Chicken gastrointestinal system

Intestinal health is essential for production success in broiler chickens. Changes in this complex system may lead to poor performance, increased mortality and condemnations as well as higher medication costs (Hafez, Reference HAFEZ2011). Additionally, intestinal health issues may pose a food safety risk for consumers.

The structure and function of the broiler gastrointestinal system (GIT) have been well reviewed in literature, and hence will not be described here (Dibner and Richards, Reference DIBNER and RICHARDS2004). The key function of the GIT is to digest and absorb dietary nutrients and excrete waste (Kiarie et al., Reference KIARIE, ROMERO and NYACHOTI2013). The mechanisms of nutrient absorption within the broiler GIT are dependent on nutrient type, but can be by diffusion or specific transporters. The secondary function of the GIT is one which involves immune response (Yegani and Korver, Reference YEGANI and KORVER2008). The GIT provides the largest surface area in the body and is continually exposed to pathogenic organisms and harmful substances, demonstrating the importance of immune function (Choct, Reference CHOCT2009). Numerous interactions between microbes, feed antigens, the immune system, and gut associated lymphoid tissue (GALT) occur in the GIT. GALT has the function of providing immune cells and their products to defend against pathogens (Janardhana et al., Reference JANARDHANA, BROADWAY, BRUCE, LOWENTHAL, GEIER, HUGHES and BEAN2009).

The GIT harbours a large number of diverse microbes. These microbes may be commensal or pathogenic and affect host nutrient utilisation and intestinal development either positively or negatively (Dumonceaux et al., Reference DUMONCEAUX, HILL, HEMMINGSEN and VAN KESSEL2006). Bacteria are the most abundant and diverse form of microbe in the intestine (Apajalahti et al., Reference APAJALAHTI, KETTUNEN and GRAHAM2004; Choct, Reference CHOCT2009; Yeoman et al., Reference YEOMAN, CHIA, JERALDO, SIPOS, GOLDENFELD and WHITE2012). Depending on microbial composition, these bacteria can manifest in various ways from a severe clinical presentation of disease to no clinical effect.

Under normal circumstances, a balanced intestinal microbial community (MC) provides a barrier against pathogen colonisation and contributes to the overall health of the host. Optimal function includes producing metabolic substrates such as vitamins and short-chain fatty acids, and stimulating the immune system (Gaggía et al., 2010). Studies have demonstrated that intestinal microbial composition and associated metabolic activities can influence a chick's gastro intestinal (GIT) development, gene expression, physiology, and resistance to infection (Torok et al., Reference TOROK, HUGHES, MIKKELSEN, PEREZ-MALDONADO, BALDING, MACALPINE, PERCY and OPHEL-KELLER2011). Intestinal MCs carry out functions such as nutrient utilisation, mucous secretion, immune development, and cytokine expression (Kiarie et al., Reference KIARIE, ROMERO and NYACHOTI2013).

A better understanding of the microbial ecology of the chicken intestinal microbiome is necessary to develop strategies to improve feed efficiency and growth, avoid enteric disease, and reduce growth of pathogens of public health significance (Gong et al., Reference GONG, FORSTER, YU, CHAMBERS, WHEATCROFT, SABOUR and CHEN2002; Kiarie et al., Reference KIARIE, ROMERO and NYACHOTI2013). Numerous studies have demonstrated that bacterial diversity and numbers vary throughout the different parts of the GIT (Yegani and Korver, Reference YEGANI and KORVER2008). Taxonomic richness of bacteria is highest in the caecum, where the longest digesta transit times and most microbial fermentation occur (Gong et al., Reference GONG, FORSTER, YU, CHAMBERS, WHEATCROFT, SABOUR and CHEN2002; Stanley et al., Reference STANLEY, DENMAN, HUGHES, GEIER, CROWLEY, CHEN, HARING and MOORE2012a). A culture-independent analysis of the chicken caecal microbiota by Apajalahti et al. (Reference APAJALAHTI, KETTUNEN and GRAHAM2004) estimated that the caecum consists of over 600 species of bacterium from more than 100 genera, with a large proportion of the bacteria belonging to unclassified species.

