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Inherent digestive tract insufficiency in monogastric animals: culpability of the gut microbiome and dietary approaches for optimizing intestinal health

Published: August 26, 2021
By: Elijah G. Kiarie / Department of Animal Biosciences, University of Guelph, Guelph, ON.
Summary

Although pigs and poultry are highly efficient in converting feed to food products, they still excrete significant amounts of undigested nutrients. For example, broilers lose almost 25-30% of ingested dry matter, 20-25% of gross energy, 30-50% of nitrogen and 45-55% of phosphorus intake in the manure. Undigested nutrients have negative implications on production efficiency, profitability and sustainability of farm operations. Moreover, the undigested nutrients serve as substrates for enteric pathogens with implications to animal (e.g. E. coli, clostridia) health and human (e.g. salmonella, campylobacter) health via contained animal products. The peculiarity is that feedstuffs contain anti-nutritional factors (ANF) such as phytic acid or fractions that are not degraded sufficiently or indeed at all by the conditions and the array of digestive enzymes in the gastrointestinal tract. Moreover, the newly hatched chicks and weaned piglets have limited capacity to express endogenous enzymes. Arguably with restriction on use of preventive antibiotics, there is need to explore and implement alternative dietary approaches to enhance digestive function. Supplemental feed enzymes improve nutrient utilization linked to reduced nutrients excretion and enteric pathogen load. Moreover, nutritional strategies for stimulating juvenile gut maturation (e.g. epidermal growth factor, feed structure), nurturing favorable gut microflora (e.g. probiotics, prebiotic), suppressing enteric pathogens (e.g. organic acids, low crude protein diets) and maintaining intestinal integrity (e.g. yeast metabolites) should be integral in AGP free feeding programs. These dietary approaches in combination with improvements in management, vaccination programs and/or genetics will be effective in optimizing growth performance of poultry and pigs raised without or with reduced antibiotics for growth promotion.

Introduction
Advances in genetics has certainly produced commercial strains of poultry and pig with greater performance (e.g. growth, reproduction) with minimal feed input. For example, over the last 5 decades, the body weight of broilers at 42 days has increased by 25-50 g per year and the feed conversion ratio to 2 kg body weight has improved 2-3 points annually (Havenstein et al., 2003; Gous, 2010; Aviagen, 2019). With the introduction of crosses in the early 60's, specialization in dam and sire lines have been very successful in effecting genetic improvement of economically important traits in pigs, especially daily gain, backfat thickness, feed efficiency and litter size. An annual genetic progress for gain of +20 g/day, lean meat of +0.5% and litter size of +0.2 piglet/litter has been achieved over the last few decades (Krupa et al., 2017; Merks, 2018). The nutrition of these animals has also evolved overtime but not as much as genetic advances(Kiarie and Mills, 2019); for example genetic selection brought about by breeding companies is responsible for 85-90% of the improvements in broiler growth, and advances in nutritional management contributed only 10-15% (Havenstein et al., 2003). However, the necessity to achieve and sustain genetic potential has been the driving force behind continuous advances in nutrition concepts seen in modern day commercial pig and poultry enterprises. In this context, feeding, a major control point of profitability has evolved and progressed both in terms of understanding digestive physiology and metabolism, and in the more precise evaluation of the quality of dietary raw materials. Advances in monogastric nutrition is clearly exemplified by the widespread adoption of net energy, standardized ileal digestible amino acids ideal ratio and digestible phosphorous concepts enabling nutritionists to formulate cost-effective and optimal diets (NRC, 1994, 2012). However, the modern-day nutritionists perceive dysfunctional gastrointestinal tract as a potential ratelimiting factor in the survival and productivity of monogastric farm animals (Kiarie et al., 2019a).
This perception has been fostered by the emergence of ideas and concepts concerning the development and function of the digestive tract in the light of advances in genetic improvement and restriction on the use of antibiotic growth promoters and anti-coccidial drugs. The intention of this review is to provide insights in digestive tract insufficiency in monogastric farm animals, the implications of gut microbiome and dietary approaches for enhancing gut function and health without recourse to antimicrobial growth promoters. 
What is it about the digestive tract in monogastric farm animals?
