decontamination techniques prior to packaging shell eggs.

Almonds, walnuts, and cashews are the major tree nuts produced in the world. The United States is the largest producer of tree nuts ( 1 ). Peanuts, also known as groundnuts, are produced largely in China, followed by India ( 1 ). Almonds are the major nuts produced by the United States, followed by peanuts, walnuts, and pistachios in this order ( 1 ). According to the 2014–2015 Global Statistical Review and world nut and dried fruit map, the world’s tree nut production increased by 5.4% compared to the previous season ( 1 ). By definition, nuts can be divided into several categories, including drupes (e g., almonds, coconuts, pecans, pistachios, walnuts), legumes (e.g., peanuts), nuts (e.g., acorns, chestnuts, hazelnuts), and seeds (e.g., brazil nuts, cashews, pumpkin, pine nuts, sesame, sunflower) ( 2 ). Nuts are consumed as a whole or as an ingredient in confectionary, bakery, and snack products. Nuts can be consumed raw or can be processed by thermal treatments such as oil roasting, dry roasting, blanching, and others.

In the United States, the most popular fish and seafood products consumed per capita in 2015 were shrimp (4.00 lb), salmon (2.88 lb), tuna (2.20 lb), tilapia (1.38 lb), pollack (0.97 lb), pangasius (0.74 lb), cod (0.60 lb), crab (0.56 lb), catfish (0.52 lb), and clams (0.35 lb) ( 1 ). Fresh fish and seafood are highly perishable, and microbiological spoilage is one of the important factors that limit shelf life and safety. Fresh seafood can be contaminated at any point from rearing or harvesting to processing to transport or due to cross-contamination by consumer mishandling at home.

Undoubtedly, water is one of the world’s most precious commodities, and since the beginning of agriculture, irrigating crops and relocating water to hydrate livestock have been essential to sustain society. The first irrigation system is believed to have been a bucket ( 1 ) carried back and forth from a river to irrigate plants. Today, the world’s most important use of water is for agriculture, more specifically for the production of crops and raising of livestock. In the United States 330 million acres of land are used for the production of food and other agricultural products ( 2 ). In 2010 alone over 126 billion gallons of water were used for irrigation, livestock, and aquaculture production, accounting for a total of 37% of total water use in the United States ( 3 ). Agriculture accounts for approximately 33% of total water use in Europe, and water use is more intensive in the southern parts of Europe, where 80% of total water consumption is for irrigation of crops ( 4 ). According to the Organization for Economic Cooperation and Development, there will be a 55% increase in the demand for water by the year 2050 due to increases in manufacturing, thermal power, and domestic industries that will put water availability for agriculture at risk ( 5 ).

Biological soil amendments (BSAs), including manure, compost, and compost teas (CTs), play an important role in conventional and organic agriculture. The use of these amendments can provide nutrients to soils, improving soil fertility and crop production. However, recent outbreaks of bacterial, viral, and parasitic infections associated with produce commodities over the past decade have focused more attention on agricultural inputs used to grow fresh fruits and vegetables. In response to these outbreaks, proposed rules from the U.S. Food and Drug Administration (FDA) have been issued, titled “Standards for the Growing, Harvesting, Packing and Holding of Produce for Human Consumption” Supplemental to the Proposed Rule ( 1 ). As part of these standards, the FDA has proposed specific rules and guidelines for how several BSAs can be applied to soils and fields intended to grow produce for human consumption.

Preharvest measures to reduce zoonotic pathogens in food animals are critical components in farm-to-table food safety approaches, which recognize that food production and safety occurs along a continuum. The encompassing goal of an integrated food safety program is to improve public health by reducing the risk of human foodborne illness, while the more specific goal of preharvest food safety strategies is to reduce the pathogen load of animals and/or animal products (such as milk or eggs) that are brought to harvest, in order to enhance the efficacy of postharvest interventions and reduce pathogens in the final product. As an example, the presence of pathogens in cattle feces and on cattle hides has been associated with beef carcass contamination ( 1 – 4 ). Cattle with high levels of Salmonella on their hides on entry into commercial processing were often coincident with preevisceration carcasses that were contaminated with the pathogen ( 4 ). Correspondingly, studies conducted in commercial beef processing plants have demonstrated that reducing Escherichia coli O157:H7 prevalence on cattle hides reduces its prevalence on resultant carcasses ( 5 – 7 ). As another example, the risk of broiler carcass contamination is greater when there is a higher degree of Campylobacter intestinal colonization of birds entering slaughter ( 8 – 10 ).

