Animal welfare and food safety in modern animal production

Animal welfare and food safety in modern animal production

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Lucas J. Lara1 and Marcos H. Rostagno2 1 Federal University of Lavras, Lavras, Brazil, 2Purdue University, West Lafayette, IN, United States

5.1

Introduction

The animal production industry has been going through a period of significant change as pressure mounts to keep pace with a constantly increasing demand for animal protein (meat, poultry, milk, and eggs) led by global population and socioeconomic developments. However, simply increasing production is not enough, as consumers are increasingly concerned about how their food is produced, as well as where it comes from and how safe it is. As a consequence, animal welfare and food safety standards have become increasingly relevant, and are often perceived as indicators of quality and astutely used for driving marketing strategies. Stress is intrinsically part of the general concept of animal welfare, and inevitably, all farm animals will experience some level of stress during their lives. This situation is a very common challenge for any animal production system as the occurrence of stress reduces the fitness of the animals by affecting their overall balance or homeostasis, through deregulation of the neuroendocrine immune system axis. The consequences of stress can vary widely, from simple failure to achieve production performance targets (Mitlohner et al., 2001; Collier et al., 2006; Estevez, 2007; White et al., 2008) to variable degrees of incidence of subclinical and clinical infections and diseases (Rauw et al., 1998; St-Pierre et al., 2003; Vecerek et al., 2006; Duff and Galyean, 2007; Ritter et al., 2007; Fitzgerald et al., 2009; Lara and Rostagno, 2013). However, although the link between stress in farm animals and food safety is generally accepted, our understanding of how this interaction actually occurs is very limited. Farm animals infected/colonized by foodborne pathogens, such as Salmonella enterica, Campylobacter jejuni, and Escherichia coli O157:H7, provide a source from which these bacteria may contaminate their final products (poultry, pork, beef, eggs, and milk). In fact, many studies conducted around the world have shown that a highly variable, but most of the time significant, proportion of farm animals carry foodborne pathogens within their gastrointestinal tract (Rostagno et al., 2003; Wesley et al., 2005; Woerner et al., 2006; Arsenault et al., 2007c; Fox et al., 2008; Young et al., 2009; Cernicchiaro et al., 2013; Mughini-Gras et al., 2014; Flockhart et al., 2016). Moreover, it has been estimated that live pigs carrying Salmonella are 3 4 times more likely to produce contaminated carcasses (Berends et al., 1996), while positive correlations have been found between fecal and hide prevalence of Advances in Agricultural Animal Welfare. DOI: http://dx.doi.org/10.1016/B978-0-08-101215-4.00005-5 Copyright © 2018 Elsevier Ltd. All rights reserved.

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E. coli O157:H7 in beef cattle (Woerner et al., 2006; Fox et al., 2008), and between cecal prevalence of Salmonella and Campylobacter, and carcass contamination, in chickens and turkeys (Arsenault et al., 2007a,b; Reich et al., 2008). In this review, we compile and present the current knowledge available in the scientific literature examining what is known about the relationship between stress in farm animals and microbial food safety risk. It is important to highlight that although potential issues resulting from changes in animal welfare and food safety regulations and standards are not within the scope of this review, they do have the potential to impact each other, positively or negatively. As consumers’ perspectives are constantly changing due to a multitude of influential factors, it is critical to realize that regulatory bodies and large corporations in the food industry are heavily influenced and respond to consumer pressures, creating an extremely challenging and fluid environment for the entire animal production industry, as well as for the scientific community.