Undoubtedly, pigs and poultry are highly efficient in converting feed to food products, but they still excrete significant amounts of undigested nutrients. For example, broilers lose almost 25-30% of ingested dry matter, 20-25% of gross energy, 30 -50% of nitrogen and 45-55% of phosphorus intake in the manure (Ravindran, 2012). Pigs of different breeds and ages were observed to digest 78% of gross energy in typical corn and soybean meal diet (Urriola and Stein, 2012). Addition of 30% corn dried distiller’s grains with solubles to this diet resulted in further reduction of digestible gross energy. 
I. Juvenile gut biology
Genetic selection for increased meat production efficiency has dramatically altered the physiological timeline of broiler chickens (Ferket, 2012). For example, between 2005 and 2010, duration to raise 2.5 kg broiler reduced by 0.74 days per year (Gous, 2010). The significance of decreasing time to slaughter weight is that embryonic and early post-hatch periods constitute a greater proportion of a bird’s life. For example, 21-day incubation period and the 10-day posthatch period of the chick accounts for about 50% of a 2.5 kg broiler; yet gut maturation does not happen until after 10 days post-hatch (Uni and Ferket, 2004). Thus, the capacity for the intestine to absorb and assimilate nutrients may pose a proximal constraint upon the rate of growth of newly hatched chicks. In pigs, the gastrointestinal tract (GIT) of the newly weaned pig is poorly developed having: (1) an immature immune system, (2) limited enzyme secretory capacity, (3) sensitive to allergenic feed proteins, and (4) unstable gut microbiota (Lindemann et al., 1986; Pluske, 2016).
II. Inherent digestive insufficiency 
Feedstuffs contains anti-nutritional factors (ANF) such as phytic acid or fractions that are not degraded sufficiently or indeed at all by the conditions and the array of digestive enzymes in the gastrointestinal tract (Kiarie et al., 2013; Kiarie et al., 2016; Kiarie and Mills, 2019). This inherent digestive inefficiency in monogastric animals is seen as the reason of commercial development and application of exogenous feed enzymes technology. Indigestible complexes can impede normal digestion and absorption processes of nutrients including carbohydrates and protein (Slominski, 2011). For complete monogastric diets, the digestibility of dry matter varies between 70 and 90% but the variation is larger for specific feed ingredients (10 to 100%). Most of the variation in dry matter digestibility is related to the presence of dietary fiber (DF) which is less digestible than other nutrients (<40% vs. 80-100% for starch, sugars, fat or protein) and reduces the digestibility of other dietary nutrients such as crude protein and fat (NRC, 1994, 2012). The consequences of variable and low nutrient digestibility range from economic through increased feed costs, proliferation of pathogens in the gut, poor feed efficiency to ecological through nutrient loading and emissions into the environment (Kiarie et al., 2013; Kiarie et al., 2016; Kiarie et al., 2019b). Moreover, undigested feed increases visceral weight, consequently increasing utilization of dietary energy and amino acids for maintenance at the expense of tissue deposition (growth) (Cant et al., 1996; Agyekum et al., 2012).
Culpability of gut microbiota in the context of digestive insufficiency 
The GIT host a diverse community of organisms with symbiotic relationship with the host. The balance in this ecosystem is of crucial importance in maintaining nutritional, physiological and immunological functions of the host. The diversity of bacterial populations within a micro-habitat in the GIT is influenced by factors such as digesta flow rate, pH, anoxic conditions, types of endogenous and dietary substrates, inhibitory factors such as bacteriocins and short chain fatty acids (SCFA), and competitive advantage (Kiarie et al., 2013). Bacteria in the gut derive most of their carbon, nitrogen and energy from luminal compounds (dietary and/or endogenous) which are either resistant to attack by digestive fluids or absorbed so slowly by the host that bacteria can successfully compete for them. Thus, undigested nutrients in the gut promotes blooming of bacteria in the ceca and in the environment via excretion. It is likely that certain nutrients and their associated physico-chemical effects play a major role in maintaining the balance of the microflora in specific micro-habitats, and subsequently in determining whether a pathogenic bacterium proliferates. For example, in poultry there is greater risk of an outbreak of necrotic enteritis (NE) with the use of viscous grains (barley, wheat and rye) (Timbermont et al., 2011). This has been associated with high digesta viscosity, decreased nutrient digestibility and prolonged intestinal transit time, thus favouring growth of Clostridium perfringens in the upper gut (Kaldhusdal and Skjerve, 1996; Timbermont et al., 2011). In swine, viscous fibres have also been linked to exacerbation of post-weaning collibacillosis and swine dysentery (SD) (Pluske et al., 2002). The detrimental effects of soluble fibres in swine have been associated with the increasing digesta viscosity, undigested nutrients in the GIT and endogenous secretions. Furthermore, an increased flow of ileal undigestible protein in the hindgut can result in proteolytic fermentation that can negatively affect performance and health. Arguably, the use of AGP in the past markedly reduced negative consequences of feeding such feedstuffs and as a result performance was maintained on diets that otherwise would be problematic. Indeed, earlier studies demonstrated that the growth depressing effect of feeding broiler chickens feedstuffs that depressed nutrient digestibility was ameliorated by sub-therapeutic antibiotic supplementation (Marquardt et al., 1979; Antoniou and Marquardt, 1982). Furthermore, (Smulders, 1999) showed that sub-therapeutic antibiotics were more effective in diets with low digestible protein content versus in diets with high digestible protein content.