An emerging pathogen such as a virus can be defined as a previously unknown agent causing disease or an agent that was once an infrequent cause of illness that has become more common. It can also be defined as an infectious agent introduced into a new geographic area or one that infects a new species ( 1 ). Emergence of a viral pathogen is essentially a two-step process which requires conditions suitable for host introduction and then subsequent conditions that provide the opportunity to disseminate within a new host population ( 2 ). This is evidenced by the fact that emerging viruses and pathogens often arise in specific geographic locations ( 2 ). Numerous factors can be involved in the emergence of viral pathogens. These can include human demographic changes and behavior, travel and commerce, microbial adaptation, development of new technologies and industries, environmental perturbations, and breakdown of public health measures ( 2 ). The latter may be responsible for the re-emergence of poliovirus in parts of sub-Saharan Africa, where vaccine campaigns were suspended as a result of unfounded fears or active warfare. Historically, as human civilization developed as a result of agricultural activities, it is thought that environmental changes and increased human and domestic animal population sizes and densities permitted the introduction and spread of pathogens from wildlife reservoirs ( 3 ). Retrospective evidence suggests that viruses such as measles may have evolved from canine distemper (i.e., dogs) and/or rinderpest virus, a disease of cattle and wild even-toed ungulates such as deer, antelope, and wildebeest. It has been suggested that the variola virus, more commonly known as the smallpox virus, evolved from cowpox or, alternatively, may have evolved from camelpox, a virus of camels which is the closest known relative to the smallpox virus ( 3 ).

Common parasitic protozoal infections are frequently transmitted by food containing fecally contaminated soil or water, which may carry the environmentally resistant oocyst stage of the parasites Cyclospora cayetanensis, Cryptosporidium spp., Giardia spp., Toxoplasma gondii, or Sarcocystis spp. However, both T. gondii and Sarcocystis can also be transmitted by consumption of a cyst stage of the parasite which is present in the meat of infected animals; currently, the extent of Toxoplasma and Sarcocystis infection due to foodborne transmission is unknown ( 1 – 5 ). Differences in the definitive and intermediate hosts exist between these pathogens which impact their abundance and geographical distribution in the environment ( Table 1 ). As an example, because Giardia and Cryptosporidium spp. oocysts are excreted in large numbers by cattle, other ruminants, and a wide variety of other species (more than 109 per day), oocysts are very commonly found in the environment, while oocysts of Toxoplasma, which are exclusively excreted by felids, are restricted to areas inhabited by wild and domestic cats ( 6 , 7 ).

Researchers have stated that pathogens can contaminate food at any point along the food chain—at the farm, processing plant, transportation vehicle, retail store, or foodservice operation and the home. By understanding where potential problems exist, it is possible to develop strategies to reduce risks of contamination ( 1 ).

Providing food for the 9.5 billion people of the world by 2050 is one of the world’s greatest challenges. The change in population from 2010 to 2015 was +1.18%, with the continuing persistence of nearly 800 million chronically undernourished people ( 1 ). To meet these challenges, scientists are addressing various aspects of agriculture, including how environmental factors affect this task. Perhaps no two words have brought about more angst, frustration, and passion than “climate change,” including being a focus of political satire. It is difficult to show persuasive change over billions of years given that our technological advances have occurred most recently over the past half-century or so; however, we see change even in this relatively short period. Like many areas of science, facts associated with climate change may be formatted to persuade the intended audience. The scientific basis of climate change is complex historical data involving analysis of a myriad of sciences including physics, chemistry, and biology. Undoubtedly, there is great interest in climate change, with an increase in publications in the area of climate change relative to the life sciences and disease by 42% and 21%, respectively, from 2012 to 2013; in 2013 alone, 21 papers were cited related to climate change and food safety (MEDLINE trend performed 16 October 2016). The controversial nature of climate change may be due in part to the fact that people experience climate change so differently across the globe ( Fig. 1 ).