5.2

Stress in farm animals and effects on the gastrointestinal tract

It is difficult to define “stress.” However, the classical and widely used definition is: “the nonspecific response of the body to any demand” (Selye, 1976). More specifically, stress represents the biological reaction of the animal’s body to stimuli that disturb its normal physiological homeostasis. The hypothalamic pituitary adrenal axis and the autonomic nervous system are responsible for the stress response via synthesis and release of hormones, neurotransmitters, and neuropeptides, with the purpose of reestablishing homeostasis by regulating physiological processes. This restoration of homeostasis follows a predetermined time course and is stressor specific (Minton, 1994; Mostl and Palme, 2002; Carrasco and Van de Kar, 2003; Mormede et al., 2007; Marketon and Glaser, 2008; Mora et al., 2012). Farm animals are challenged by different types of stressors throughout their lives, independent of the environment they are raised in or the management practices they are subjected to. However, the stress response is highly variable between individual animals even within the same population, as the stress response is modulated by several factors intrinsic to the animal (e.g., genetics, species, sex, age, physiological state, past experiences, and learning), as well as by stressor characteristics (e.g., nature, timing, avoidability, frequency, severity, and duration). Furthermore, it is important to understand that farm animals within the same population will be exposed to stressors at variable times and intensities, leading to a broad spectrum of stress responses (Greenberg et al., 2002; Lafferty and Holt, 2003; Creel et al., 2013; McEwen, 2015; Romero et al., 2015). Some of the common factors that produce stress in farm animals within any animal production system include inadequate nutrition, deprivation of water and/or feed, extreme environmental temperatures (i.e., heat and cold), overcrowding, and handling (i.e., manipulation by humans). Additionally, most farm animals are transported at some

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point in their lives for a variety of reasons (e.g., availability of feed ingredients, different raising locations, and processing or harvest). The process of handling, loading, transporting, and unloading of animals generates substantial detrimental effects on their well-being by causing stress. Also during this process, animals may be exposed to a range of challenging stimuli, including handling and increased human contact, vibration, movement, and jolting during transport, as well as novel and unfamiliar environments, periods of food and water deprivation, changes in social structure, and changes in climatic conditions. These challenges perturb the homeostasis of the animals, and activate an adaptive response in an attempt to restore balance (Warriss, 2003; Rostagno, 2009). The gastrointestinal tract contains a complex nervous system with millions of neurons embedded along and within the intestinal wall. These neurons control the tract’s microcirculation, motility, and exocrine and endocrine secretions. This enteric nervous system is bidirectionally connected to the central nervous system by the sympathetic and the parasympathetic pathways composing the brain gut axis (Hao et al., 2016; Uesaka et al., 2016). Research conducted over the course of many years has shown that stress, and the associated release of catecholamines, leads to decreased gastric acid production (with increased pH in the stomach), delayed gastric emptying, and accelerated intestinal motility and colonic transit (Moon et al., 1979; Enck et al., 1989; Tache et al., 1999; Monnikes et al., 2001; Tache and Perdue, 2004; Bonaz and Bernstein, 2013). These effects lead to an increased probability that foodborne pathogens will survive gastric passage and colonize the intestinal tract. Moreover, some neuroendocrine mediators released during a stress response also exert effects on the intestinal mucosa, altering the interaction between luminal microorganisms and epithelial cells through increased intestinal permeability, mucus production, and intestinal wall motility (Lenz et al., 1988; Williams et al., 1988; Barone et al., 1990; Saunders et al., 2002; Wang and Wu, 2005; Collins and Bercik, 2009; Lyte et al., 2011). The gastrointestinal tract also contains the majority of the cells comprising the animal’s immune system (70% 80%, depending on the species), as diffused and aggregated lymphoid tissues along the intestinal wall, particularly in the small intestine (McDonald et al., 2011). It is well known that extensive crosscommunication occurs between the neuroendocrine and immune systems, via common ligands and receptors. A number of hormones, neurotransmitters, and neuropeptides are known to affect several aspects of immune development and function. Similarly, receptors for immune mediators, such as cytokines, chemokines, and growth factors are known to occur on neuronal cells and in endocrine tissues. Therefore, it is evident that an intimate multidirectional communication network exists between the nervous and immune systems along the entire gastrointestinal tract (Steinman, 2004; Marques-Deak et al., 2005; Ziemssen and Kern, 2007). As a consequence, any imbalance to any of these systems (such as a stressor) will lead to significant changes in the immune response, leading in turn to increased susceptibility to infections. In fact, it has been shown that stress mediators, such as glucocorticoid hormones and catecholamines, can markedly affect

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immune function (Marketon and Glaser, 2008; Taub, 2008; Kelley and McCusker, 2014). As a consequence, the close connection and interaction (from the anatomical and functional points of view) of these two complex systems has for a very long time been the basis of the generally accepted explanation as to how stress influences the susceptibility of farm animals to infection and colonization by foodborne pathogens.