The MC species diversity has been revealed to be more complex than previously thought. Numerous recent studies have used sophisticated molecular technology to better analyze the MC. A review on the broiler intestinal microbiome by Yeoman et al. (Reference YEOMAN, CHIA, JERALDO, SIPOS, GOLDENFELD and WHITE2012) indicates that the bacterial phylum Firmicutes is the predominant phylum in chicken crop, gizzard, small intestine, and caecum. Organisms belonging to the Lactobaccillales order have been reported to dominate in the jejunum (Stanley et al., Reference STANLEY, DENMAN, HUGHES, GEIER, CROWLEY, CHEN, HARING and MOORE2012a), small intestine locations (Gong et al., Reference GONG, FORSTER, YU, CHAMBERS, WHEATCROFT, SABOUR and CHEN2002; Dumonceaux et al., Reference DUMONCEAUX, HILL, HEMMINGSEN and VAN KESSEL2006), and caecum (Gong et al., Reference GONG, FORSTER, YU, CHAMBERS, WHEATCROFT, SABOUR and CHEN2002; Stanley et al., Reference STANLEY, KEYBURN, DENMAN and MOORE2012b). Gong et al. (Reference GONG, FORSTER, YU, CHAMBERS, WHEATCROFT, SABOUR and CHEN2002) identified E. cecorum and unidentified butyrate-producing bacteria in the ilea and caeca. Butyrate is known to increase disease resistance (Stanley et al., Reference STANLEY, KEYBURN, DENMAN and MOORE2012b). In addition to Lactobacillus spp. (24.4%), Stanley et al. (Reference STANLEY, DENMAN, HUGHES, GEIER, CROWLEY, CHEN, HARING and MOORE2012a) observed that the caecal microbiota was composed mainly of Clostridium spp. (20.1%), Bacteroides spp. (15.8%), and unknown bacteria (19.0%). Recently, Wei et al. (Reference WEI, MORRISON and YU2013) created a phylogenetic diversity census of bacteria found in the GIT of broiler chickens by performing an analysis of 16s rRNA gene sequences archived in public databases. The study represented a comprehensive look at the chicken intestinal microbiome due to the representation of different diets, geographies, and methodologies. Firmicutes accounted for 70% of the bacterial sequences, followed by Bacteriodetes (12.3%), Proteobacteria (9.3%) and unclassified sequences (5.3%).

Studies have attempted to determine which MC profiles are associated with good production performance. Such knowledge would be useful in developing novel products to improve intestinal health. Various trials by Torok et al. (Reference TOROK, HUGHES, MIKKELSEN, PEREZ-MALDONADO, BALDING, MACALPINE, PERCY and OPHEL-KELLER2011) investigating MCs in broiler chickens using microbial profiling found several operational taxonomic units (OTUs) within both the ilea and caeca which were associated with high performance as measured by feed conversion ratio. These OTUs showed high sequence identity with classified, known bacteria, including: Lactobacillus salivarius, Lactobacillus aviarius, Lactobacillus crispatus, Faecalibacterium prausnitzii, Escherichia coli, Gallibacterium anatis, Clostridium lactatifermentans, Ruminococcus torques, Bacteroides vulgatus, and Alistipes finegoldii. Stanley et al. (Reference STANLEY, DENMAN, HUGHES, GEIER, CROWLEY, CHEN, HARING and MOORE2012a) observed 20 OTUs that were more abundant in high performance birds and hypothesised to have contributed to the differences in performance measures. Except for those classified as Spiroplasma platyhelix and Lactobacillus crispatus, the performance associated phylotypes were related to, or members of, the order Clostridiales, including: Firmicutes, Clostridia, and Clostridiales. Papillibacter, Coprobacillus, Anaerotruncus, and Anaerovorax were detected in the caecum in trace amounts, which according to the author's knowledge, had been previously unreported in chicken caecal microbiota. Johnson (Reference JOHNSON2013) found a strong correlation between the presence of Candidatus division Arthromitus-like organisms in the ileum of turkey poults and performance, suggesting this organism plays a positive role in both turkey intestinal microbial development and weight gain. However, this organism has not been well studied due to difficulties in culturing as a result of its dependence on its host to perform metabolic functions.