Meta-analysis refers to the statistical combination (pooling) of data from multiple original research studies. The results from different studies on the same topic can vary, and meta-analysis provides a means of summarizing a parameter or effect across studies to develop a more precise estimate of the outcome of interest ( 1 ). The combination of data from multiple studies can be undertaken using two broad approaches: combining individual-level data from multiple studies or combining study-level results (effect sizes) from multiple studies ( 1 ). The former requires the meta-analyst to have access to all of the original data from each study subject for each study and is therefore not commonly seen in the preharvest food safety literature ( 2 ), although databases of microbial growth and inactivation kinetics for foodborne pathogens are available and growing ( 3 ). Therefore, this chapter will focus on meta-analysis in the context of combining effect sizes from multiple studies to calculate a summary effect size.

One of the major challenges to current global food production and food security is the presence of antibiotic-resistant bacteria in animals (ruminants, poultry, swine) from which foods of animal origin are produced. Foodborne diseases significantly impact public health globally, with the World Health Organization (WHO) estimating that 1 in 10 people, or approximately 600 million people worldwide, are sickened and 420,000 die annually from foodborne illnesses ( 1 ). There is concern that many foodborne bacterial pathogens are either resistant or increasing their resistance to antimicrobials commonly used for medical treatment. For example, the Centers for Disease Control and Prevention reported that in 2013, the percentage of human Campylobacter jejuni isolates with macrolide resistance increased from 1.8% in 2012 to 2.2% in 2013, and from 9.0% in 2012 to 17.6% among Campylobacter coli isolates ( 2 ). In addition, the percentage of human Salmonella ser. I 4,[5],12:i:- isolates with resistance to ampicillin, streptomycin, sulfonamide, and tetracycline continued to increase, from 17% in 2010 to 45.5% in 2013 ( 2 ). Campylobacter spp. (845,024 cases per year) and nontyphoidal Salmonella spp. (1,027,561 cases per year) are the two most prevalent causes of foodborne illness in the United States, accounting for 51% of annual foodborne illnesses due to known bacterial agents ( 3 ) and highlighting the fact that an increasing number of foodborne illnesses are becoming more difficult to treat with antibiotics.

The microbial safety of agricultural products starts at the preharvest/preslaughter level of primary production, and this stage may be considered as one of the most crucial steps in enhancing safety along the entire farm-to-table continuum. In the United States, the safety of the food supply encompasses a variety of potential chemical, biological, microbiological, radiological, and immunological hazards that are managed by three federal agencies (U.S. Food and Drug Administration [FDA], U.S. Department of Agriculture Food Safety and Inspection Service [USDA-FSIS], and U.S. Environmental Protection Agency [EPA]) and various state agricultural, public health, and environmental protection agencies. This article will focus on hazards associated with bacteriological agents associated with fresh produce as an example of the evolving regulations for managing food safety risks. As such, the primary focus will be changes in regulations enforced by the FDA.

Free movement of safe and wholesome food is an essential aspect of the internal market within the European Union. This contributes significantly to the health and well-being of citizens and to their social and economic interests. A high level of protection of human life and health should be assured in the pursuit of community policies while allowing for flexibility when appropriate ( 1 ). These lines describe the overall policy in the European Union. The policy is practiced through different parts of the European Union regulatory framework, which is described below.