5.3

Effect of stress mediators on bacteria in the gastrointestinal tract

The gastrointestinal tract contains a very dense and metabolically active microbiota. Bacterial populations can reach 1012 1014 cells per gram of intestinal contents, comprising several hundreds of species (Zhu and Joerger, 2003; Rastall, 2004; Richards et al., 2005; Wang and Kasper, 2014; Hyland and Cryan, 2016). During a stress response, catecholamines are released by the enteric nervous system and/or spill over from the systemic circulation, creating significant local concentration increases (Aneman et al., 1996; Eisenhofer et al., 1997; Freestone et al., 2008). These changes in catecholamine concentrations affect the status and behavior of the intestinal microbiota and colonizing pathogens, as previously discussed, through suppression of the immune system and physiological alterations in the gastrointestinal tract. However, a new area of knowledge has emerged and demonstrated that the enteric nervous system can exert direct effects on intestinal microbial populations, including foodborne pathogens (Lyte et al., 2011). Early studies demonstrated the direct effect of catecholamines on bacterial growth (Lyte and Ernst, 1992, 1993; Lyte et al., 1996). Also, virulence factors, such as adhesins in enterotoxigenic E. coli and toxins in enterohemorrhagic E. coli, were shown to increase in the presence of norepinephrine (Lyte et al., 1996, 1997). The observation of direct effects of catecholamines on bacteria provided evidence of a new pathway for host stress-induced alteration of infections, and provided a theoretical framework for the emerging scientific field of microbial endocrinology, defined as a new multidisciplinary area of knowledge representing the intersection between microbiology and neurophysiology (Lyte, 1993, 2004). Research in this area is rapidly growing and generating a better understanding of how bacteria actively respond to neurohormonal products of the stress response within the host. For instance, studies conducted by Aneman et al. (1996) and Alverdy et al. (2000) indicated that enteropathogens increase the expression of virulence factors in response to environmental signals indicating host stress. In fact, Cogan et al. (2007) and Dowd (2007) showed that C. jejuni and E. coli O157:H7 increase the expression of virulence factors when exposed to norepinephrine in vitro. Moreover, Chen et al. (2003, 2006) have shown that catecholamines modulate E. coli O157:H7 adherence to the cecal epithelium, and Dunn et al. (2003) reported that translocation of Salmonella typhimurium from the intestinal tract was associated with activation of the hypothalamic pituitary adrenal axis, as well as

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noradrenergic and indoleaminergic responses. According to Karavolos et al. (2008) and Spencer et al. (2010), norepinephrine and epinephrine modulate Salmonella defenses against oxidative stress. More recently, Halang et al. (2015) showed that exposure to catecholamines enhanced growth and motility of Vibrio cholerae. According to Bearson (2016), a similar effect on the motility of E. coli and S. typhimurium occurs in the presence of catecholamines, with increased flagellar gene expression. Furthermore, epinephrine and norepinephrine are chemoattractants for E. coli O157:H7, and in S. typhimurium, norepinephrine enhances horizontal gene transfer and expression of genes involved in plasmid transfer (Bearson, 2016), which would pose a whole new facet of implications to be explored in the area of antimicrobial resistance dissemination (i.e., resistance genes exchange), not only in pathogenic, but also in nonpathogenic or commensal bacteria. Unfortunately, our current knowledge is very limited on this potential public health risk, as well as how much animal production might contribute via food safety and/or environmental contamination risks. As scientific interest and investment continue to increase, we should expect a clearer understanding of this issue in the coming years. An interesting study by Toscano et al. (2007) examined the effects of in vitro pretreatment of S. typhimurium with norepinephrine prior to infecting young pigs. Examination of the tissue distribution revealed that norepinephrine-treated bacteria were present in greater numbers and more widely distributed in gastrointestinal tissues than control bacteria. In another study, McCuddin et al. (2008) used three strains of S. enterica (serovars Saintpaul, Montevideo, and Enteritidis) and concurrent administration of a stress mediator (norepinephrine) to successfully reproduce Salmonella encephalopathy in cattle, which did not occur under normal conditions. These studies serve to demonstrate through two different approaches and in two different animal species how stress mediators (in particular, norepinephrine) are capable of affecting the dynamic host pathogen relationship, in favor of pathogens. It has become evident in recent years that the network of complex interactions between pathogens and their hosts is vital in determining the outcome of infections, with stress and its mediators playing an important role. Bacterial pathogens employ molecular sensors to detect and facilitate adaptation to changes in their niche, within the host. Moreover, intercellular bacterial communication is facilitated by the production, release, and detection of signaling molecules (called autoinducers) via a system known as quorum sensing. This communication system enables bacteria to alter their behavior in response to changes in population density and composition, such as caused by the occurrence of a stress response and its mediators. This is a very complex area of study, which is still in its infancy but which, over time, may greatly contribute to the development of potential interventions to mitigate some of the microbial effects and risks discussed here (e.g., increased colonization, virulence, and pathogenesis). Several interesting publications are available on this topic, including some comprehensive literature reviews (Kaper and Sperandio, 2005; Hernandez-Doria and Sperandio, 2013; Karavolos et al., 2013; Moreira et al., 2016; Luzader and Kendall, 2016; Papenfort and Bassler, 2016).