A number of factors influence MCs in the broiler intestine, including certain types of bacteria, viruses, and parasites. Bacterial agents may include: Salmonella spp., E. coli, and Clostridia spp; viral agents may include: reovirus, rotavirus, enterovirus, coronoavirus, parvovirus, and Newcastle disease; and parasitic agents consist of coccidia (Hafez, Reference HAFEZ2011). Non-infectious causes may shift MCs, including host genotype, gender, age (Zhao et al., Reference ZHAO, WANG, SIEGEL, HE, WANG, ZHAO, ZHAI, TIAN, ZHAO, ZHANG, SUN, CHEN, ZHANG and MENG2013), antimicrobial use (Danzeisen et al., Reference DANZEISEN, KIM, ISAACSON, TU and JOHNSON2011), space allowance (Guardia et al., Reference GUARDIA, KONSAK, COMBES, LEVENEZ, CAUQUIL, GIULLOT, MOREAU-VAUZELLE, LESSIRE, JUIN and GABRIEL2011), litter management (Torok et al., Reference TOROK, HUGHES, OPHEL-KELLER, ALI and MACALPINE2009), disease (Stanley et al., Reference STANLEY, KEYBURN, DENMAN and MOORE2012b), stress caused by high temperatures and feed withdrawal (Burkholder et al., Reference BURKHOLDER, THOMPSON, EINSTEIN, APPLEGATE and PATTERSON2008), feed composition (Jia et al., Reference JIA, SLOMINSKI, BRUCE, BLANK, CROW and JONES2009), processing (Engberg et al., Reference ENGBERG, HEDEMANN and JENSEN2002) and feed additives (Kiarie et al., Reference KIARIE, ROMERO and NYACHOTI2013).

Diet is a major factor influencing microbial composition, as different bacteria have different substrate preferences (Yegani and Korver, Reference YEGANI and KORVER2008). The broiler intestinal microbiota is influenced by dietary ingredients such as levels of fat, protein, and carbohydrate, physical structure, including particle size and processing technique and the use of antimicrobials (Torok et al., Reference TOROK, HUGHES, MIKKELSEN, PEREZ-MALDONADO, BALDING, MACALPINE, PERCY and OPHEL-KELLER2011). Hypotheses exist, but the true mechanism of action by which antimicrobials elicit their growth permitting effect is poorly understood, a knowledge gap limiting the ability to identify non-antimicrobial alternatives for gut health. Niewold (Reference NIEWOLD2007) suggested that the mechanism of action common to AGPs was an anti-inflammatory effect.

Numerous studies have evaluated the impact of antimicrobial use on the intestinal microbiome. The consensus of opinion from various research is that antimicrobial use contributes to MC shifts (Smirnov et al., 2005; Dumonceaux et al., Reference DUMONCEAUX, HILL, HEMMINGSEN and VAN KESSEL2006; Danzeisen et al., Reference DANZEISEN, KIM, ISAACSON, TU and JOHNSON2011; Lin et al., Reference LIN, HUNKAPILLER, LAYTON, CHANG and ROBBINS2013; La Vorgna et al., Reference LA VORGNA, SCHAEFFER, BADE, DICKSON, COOKSON and DAVIS2013; Singh et al., Reference SINGH, KARIMI, DEVENDRA, WALDROUP, CHO and KWON2013) with effects that are specific to the antimicrobial investigated. These shifts cause a proliferation of bacteria which may be beneficial to the host, providing nutritional and health benefits, including competitive exclusion with pathogenic bacteria, aiding in the digestion of certain feed components, producing essential metabolites or degrading anti-nutritional dietary components (Dumonceaux et al., Reference DUMONCEAUX, HILL, HEMMINGSEN and VAN KESSEL2006). Other impacts of antimicrobial use can be alterations in processes such as mucin biosynthesis involved in intestinal function and health, including nutrient uptake (Smirnov et al., Reference SMIRNOV, PEREZ, AMIT-ROMACH, SKLAN and UNI2005) and increased body weight - likely the result of increased nutrient absorption capacity due to thinning of intestinal wall (Singh et al., Reference SINGH, KARIMI, DEVENDRA, WALDROUP, CHO and KWON2013).

