Gut Health of Poultry: History
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Subjects: Agriculture, Dairy & Animal Science
Contributor:
Samiru Wickramasuriya

“Gut health” refers to the physical state and physiological function of the gastrointestinal tract and in the livestock system; this topic is often focused on the complex interacting components of the intestinal system that influence animal growth performance and host-microbial homeostasis.

  • chicken
  • gut health
  • gut diseases
  • gut–brain axis
  • gut integrity
  • immunity
  • microbiota

1. Introduction

The importance of gut health in animals goes beyond the physical barrier of the gut [1]. Although substantial scientific findings on gut health-related topics have been published, the understanding of its composition, importance, regulation, or interactions is still at the rudimentary stage. Nonetheless, the fact that gut health has been a matter of contention in scientific research reflects its importance in various aspects of animal nutrition and production. The term “gut health” encompasses broader areas of the physical state and physiological function of the many parts of the gastrointestinal (GI) tract [2]. Bischoff [3], while proposing the definition of gut health, used the definition as outlined by the WHO and defined the “gut health in human medicine” as a state of physical and mental well-being in the absence of GI complaints that require the consultation of a doctor, in the absence of indications or risks of bowel diseases, and the absence of confirmed bowel diseases. This definition of gut health in human medicine may be applicable to animals as well, including poultry, due to the similarity in structure, physiology, and function of the gut, despite quantitative and qualitative differences that may exist between animals and humans. Kogut and Arsenault [4] defined gut health as “the absence/prevention/avoidance of disease so that the animal is able to perform its physiological functions in order to withstand exogenous and endogenous stressors”. Later, Celi et al. [5] proposed the definition of gut health as “a steady-state, where the microbiome and the intestinal tract exist in symbiotic equilibrium, and where the welfare and performance of the animal are not constrained by intestinal dysfunction”. These definitions show that gut health is a holistic term and point out the importance of complex interactions of various components of the gut interacting with the host animal and the environment to maintain homeostasis. Indeed, Jha et al. [6] revised the early definition by Conway [7] on gut health being the function of three major components (i.e., diet, the mucosa, and the commensal microbiota); they suggested that gut health is holistically the function of four major components, including diet (i.e., nutrition), mucosa, microbiome, and the immune system, in a holistic way. Thus, understanding the four major components is a prerequisite to defining gut health and will also expand our knowledge of their functions in determining gut health. Further, a wide range of intrinsic and extrinsic factors [5] affecting gut health (e.g., gut components) need to be better elucidated.