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5.4

Advances in Agricultural Animal Welfare

The impact of stress in farm animals on food safety risk

As previously discussed, a multitude of factors can lead to quantitative and/or qualitative disruptions of the complex gastrointestinal microbiota of farm animals, causing increased susceptibility to infection and colonization by foodborne pathogens. Some of these disruptive factors include antimicrobial compounds, feed additives, dietary changes, and a variety of stressors. As a consequence, levels of pathogens in the gastrointestinal tract as well as shedding from subclinically infected animals (i.e., carriers) may be affected by many circumstances. For instance, during the process of being transported from production farms to abattoirs, animals are exposed to a variety of potential stressors (Warriss, 2003; Averos et al., 2008). As a consequence, it is believed that the number of animals carrying and shedding foodborne pathogens increases in response to stressors. In pigs, studies have shown that transportation leads to increased shedding of Salmonella (Williams and Newell, 1970; Isaacson et al., 1999; Marg et al., 2001). However, the effect is not always straightforward, particularly because stressor intensity and the additive effects of multiple stressors seem to interact, creating a dynamic scenario (Rostagno et al., 2005; Scherer et al., 2008). Nevertheless, it is clear that stress generated by the process of moving pigs to the processing facilities does have the potential to increase the risk of foodborne pathogens. For instance, a recent study by Artuso-Ponte et al. (2015) demonstrated that the administration of a herbal extract supplement (quaternarybenzo(c)phenanthridine alkaloid) to finishing pigs was effective in reducing transportation stress, determined by significantly reduced salivary cortisol. Moreover, the intervention also resulted in reduced Salmonella shedding, thus positively impacting both animal welfare and pork safety. An additional interesting observation of the study consisted of a high positive correlation between salivary cortisol and Salmonella shedding after transportation in all groups of pigs studied. In broiler chickens, several studies have shown that transportation prior to processing at the abattoir leads to increased shedding of Salmonella (Mulder, 1995; Corry et al., 2002; Marin and Lainez, 2009). Interestingly, a study conducted by Barham et al. (2002) showed an increased prevalence of Salmonella in feces and on hides of cattle transported to the abattoir, whereas the same did not occur with E. coli O157:H7 in the same animals. Miniham et al. (2003) also did not detect any difference in E. coli O157:H7 in fecal samples of cattle transported to the abattoir. These studies suggest that transportation stress does not affect all pathogens equally, particularly in regard to fecal shedding. Additional studies in cattle have reported that Salmonella and E. coli O157:H7 frequency and levels increased on hides upon transport from feedlots to abattoirs, as well as when animals were subjected to preslaughter lairage (Reicks et al., 2007; Arthur et al., 2007; Dewell et al., 2008a,b). However, it is important to highlight that increased hide contamination does not directly imply increased infection frequency or shedding, although it suggests increased environmental contamination, leading to increased risk of carcass contamination with foodborne pathogens.