Additionally, antimicrobial supplementation selects for the presence of resistance genes in the intestinal microbiota. Resistance in commensal intestinal bacteria such as E. coli and Salmonella spp. is of particular concern as these pathogens have been isolated from retail chicken products, and can find their way into the environment (Diarra et al., Reference DIARRA, SILVERSIDES, DIARRASSOUBA, PRITCHARD, MASSON, BROUSSEAU, BONNET, DELAQUIS, BACH, SKURA and TOPP2007). Zhou et al. (Reference ZHOU, WANG and LIN2012) suggested that normal intestinal microbiota play an influential role in development and transmission of antimicrobial resistance via horizontal gene transfer. However, because culture of most intestinal organisms is challenging, the ability to research the antimicrobial resistance reservoir in the poultry intestinal microbiome is limited (Zhou et al., Reference ZHOU, WANG and LIN2012). Diarra et al. (Reference DIARRA, SILVERSIDES, DIARRASSOUBA, PRITCHARD, MASSON, BROUSSEAU, BONNET, DELAQUIS, BACH, SKURA and TOPP2007) demonstrated that the GIT of broiler chickens can be colonised by multi-drug resistant E. coli, and that the use of growth promotants may exert selection pressure for the development of such bacteria. The presence of class 1 integrons in E. coli, mobile genetic elements able to capture resistance genes, indicated a potential for horizontal transfer of resistance genes between E. coli bacteria and other chicken intestinal bacteria of public health importance.

Stress is another factor shown in various studies to have deleterious impacts on animal production and welfare (Lara and Rostagno, Reference LARA and ROSTAGNO2013). Although the mechanisms are not well understood, there is increasing evidence that stress can alter host-pathogen interactions in the intestine to cause shifts in intestinal MCs (Rostagno, Reference ROSTAGNO2009). Stress may cause colonisation and proliferation of pathogens of public health significance, such as Salmonella and Campylobacter spp. (Rostagno et al., 2009; Lara and Rostagno, Reference LARA and ROSTAGNO2013). Burkholder et al. (Reference BURKHOLDER, THOMPSON, EINSTEIN, APPLEGATE and PATTERSON2008) demonstrated that environmental heat stress led to changes in epithelium structure and in normal microbiota, including increased attachment of Salmonella enteritidis, a pathogenic serotype. An imbalance in gastrointestinal populations may weaken the immune system and predispose broiler chickens to colonisation of the GIT by a variety of pathogenic, and potentially zoonotic, bacteria.

Shifts in the proportions of intestinal bacterial populations can have very detrimental effects on flock health (Gaggía et al., 2010) and pose public health concerns (Diarra et al., Reference DIARRA, SILVERSIDES, DIARRASSOUBA, PRITCHARD, MASSON, BROUSSEAU, BONNET, DELAQUIS, BACH, SKURA and TOPP2007). Reductions in flock uniformity, reduced weight gain and feed conversion are among the clinical outcomes of enteric disease which have devastating financial impacts. Until recently, researchers have focused on the most severe clinical form of named classical intestinal diseases such as necrotic enteritis and coccidiosis. It is now understood that a spectrum of clinical severity exists for a variety of enteric pathogens, which ranges from severe disease to mild clinical, subclinical, or no effect. The less severe forms of enteric diseases, particularly the subclinical forms, have an impact on production with few clinical signs. These subclinical forms of disease, in addition to the new intestinal health issue dysbacteriosis which is less commonly found in the literature, will be discussed below.