Elie Metchnikoff, who is “regarded as the grandfather of modern probiotics” ( 1 ) mentioned in his book The Prolongation of Life, published in 1907, that a researcher at the Pasteur Institute, Dr. Belonowsky, had shown that administration of the “Bulgarian bacillus cures a special intestinal disease known as mouse typhus” ( 2 ). Although likely impossible to prove, this passage in a book might have been one of the first to describe experimental probiotic action against an intestinal pathogen. Whatever one might think today about Metchnikoff’s ideas and his preoccupation with “putrefaction” in the digestive tract, he provided what could still be considered the basis of the modern definition of a probiotic when he wrote with reference to lactic bacilli, “The latter become acclimatized in the human digestive tube as they find there the sugary material required for their subsistence, and by producing disinfecting bodies benefit the organism which supports them” ( 2 ). With the term “disinfecting bodies,” Metchnikoff was referring primarily to lactic acid, but he was also aware, based on Belonowsky’s research, that more than lactic acid was involved in the probiotic action of the “Bulgarian bacillus.” Nowadays, most authors have settled on a broad definition of probiotics as “live microorganisms that, when administered in adequate amounts, confer a health benefit to the host” ( 3 ); however, with respect to food safety, this definition might not be broad enough. Certainly, a food animal host that is healthier as a consequence of probiotic administration would be less likely to be a food safety concern, but would live microorganisms that reduce a human pathogen such as Campylobacter jejuni in the chicken’s intestinal tract without any noticeable health benefits to the host not also be a probiotic? Similarly, a product that would reduce the Escherichia coli 0157:H7 carrier state in cattle would also fall into that category.

There has been a marked shift in consumer preferences about food choices. Today, consumers not only demand safe, inexpensive, tasty, and healthy food but also expect animal welfare and environmental safety. Consumers have become more curious about the source of meat—whether it comes from a conventional or an antibiotic-free farm (ABF) and if biosecurity requirements were met. To ensure the supply of safe meat to consumers, preventive measures need to be taken at the farm when animals are alive. This is where the concept of preharvest food safety comes from. Preharvest food safety is the combination of measures and interventions adopted at the farm to detect harmful pathogens and to reduce pathogen load in the food chain. Preharvest food safety is not only about the food animals and the microbes they carry but also includes the surrounding environment and human activities. The farm is a dynamic environment where pathogens, food animals, human interventions, environmental factors, and other animal species interact closely.

Preharvest food safety is a complex system because pathogen transmission and dissemination within a farm environment are determined by multiple interrelated factors, including ecological, evolutionary, environmental, and management drivers that act on different scales of time, space, and organizational complexity. The nonlinear dynamics of pathogen transmission and the complexity of the systems involved pose challenges in understanding key determinants of preharvest food safety and in identifying critical points and designing effective mitigation strategies. Mathematical modeling provides tools to explicitly represent the variability, interconnectedness, and complexity of such systems ( 1 ). In biology, mathematical models have contributed to numerous insights and theoretical advances, as well as to changes in public policy, health practice, and management ( 2 ). Mathematical biology has, indeed, become one of the most prominent interdisciplinary areas of research, but the use of mathematical models in preharvest food safety is recent ( 3 ). Results from modeling research in preharvest food safety have been published mostly since the 2000s. Most of these publications describe the development of epidemiological models to represent foodborne pathogen transmission in animal farming, following the longstanding tradition of applying mathematical modeling in epidemiology ( 4 , 5 ).

The term “One Health” describes a discipline, a theory, and a way of thinking that bring together human, animal, and environmental health. A majority of infectious diseases critical to food safety in humans are zoonoses. In fact, the Centers for Disease Control and Prevention (CDC) states that scientists estimate that more than 6 out of every 10 known infectious diseases in people are spread from animals and that 3 out of every 4 new or emerging infectious diseases in people are spread from animals (https://www.cdc.gov/onehealth/index.html). Through the broad One Health concept, scientists can probe solutions and develop a better understanding of how to address the growing problems concerning human medicine, animal medicine, and environmental sciences. Educational advances in One Health are occurring quickly through many undergraduate, graduate, and professional programs across agricultural sciences and veterinary medicine, as well as in public and human health. Traditionally, human health has been managed separately from animal health, and the health of the environment has been considered less than the latter. This is even more true in the recent past given the increase in specializations in human medicine, such as personalized medicine. Large government agencies and numerous private programs and companies work to protect human and animal health; therefore, clinicians, veterinarians, and environmentalists must all join together to fully address One Health.