Dietary concepts and approaches for maintaining functional gut without recourse to antimicrobial growth promoters
I. Stimulating functional gastrointestinal (GIT) development
There are numerous functional ingredients, factors and /or nutrients that are known to enhance GIT development and could be strategically applied in starter diets to enhance digestive capacity and resilience to enteric pathogens. For example, epidermal growth factors (Kim et al., 2017), yeast metabolites (Kiarie et al., 2010; Kiarie et al., 2011; Kiarie et al., 2012; Leung et al., 2019) and organic acids(Kiarie et al., 2018). Poultry requires a certain amount of diet structure for proper gut development and functionality. For example, data suggest course feed structure (created by grain particle size manipulation, inclusion of insoluble fiber or access to litter) may improve digestive function and development including increased secretion of acid and enzymes (Mateos et al., 2012). Diet structure plays an important role in stimulating gizzard development, controlling digesta passage rate and improving gut motility by enhancing endocrine cholecystokinin release which stimulates the secretion of pancreatic enzymes and gastroduodenal refluxes (Mateos et al., 2012). This was demonstrated by (Xu et al., 2015) who replaced (wt/wt) finely ground corn (294 μm, as per the industry standards) with 25% and 50% course ground corn (1,362 μm) to create three diets with mean particle sizes of 432, 541 and 640 μm. These diets were fed to broiler chickens to 50 days of age to conclude that birds fed diets containing 25 and 50% course corn exhibited increased BW, improved FCR, and increased apparent ileal digestibility of energy and crude protein, linked due to enhanced gizzard development. A longer retention time in the gizzard leads to more exposure of feed particles to gastric juices that improves digestion, thereby contributing to a better feed efficiency. 
II. Reducing undigested substrates by use of feed enzymes 
Beneficial effects of feed enzymes are inextricably linked to the amount of the undigested fat, protein and starch in the ileum. Accelerated intestinal digestion and removal of what would otherwise be apparently undigested without feed enzyme must clearly limit the nutrients available for the microbes (Kiarie et al., 2013; Munyaka et al., 2016). As illustrated in Table 1, almost all commercial feed enzymes address such ANF to varying degrees (Kiarie et al., 2016). Therefore, the utility of feed enzyme technology in monogastric nutrition is to degrade ANF in feedstuffs and to complement endogenous enzymes in gut compromised animals particularly hatchlings and weanlings. As alluded to microbiome profile and metabolic function is partly reflective of feed composition (Apajalahti et al., 2004, 2007). It is therefore plausible that manipulating diet digestibility will influence GIT microbiome (Kiarie et al., 2013).