2. Structure and Physiology

2.1. Chicken Gut and Its Relation to Gut Health

Although all poultry species possess similar gut structures, the chicken gut has unique anatomical, histological, and physiological features, which are distinct from other avian species, as well as mammals. Notably, the intestinal tract in chickens is relatively shorter than that in mammalian animals, and hence, chickens have a lesser retention time of feed and digestive capacity than in their mammalian counterparts [8]. Therefore, it is important to maintain the optimal functionality of chickens with a good gut health status as they develop to maximize the feed efficiency and growth.
Similar to other avian species, chickens use their beaks to obtain feed. Compared with other poultry species, chickens have a heavily keratinized tongue, owing to the absence of a stratum granulosum [9]. Interestingly, antimicrobial peptides (AMPs), such as beta-defensins, gallinacin-3, and gallinacin-6, are expressed in chicken tongue, along with the presence of Langerhans cells, indicating their crucial role in the first line of immune defense against pathogens locally [10]. Secretions from the salivary glands contain salivary enzymes, such as amylase, and the salivary mucus initiates a chemical/mechanical defense mechanism against pathogens to maintain optimum gut health [10].
In chickens, feedstuff, once ingested through the mouth, passes into the crop through the esophagus. The crop serves as temporary storage for feedstuff, which is mixed with water. Chickens have a proventriculus (glandular stomach) together with a gizzard (muscular stomach). The proventriculus initiates the digestion of feed by secreting hydrochloric acid and digestive enzymes [11]. Tabata and Yasugi [12] reported that the expression of a spasmolytic polypeptide on the surface cells of the chicken proventriculus plays an important role in the repair of the mucosal epithelium to maintain the status of good gut health. In addition, the proventricular mucus forms a physical barrier to provide protection against pathogens [10]. Beyond this physical barrier, the expression of a moderate level of beta-defensin 6 in the proventricular mucosa indicates a broad-spectrum antimicrobial activity to exclude pathogens [13].
The gizzard, a distinctive feature of the chicken GI tract, is located at the posterior of the proventriculus. Although mainly mechanical digestion occurs in the gizzard, the digestive action of pepsinogen and hydrochloric acid has also been reported in this region, owing to a short retention time of the digesta in the proventriculus [14]. Hydrochloric acid lowers the gizzard pH, which provides a beneficial effect on gut health through disinfection. Gizzard development helps to improve pancreatic enzyme secretion in the small intestine, enhances GI tract motility, and improves nutrient digestibility, thereby enhancing gut heath and function [15].
The small intestine aids in nutrient digestion and absorption with the help of epithelial finger-like projection villi [11]. The breakdown of feed into nutrients takes place in the intestinal lumen with the aid of gastric enzymes secreted by the pancreas and bile secreted by the liver. After digestion, the absorption of nutrients occurs through the wall of the small intestine into the bloodstream. In addition to digestion and absorption, the small intestine also plays a dynamic role in maintaining the gut health of chickens and functions in both innate and humoral immunity in the small intestine [10][16]. Four types of barriers, including microbial, chemical, physical, and immunological, work integrally in the intestine to maintain the intestinal barrier functions to prevent the growth of harmful entities, including pathogens, toxins, and foreign antigens [17][18].
Fermentation of the fiber or undigested nutrients in the digesta takes place in the caeca, with the aid of microbes, to produce volatile fatty acids in chickens [19]. Chicken caeca possess both innate and humoral immune functions similar to the small intestinal segment [10]. It also plays a prominent role in gut health by providing a niche for large microflora, including zoonotic bacteria [20]. The proximal part of the caeca contains lymphatic tissues, which form a tonsil [21]. The presence of lymphoid nodules throughout the mucus membrane provides evidence of a greater immune defense mechanism in the chicken caeca to maintain gut immune homeostasis. The large intestine or colon is relatively shorter in chickens in contrast to mammals. Moreover, chicken large intestine is also comparatively shorter than its small intestine. It is still to be determined whether the large intestine in chickens plays a similar role in maintaining gut health as the upper segments of the intestine.

2.2. Gut–Brain Axis and Gut Health

The gut–brain axis refers to the bidirectional communication system between the GI tract and the central nervous system; it plays a responsible role in mediating neural, immunological, and hormonal signaling [22]. This complex system allows the gut to influence the brain through visceral messages. These visceral messages created by the host or gut microbes interact with the enteric nervous system to transduce signals into the brain. In response, signals from the brain influence the gut functions (motor, sensory, and secretory modalities) and immune function. This dual interaction between the gut and the brain not only influences gut physiology but can also affect local pathological processes. The gut–brain axis system is well-documented in mammals [22][23]. However, limited information on the chicken gut–brain axis undermines our understanding of how the brain influences gut health in chickens. The comparison of mammalian and avian neural structures, together with the gut microbiome, described by Villageliũ and Lyte [24], confirms the existence of the chicken gut–brain axis. Based on the literature, we developed a gut–brain axis model for chickens, as shown in Figure 1. When chickens encounter enteric stress or inflammation, the intestinal epithelium, enteric muscles, and associated immune cells transmit signals to the brain via the central nervous system (vagus nerve). Further, it induces leucocytes to release cytokines into circulation from the intestine [25].
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Figure 1. Proposed gut–brain axis model for chickens. The gut–brain axis refers to the bidirectional communication system between the central nervous system and the GI tract. When chickens encounter enteric stress or inflammation, the intestinal epithelium, enteric muscles, and associated immune cells transmit signals to the brain via the central nervous system (vagus nerve). Further, it induces the leucocytes to release cytokines into circulation from the intestine. Cytokines trigger the activation of the central nervous system. Neurotransmitters produced by chicken gut microbes also induce the central nervous system. All these stimuli from the intestine via the vagus nerve activate the hypothalamic–pituitary–adrenal (HPA) axis and increase the serum corticosterone levels. Corticosterone thereby modulates heterophile migration into the inflammation site of the GI tract to attune inflammation. Activation of the HPA axis leads to sickness behavior in chicken, owing to elevated cortisol secretion.