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Worth mentioning are the reported effects of weaning and movement/transportation of calves as a risk factor for E. coli O157:H7 and Salmonella infection and shedding (Corrier et al., 1990; Hancock et al., 1997; Bach et al., 2004; Fairbrother and Nadeau, 2006). The reported effect on E. coli O157:H7 in these studies contrasts with the previous studies conducted with market-age cattle, suggesting that an age-related effect or predisposition exists. In this case, exposure to stressors at an early age may predispose to increased colonization with E. coli O157:H7. This is a very interesting area of investigation with many potential ramifications and implications from the food safety point of view, and which warrants further study. Still related to the transportation of farm animals, in many cases feed is withdrawn before and during transportation to the abattoir to clear the gastrointestinal tract of fecal contents, thus reducing the risk of fecal contamination of carcasses. However, studies conducted in pigs have shown that periods of feed withdrawal lead to cecal fermentation changes, with increased pH and decreased concentrations of short chain fatty acids. These effects in turn lead to changes in the intestinal microbial ecosystem, resulting in increased numbers of Enterobacteriaceae and Salmonella in the feces of market pigs entering the abattoir (Nattress and Murray, 2000; Martin-Pelaez et al., 2008, 2009). In a study conducted by Harvey et al. (2001), increased levels of Campylobacter were also observed in pigs subjected to feed withdrawal. In broiler chickens, multiple studies have shown that the stressful harvesting practices of feed withdrawal and transportation cause significant increases of Campylobacter and Salmonella (Stern et al., 1995; Line et al., 1997; Ramirez et al., 1997; Byrd et al., 1998; Corrier et al., 1999; Whyte et al., 2001). Also, Barreiro et al. (2012) reported that feed withdrawal caused increased numbers of E. coli and Enterococcus in broilers. In a study conducted by Burkholder et al. (2008), feed withdrawal caused changes in the normal intestinal microbiota and epithelial structure in broilers, leading to increased attachment of Salmonella. In turkeys, Wesley et al. (2009) reported a significant increase of Campylobacter prevalence in market-age birds subjected to feed withdrawal and transportation, while Dutta et al. (2008) showed that Listeria monocytogenes colonizes liver and synovial tissues of cold-stressed turkeys, and may constitute a source of contamination during processing. Dietary stress (feed restriction or withdrawal) in cattle has also been shown to increase bacterial shedding, such as generic E. coli and E. coli O157 (Cray et al., 1998; Reid et al., 2002). Feed removal for an extended period of time was for many years a very commonly used method by the layer industry (egg production industry) to induce molting and stimulate multiple egg-laying cycles in aging hens (Golden et al., 2008). However, research has demonstrated that feed removal during forced molting decreases the resistance of hens to Salmonella enteritidis infection (Holt, 1993; Durant et al., 1999), resulting in increased severity of infection and shedding (Holt and Porter, 1992a; 1993). Increased horizontal spread of infection to molted hens in neighboring cages (Holt and Porter, 1992b, 1993; Holt, 1995), and finally, increased egg contamination (Holt, 2003; Humphrey, 2006; Golden et al., 2008; Denagamage et al., 2015) and consequent food safety risk to consumers. It is important to mention that feed removal to induce molting is generally no longer used in the

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North American and European egg production industries, and that the purpose of the information presented here was simply to further demonstrate the interrelation between the stress caused by feed removal and the occurrence of Salmonella in poultry. Environmental thermal stress, in particular heat stress, is another factor that can lead to colonization of farm animals by pathogens, increased fecal shedding and horizontal transmission, and consequently, increased contamination risk of animal products (Lara and Rostagno, 2013). These effects may occur through different pathways, from favoring the pathogen’s ecology and epidemiology to affecting the host’s ability to cope with the infection/colonization, as previously discussed in this review. Nevertheless, although a lot of knowledge is available on the effects of thermal stress on physiology and productivity (Slimen et al., 2016), very little has been published on the effects of heat stress on the intestinal microbial ecosystem of farm animals. In pigs, an association between the thermal environment (temperatures below or above thermal neutral zone) within a barn and Salmonella shedding has been reported (Pires et al., 2013). Several epidemiological studies have reported seasonal effects on the occurrence of Salmonella and Campylobacter in flocks of broilers and laying hens (Patrick et al., 2004; Wales et al., 2007; Van Der FelsKlerx et al., 2008; Jorgensen et al., 2011). In broilers, changes in intestinal microbial community structure were observed due to heat stress, which also lead to increased mucosal attachment of S. enteritidis (Burkholder et al., 2008). Heat stress in broilers has also been shown to increase intestinal inflammation and translocation of S. enteritidis, resulting in increased levels of the pathogen in the spleen (Quinteiro-Filho et al., 2010). Cold stress applied to chickens in the first 7 days of life was shown to increase activity of the hypothalamic pituitary adrenal axis and the sympathetic nervous system, leading to long-term immune cell dysfunction and increased Salmonella Heidelberg invasion and persistence (Borsoi et al., 2015). A seasonal effect, with higher E. coli O157:H7 prevalence in summer months and with warmer temperatures has also been reported in feedlot cattle (Renter et al., 2008). In dairy cattle, increased environmental temperature has been shown to increase shedding of shiga toxin-producing E. coli (Venegas-Vargas et al., 2016) and Salmonella (Likavec et al., 2016). Evaluation of the effects of environmental stressors on the host pathogen interaction is an area of increasing interest and importance, particularly for farm animals commonly raised outdoors, as well as due to the increasing trend toward alternative production systems that aim to improve animal welfare by offering confined animals access to the outdoors.