Table 1. Commercial feed enzymes and target substrates
Table 1. Commercial feed enzymes and target substrates
Furthermore, fiber degrading enzymes could release hydrolysis products “prebiotic” that can modulate intestinal microbiota (Courtin et al., 2008; Kiarie et al., 2013; Wealleans et al., 2017; Bedford, 2018). Utility of feed enzymes in transitioning weaned pigs has also been demonstrated in studies that compared feed enzymes and antimicrobial growth promoters. For example, a supplemental multi-enzyme blend caused similar performance and digestibility of gross energy and crude protein to pigs fed an antibiotic in the early phase of weaning (Table 2) (Kiarie et al., 2015). Supplemental xylanase reduced grow-finishing pig mortality from 4.0 % to 2.4% and improved gain: feed from 0.286 to 0.290 (Figure 1) (Zier-Rush et al., 2016). The aforementioned studies and others in the literature (Bedford and Cowieson, 2012; Kiarie et al., 2013) suggests that feed enzymes could be a tool for not only improving feedstuffs digestibility but could also influence gut health, livability, uniformity and carcass value in pigs.
Table 2. Effects of feeding an antibiotic (PC) and a multi-enzyme (ME) blend on growth performance and coefficients of total tract apparent digestibility (CTTAD) in nursery pigs
Table 2. Effects of feeding an antibiotic (PC) and a multi-enzyme (ME) blend on growth performance and coefficients of total tract apparent digestibility (CTTAD) in nursery pigs
Figure 1. Effects of supplemental xylanase on mortality in grow-finishing pigs (Zier-Rush et al., 2016).
Figure 1. Effects of supplemental xylanase on mortality in grow-finishing pigs (Zier-Rush et al., 2016).
III. Low crude protein synthetic amino acids supplemented diets
In monogastric nutrition, protein (amino acids) is the second most expensive component of the feed after energy. The protein supply may have a significant impact on the intestinal microbiota, both qualitatively and quantitatively. High protein diets increase the concentrations of proteolytic bacteria, especially clostridia and E. coli (Heo et al., 2013). From the viewpoint of animal health, it is interesting that there seems to be a link between enteric pathogens and certain protein sources. With respect to poultry, administration of feed with animal derived proteins led to a sharp increase in the concentrations of Clostridium perfringens and necrotic lesions in the intestinal mucosa (Drew et al., 2004). Adjusting protein supply and amino acid profiles can be considered as essential to achieve optimal performance and to control the intestinal formation of metabolites such as ammonia and biogenic amines from protein fermentation, that are generally considered detrimental (Nyachoti et al., 2006; Heo et al., 2013; Parenteau et al., 2020). The use of supplemental amino acids would offset or minimize the need to use some of expensive animal proteins, which could reduce the cost of feeds. Furthermore, extensive use of supplemental amino acids would allow to more precisely meet the animal dietary requirements while reducing dietary crude protein. This change in formulation can positively impact gut health and the environment by reduction of environmental excretion of nitrogen and reduce metabolic stress of detoxifying N-catabolites.
IV. Nurturing favorable microflora 
Intensive rearing conditions do not usually allow for the natural microbial succession required for the establishment of a positive microbiota and the sufficient development of gut mucosal immune system (Friedman et al., 2012; Stanley et al., 2013). To optimize performance of pigs and poultry raised with AGP free feeding programs, it is essential to manage the composition of intestinal microbial community to avoid the inherent intestinal health risks of intensive production systems. In a drug free production system, the emphasis shifts from fighting the unfavorable organisms with antibiotics to nurturing the favorable organisms i.e. working with nature to ensure a favorable and stable intestinal ecology (see figure 2). (Collet, 2012) opined that the three most important legs of an effective intestinal management program includes “seeding” the gut with favorable organisms, "feeding" the favorable organisms and "weeding" out the unfavorable organisms.
Seeding the gut with favorable organisms:The first week after hatch for chicks or weaning for piglets is the most critical period. These young animals are susceptible to environmental and health challenges due to undeveloped digestive, thermoregulatory and immune systems. For example, colonization of mucosal surfaces in newly hatched chickens is dependent on environmental exposure mainly through feeds, litter, water etc (Stanley et al., 2013). Thus colonization of the gut with pioneer bacteria species, that are able to modulate expression of genes in the gut epithelia to optimize nutrient assimilation and create favorable conditions for establishment of a stable and beneficial climax flora, should be the starting point of any gut health management program (Collet, 2012). In this context, probiotics or direct fed microbials appear to be most effective during the initial development of the microbiota, or after any dietary change or stress and following antibiotic therapy and thus can be interpreted in the context of the ecological phenomena of primary and secondary succession in which a community is established or reestablished following a disturbance (Collet, 2012). As methodological advancements continue, a progress toward development of novel probiotic approaches is plausible particularly in the area of probiotics with immunomodulation capabilities (Waititu et al., 2014; Neijat et al., 2019).