3. Intestinal Immune System in Gut Health

Since the gut is constantly challenged by the antigenic substances from the diet and the dynamic ecosystem of gut microbiota populations, inflammation, which is an important part of innate and adaptive immune responses to protect the host against antigenic challenges, plays a critical role in the healing process and dictates the status of the gut health. Although inflammation is a vital response to infections for the survival of the host, the balance of factors that promote and regulate inflammatory responses needs to be better understood. In livestock, inflammation that is initiated by diet or external stressors often causes dysbiosis, with unwanted consequences on growth performance and gut health [26]. Thus, studies on effective methods for chicken production are directed towards balancing pro- and anti-inflammatory responses to prevent overzealous chronic inflammatory responses that can be detrimental to gut health. The main limitation of an anti-inflammatory approach in chickens is their vulnerability to infections, particularly in young chickens, since their immune systems are not fully developed. Gut inflammation is initiated by gut resident immune cells, mostly innate immune cells, including APCs and heterophils, that express pattern recognition receptors (PRRs). In the chicken gut, various toll-like receptors (TLRs), including TLR1, 2, 3, 4, 5, 7, and 15, are expressed [27], and the activation of TLRs induces downstream signaling pathways, such as mitogen-activated protein kinase (MAPK) and nuclear factor kappa beta (NF-κB). This results in a protective immune response supported by the recruitment of immune cells and the expression of associated proinflammatory mediators and AMPs. The process of inflammation consumes nutrients, which are routed from productive purposes, thus reducing the appetite in poultry. Therefore, it is critical to find a point of balance between inflammation and anti-inflammation for a healthy gut in poultry.

GALT plays a major role in the gut immune response, inducing a full spectrum of innate and adaptive immune responses that vary depending on the nature of the stressors, including pathogens. The common features of the host immune response aim to limit the infection. The mucus layers, with varying thicknesses and compositions, trap invasive bacteria via the luminal flow, as well as providing lubrication, and colonization sites, nutrients for commensal bacteria, and a transport system between the gut contents and epithelial linings [28]. The optimum mucus layer thickness is represented as the number of goblet cells secreting mucins. Mucins can be either neutral or acidic, and the latter protects against bacterial translocation [29]. Abnormal mucus layer thickness is associated with enteric infection and poor performance [30]. Besides the mucus layer, AMPs and secretory IgA (sIgA) are integral components of the gut immune system. AMPs are expressed by a variety of cells, including Paneth cells. Defensins are the most studied AMPs in chickens; the chicken genome encodes for 14 β-defensin genes, also known as gallinacins, but no α-defensins [31]. NK-lysin, a homolog of human granulysin, has also been reported to play a role in gut infection by protozoan parasites such as Eimeria spp. [32][33][34]. They possess broad-spectrum antimicrobial activities against Gram-negative and Gram-positive bacteria, fungi, viruses, and protozoa [35]. They are also involved in the modulation of immune responses and determination of the microbiota composition [31]. IgA is secreted from the plasma cells present in the lamina propria; they can neutralize pathogens and facilitate their removal from the GI tract and play a role in intestinal homeostasis, including establishment, maintenance, and the control of commensal microbes [36]. Since lamina propria IgA-positive cells and intestinal IgA levels are both significantly reduced in germ-free animals, they could play a potential role in the gut microbiota [37]. Several studies have been conducted on the relationship between gut microbiota and the host immune response. The mucus secreted from goblet cells can act as a source of nutrients for the resident microbiota, which can be used to inhibit the expansion of other bacteria [38]. Controlled inflammation requires gut microbiota to regulate the gut immune response either towards inflammation or tolerance [39].