5.5

Conclusion and implications

Infection and colonization of farm animals by foodborne pathogens, and the subsequent dissemination of those pathogens along the food chain, constitute a major public health concern worldwide. Based on this scientific review, it is clear that stress in farm animals can significantly affect food safety risk through a variety of

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potential mechanisms and pathways. However, while there is evidence linking stress to pathogen carriage and shedding in farm animals, many gaps in knowledge still exist and further study is warranted, so that risk factors can be avoided/minimized and intervention strategies applied to reduce risk to consumers. Protecting animal welfare and health is critical for maximizing productivity and efficiency as well as for reducing food safety risk, and consequently maintaining public health and consumer confidence. However, this is no simple task as animal production systems are very complex and the industry faces very broad and intricate challenges. Worth noting is that although the world population is increasingly removed from farming and food production, consumers are increasingly concerned and want more transparency and information about where and how their food is produced, with ethical concerns becoming a driving factor in consumers’ choices. However, as consumers demand more from the food industry, complex challenges (and interests) arise, particularly when the media provides misinformation. This scenario causes a lot of confusion and often creates perceptions that may be mistaken. For instance, consumers often assume that improved animal welfare automatically means improved food safety. If looking only through the perspective offered by this literature review, the assumption could be perceived as being correct. However, due to the complexity of the subject, we chose to focus on just one aspect of animal welfare (i.e., the effects of stress as a risk factor), leaving out other aspects that could also affect food safety risk, such as the effects of housing and management changes on the eco-epidemiology of foodborne pathogens. An entire book would probably be needed to cover all the potential aspects of the relationship between animal welfare and food safety. But, to be fair we must note that given the inherent complexity of modern animal production systems, as well as of host pathogen interactions, there are situations in which animal welfare standards may be improved, but at the expense of increased food safety risk. As an example, we could mention the trend of offering farm animals access to the external/outdoor environment, which exposes them to different stressors, besides allowing the emergence of pathogens not occurring in modern confined production systems (e.g., parasites, due to direct contact with soil). On the other hand, practices aiming to improve animal health and food safety (or minimizing risks), such as restrictive confinement can have detrimental animal welfare effects. The purpose here is to show that a balanced approach is essential to accommodate different needs within complex production systems. Interestingly, to date, there is no conclusive scientific evidence indicating differences in the incidence of the most common foodborne pathogens (such as Salmonella, Campylobacter, or E. coli) in different animal production systems, even though a significant number of studies have been published. The observed frequent report of conflicting results is likely due to the large number of variables and confounders usually involved (Jacob et al., 2008; Kijlstra et al., 2009; Young et al., 2009; Loo et al., 2012). As previously mentioned, there is still a lot to study and understand as we evolve in this area. However, due to the inherent complexity of animal production systems, it is critical that decisions/changes are made based on science rather than on emotions or simplistic perceptions. Otherwise, there could be

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unintended consequences and compromises in advances made during several decades of study and investment. Globalization of food trade provides greater food access, but also presents further potential for complications, such as the impact created by trade agreements and restrictions influencing animal welfare and food safety standards, sometimes based on diverging purposes, such as competitive marketing, market access, and market protection. Furthermore, over the last few years, the influence of large food retailers and restaurant chains with global reach has been a key driving factor. Using consumers’ perceptions to target marketing strategies, these large corporations many times impose specific standards on producers and suppliers even when those standards are not demanded by regulations. These do not necessarily translate into improved animal welfare or food safety outcomes, and in some cases, may even compromise those outcomes through some of the pathways highlighted in this review.

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