Figure 2. Strategies for maintaing a functional gut in the context of AGP feeding programs
Figure 2. Strategies for maintaing a functional gut in the context of AGP feeding programs
Feeding the favorable organisms:In addition to seeding the gut with the correct pioneer species, it is crucial to enhance their ability to proliferate, compete and colonize to stall pathogen proliferation. There are many feed additives that could be used to promote proliferation of beneficial microbiome (Patterson and Burkholder, 2003). A major advantage of the symbiotic relationship between the microbiota and the host, is the ability of these organisms to provide energy to the intestinal epithelium in the form of SCFA from fibrous sources which is otherwise not digestible to the animal. Some oligosaccharides, such as inulin and oligofructose, yeast metabolites have been proposed as ‘prebiotics’ because of their potential to selectively stimulate growth of Bifidobacterium spp. within the human large intestine, suppress proliferation of potential pathogens and modulate a variety of human enteric conditions and diseases (Gibson and Roberfroid, 1995). Prebiotics are defined as ‘non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and (or) activity of one or a limited number of bacteria in the colon, and hence improve host health’ (Gibson and Roberfroid, 1995). The peculiarity with prebiotics is that they promote production of short chain fatty acids which are known to have a microbiota stabilizing effect and butyrate in particular has been shown to stimulate the production of host defense peptides (β-Defensins and Cathelicidins) (Sunkara et al., 2011). By providing a competitive advantage to the acid tolerant organisms such as the Lactobacilli and a competitive disadvantage to the acid intolerant organisms like the ClostridiaSalmonella and E. colithere is tremendous opportunity to maintain a functional and healthy gut. Such manipulation of the microbiota has both short and long term (Collet, 2012). It is important to keep in mind that a single layer of cells provide a barrier between the host and external pathogens and to maintain this barrier, the epithelial layer must be regenerated. The interaction between the epithelial layer and microorganisms present in the GIT impacts the cell replacement rate and thus growth efficiency (Willing and Van Kessel, 2007).
Weeding out the unfavorable organisms:Nurmi and Rantala introduced the term competitive exclusion (CE) more than 4 decades ago following observation that oral gavage of newly hatched chicks with intestinal contents from salmonella-free adult birds reduced Salmonella colonization (Nurmi and Rantala, 1973). Competitive exclusion generally refers to a reduction in colonization by a pathogen due to several possible mechanisms: physical occupation of a site, resource competition in a physical or chemical niche, or direct physical or chemical insult to the potential colonist (Oakley et al., 2014). Although the underlying mechanisms remain poorly understood, pioneering work of Nurmi and Rantala (1973) has inspired development of several commercial products (Oakley et al., 2014). However, practical application remains elusive because undefined cultures are often more effective in controlling salmonella than the defined cultures in commercially regulated products (Oakley et al., 2014). Alternative strategies have capitalized on increasing understanding of the molecular basis that pathogens use to attach to the mucosal for colonization. Microbe attachment to host cell docking sites on the intestinal epithelium is dependent on surface molecule structure and this is the pivotal first step in the colonization and infection (Giron et al., 2002). For example, blocking the attachment mechanism of unfavorable organisms with a type-1 fimbria blocker can reduce their capacity to compete with the favorable organisms in the gut (Giron et al., 2002). Products that mimic docking sites for specific gut epithelia glycoproteins may be useful in preventing attachment and colonization by gut pathogens recognizing these sites (Giron et al., 2002). For example, several bacteria exhibit a binding effect specific for the sugar mannose (Mirelman et al., 1980). Mannose in the cell wall may cause the yeast or its residue to act as a decoy for the attachment of bacteria to the intestinal wall and this has been the basis of commercial success of many yeast based products (Kiarie et al., 2010; Kiarie et al., 2011; Kiarie et al., 2012; Corrigan et al., 2015).
Published in the proceedings of the Animal Nutrition Conference of Canada 2020. For information on the event, past and future editions, check out https://animalnutritionconference.ca/.

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