4. Microbiota in Chicken Gut Health

The chicken gut is home to more than 100 trillion microorganisms collectively called the gut microbiota, whose membership includes bacteria, fungi, protozoa, and viruses [40]. Among these microbes, bacteria play a dominant role in intestinal functions. They are colonized in different segments with vast diversities; they help in digestion, developing the local immunity, and intestinal health.
The crop and gizzard are usually dominated by Lactobacilli and Streptococci, accounting for 103–104 colony-forming units/g [41]. Compared to the rest of the small intestine, the ileum contains the richest bacterial community, whereas the duodenum has the lowest bacterial density [42]. The majority of the microbiota community in the duodenum are Lactobacilli and Bifidobacteria [43]. Lactobacilli, Enterococci, and Clostridiaceae are commonly detected in the jejunum [44], while Streptococci, Bacteroides, Clostridia, Escherichia coli, Ruminococci, Enterococci, and Lactobacilli are dominated in the ileum [45]. In comparison to the ileum, the ceca harbor a more diverse, abundant, and stable microbial community that is composed of the genera Bacillus, Clostridium, Enterococcus, and Ruminococcus [46][47]. Similar to the caeca, the cloaca also shows a more diverse and abundant bacterial population, consisting of Clostridia, Streptococci, Enterococci, and E. coli [45].
One of the key functions of the gut microbiota is extracting essential nutrients from the diet and making them available to the chicken [48]. This involves the extraction, absorption, and synthesis of a wide variety of biochemicals with growth-promoting effects, including water- or lipid-soluble vitamins (e.g., vitamin B and vitamin K), organic acid (lactic acid), complimentary enzymes (e.g., non-starch polysaccharides (NSPs)), and antimicrobial compounds [49]. Soluble dietary fibers and resistant starch are actively fermented by cecal microbiota to produce metabolites such as short-chain fatty acids (acetate, butyrate, and propionate), which are beneficial to the physiological functions of chickens [50]. The intestinal microbiota significantly influences the drug metabolism [51] and nitrogen metabolism [52]. Thus, an imbalance in the microbial community affects gut microbial fermentation, host metabolism, and gut health.
The gut microbiota produces metabolites and influences intestinal homeostasis [53]. Maintaining a balanced homeostasis supports the tolerance for infections and nonpathogenic stressors [54]. Metabolites, mediated by the microbiota, are regarded as major modulators of host-microbiota communication and closely interact with the host immune system, which, along with diverse types of immune cells, mediates various immune signaling pathways [55].
The gut microbiota is also involved in protecting gut barrier functions to improve gut health. The gut microbiota protects the intestinal barrier by attaching to the epithelial walls of the enterocyte and reducing the colonization of pathogenic bacteria [49]. Simultaneously, the beneficial bacteria, including Lactobacillus plantarum, L. reuteri, and L. rhamnosus, help the development of the mucosal epithelia, especially immune cells whose primary function is to protect the gut barrier against pathogens [44]. The inner layer of the mucus functions as a highly efficient first line of defense against pathogenic microbiota, such as Clostridium jejuni and Helicobacter pylori [56]. Sommer et al. [57] reported that the intestinal microbiota has a significant impact on the mucus layer based on the observation of fewer goblet cells in germ-free mice. Moreover, the commensal microbial population works against the pathogen invasion through competitive exclusion, thus maintaining gut homeostasis [42].

5. Intestinal Infections and Their Impact on Gut Health

Intestinal infection caused by parasites, viruses, and bacteria is a major factor that causes dysbiosis and disturbs the intestinal immune homeostasis. Some of these diseases are the results of secondary infections and may involve respiratory tracts and other organs. Based on the nature of the causative agent, intestinal infections can be divided into three categories: parasitic, bacterial, and viral diseases (Figure 2).
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Figure 2. Major intestinal infectious diseases in poultry. Based on the nature of the causative agent, intestinal infections can be divided into three categories: parasitic, bacterial, and viral diseases.

5.1. Parasitic Diseases

Coccidiosis is a common intestinal disease caused by several species of the protozoan parasite of the genus Eimeria, which invades the intestinal lining of chickens. It is one of the major intestinal infectious diseases of poultry that causes severe economic losses worldwide [58][59]. Coccidiosis is initiated when chickens ingest the environmentally resistant Eimeria oocysts. These Eimeria spp. characteristically infect a specific site of the intestinal tract, resulting in severe inflammation and necrosis in the submucosa, although the mechanism of site-specificity of Eimeria is not well-known [60][61]. For every oocyst ingested, innumerable parasites are reproduced in the intestine and transmitted to the entire poultry house via contaminated feces. The invasion of these Eimeria sporozoites into the intestinal tract and their subsequent intracellular development damages the intestinal epithelium, obstructing nutrient absorption and immune suppression of the host chicken for their survival. Consequentially, poor growth performance and higher mortality have been reported in chickens [62].

Blackhead (Histomoniasis) is a chicken gut disease caused by the single-celled protozoa Histomonas meleagridis. Although it is relatively common in captive-raised game birds and turkeys [63], it is also found in several other avian species, including grouse, quail, and pheasants [64]. The pathogenesis of H. meleagridis begins with the colonization of the caecum of the birds, thereafter leading to severe intestinal inflammation and necrosis [65]. Histomonas parasites penetrate the blood vessels and reach the liver via the portal veins [63]. Moreover, unusual lesions have also been reported in other visceral organs of turkey, such as the kidneys, lungs, and bursa of Fabricius [66]. In chickens, lesions are mostly found in the caecum, with less or no necrosis in other organs [67].

5.2. Bacterial Diseases

NE is an enteric disease of poultry caused by C. perfringens, and coccidiosis is its primary risk factor. C. perfringens is a spore-forming, anaerobic Gram-positive bacilli that is widely distributed in freshwater or soil. It is also found as a member of the normal intestinal flora of birds [68]. C. perfringens strains are classified into five toxin types (A–E), according to the toxins they produce [69]. B-like toxin (NetB) produced by C. perfringens is identified as the causative agent of NE. However, a simple infection is not sufficient to provoke the disease. Increased consumption of barley, wheat, or other poorly digestible proteins and coinfection by Eimeria spp. are various predisposing factors that trigger the disease [70][71].

Ulcerative enteritis (UE) is one of the most common acute bacterial diseases in quail caused by the bacterium Clostridium colinum. Several predisposing factors, such as coccidiosis, chicken infectious anemia virus (circovirus), Gumboro disease, and stress conditions, may increase the incidence of UE and subsequent mortality [72]. Intestinal lesions are characterized by multiple ulcers throughout the tract, including the duodenum, jejunum, ileum, and cecum; peritonitis and multifocal necrotizing hepatitis are also observed in many cases [73]. 

Salmonellosis is a collection of infectious diseases caused by the species belonging to the genus Salmonella. Imbalance in the normal intestinal microflora due to antibiotic abuse, deficiency of nutrients, and Eimeria infections has been associated with Salmonella proliferation and colonization in the GI tract [74]. In chickens, enteric lesions induced by Salmonella infections are often associated with secondary infections with fowl typhoid (FT) and Pullorum disease (PD). FT and PD are the most significant bacterial diseases in chickens [75]. FT is an acute or chronic septicemic disease of mature chickens caused by Salmonella Gallinarum, whereas PD, caused by Salmonella Pullorum, is an acute systemic infection occurring more in young broiler chickens.

5.3. Viral Diseases

The poultry coronavirus, also known as the infectious bronchitis virus (IBV), is a highly contagious, acute disease-causing agent of poultry. High mortality is the major concern of coronavirus infection. However, poor growth performance, impaired feed efficiency, renal disease, insufficient egg quality, and decreased egg production are other issues associated with IBV infection [76]. Although IBV mainly replicates in the epithelial surface of chicken respiratory tracts and causes respiratory illness, it can also replicate in the enteric tract, oviducts, and the kidneys [77][78]. However, the replication of IBV in the chicken intestine does not cause any pathological changes [79]. The susceptibility of birds to the IBV strains is triggered by various factors, including environmental stress, age, and genetics [80]. The domestic chickens and pheasants (Phasianus spp.) are primarily the susceptible hosts for IBV [81].

Avian reovirus (ARV) is a nonenveloped, double-stranded RNA virus belonging to the genus Orthoreovirus in the Reoviridae family [82]. ARV is ubiquitous among commercial poultry and has been reported to be responsible for a variety of disease conditions in poultry, including malabsorption syndrome (MAS), runting-stunting syndrome (RSS), tenosynovitis, gastroenteritis, and immune suppression [83][84][85]. The most common mode of transmission of ARV is the fecal–oral route; following which, the initial replication occurs in the mucosa of the intestinal and respiratory tracts. However, infection via egg transmission has also been reported [86][87].

Adenoviruses are nonenveloped, icosahedral viruses that belong to the family Adenoviridae. Adenoviruses can be subdivided into a mammalian adenovirus (mastadenovirus) and avian adenovirus (aviadenoviruses) [88]. Further, avian adenoviruses can be subdivided into groups I, II, and III. Group I avian adenoviruses are usually found in excreta or in the tissues of birds with GI diseases. Various diseases, including runting/MAS [89], proventriculitis [89], ventriculitis [90], enteritis [91], and mortality syndrome [92], are associated with group I.

6. Factors Affecting Intestinal Health

A wide range of factors affecting chicken gut health has been identified. Understanding their mechanisms is critical to maintaining a healthy chicken flock in a profitable way. Different researchers have categorized these factors in various ways [49][93]. Host factors, feed and feeding factors, and environment and biosecurity factors are the main factors that affect intestinal health(Figure 3).
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Figure 3. Factors affecting chicken gut health. A wide range of factors affecting chicken gut health can be categorized into three categories: host factors, feed and feeding factors, and environment and biosecurity factors. A single factor or many factor combinations can significantly affect the structure and physiological function of the chicken gut, altering the gut health and performance.

This entry is adapted from the peer-reviewed paper 10.3390/vaccines10020172

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