Coccidiosis

Seven species of Eimeria spp. are known to induce coccidial infection which can present in three forms - severe, mild or subclinical. The severe clinical form, depending on Eimeria spp., may elicit a range in the severity and type of symptoms, including diarrhoea, morbidity, reduction in weight gain and feed conversion, intestinal lesions and haemorrhaging, and even mortality. Coccidiosis in poultry has been thoroughly reviewed by Williams (Reference WILLIAMS2005). Mild infection does not produce any severe effects although subclinical infection is associated with slight decreases in growth and feed efficiency. Despite strict biosecurity and management protocols, it is extremely challenging to keep commercial flocks free of coccidia because Eimeria spp. are ubiquitous in the environment (Allen and Fetterer, Reference ALLEN and FETTERER2002). Coccidiosis infection in poultry is distributed worldwide, although it is uncommon to find severe clinical cases due to widespread implementation of control measures such as anticoccidials (Williams, Reference WILLIAMS1999). Martynova-Van Kley et al. (Reference MARTYNOVA-VAN KLEY, OVIEDO-RONDÓN, DOWD, HUME and NALIAN2012) investigated the microbial shifts which occurred in broiler chickens challenged with Eimeria spp. Results indicated that challenge did not affect intestinal MC diversity, however, composition was altered. Pre-infection, caecal contents predominantly consisted of bacterial species belonging to genera Subdoligranulum, Coprococcus, Alistipes, Lactobacillus, and Faecalibacterium, whereas post-infection samples were mainly from Escherichia/Shigella and Bacteroides spp. Hume et al. (Reference HUME, CLEMENTE-HERNANDEZ and OVIEDO-RONDÓN2006) also demonstrated dramatic changes in MC in the duodenal, ileal, and caecal intestinal sections of birds following challenge with mixed Eimeria spp.

Necrotic enteritis

Clostridium perfringens is a Gram positive, spore-forming anaerobic bacterium that is commonly found in environment and intestinal tract of animals and humans as part of normal intestinal microbiota. However, C. perfringens is also the causative agent of one of the most prevalent and economically devastating diseases in poultry, necrotic enteritis (NE) (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). In poultry, the clinical form of disease is characterised by depression, ruffled feathers, diarrhoea, huddling, anorexia and often, high mortality. There is also a mild form of the disease, subclinical NE, which has been described by Wilson et al. (Reference WILSON, TICE, BRASH and St. HILAIRE2005). Subclinical NE has been estimated to decrease body weight by up to 12% and increase feed conversion ratio by 10.9% compared with healthy birds, imposing a significant economic burden (Skinner et al., Reference SKINNER, BAUER, YOUNG, PAULING and WILSON2010). Predisposing factors for NE include: coccidiosis, diet, high density, stress, and immunosuppression (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). However, aspects regarding initiation and progression of the disease, including the role other microorganisms play, is poorly understood. Stanley et al. (Reference STANLEY, KEYBURN, DENMAN and MOORE2012b) contrasted MCs between healthy birds and NE challenged birds. Researchers observed that C. perfringens challenge significantly altered intestinal MC in the caeca, including a reduction in the number of butyrate producers and a 3.7 fold increase in an unclassified order of Mollicutes compared with healthy birds. These authors suggested that the disturbance in the composition of caecal microbiota may play a role in development and manifestation of NE. In another study by Feng et al. (Reference FENG, GONG, YU, JIN, ZHU and HAN2010), a decrease in numbers of Lactobacillus spp. was noted following C. perfringens challenge, particularly the suppression of L. aviarius. Liu et al. (Reference LIU, GUO and GUO2012) noted significantly smaller villus height and villus height: crypt depth ratio in ileum and jejunum of birds challenged with C. perfringens.

Dysbacteriosis

Dysbacteriosis collectively encompasses a widespread syndrome causing intestinal health problems in broiler chickens. This syndrome has been reviewed by Teirlynck et al. (Reference TEIRLYNCK, GUSSEM, DEWULF, HAESEBROUCK, DUCATELLE and VAN IMMERSEEL2011) and briefly by Wilson et al. (Reference WILSON, TICE, BRASH and St. HILAIRE2005), where it is defined as ‘shifts in enteric bacterial populations to qualitatively and/or quantitatively abnormal microbiota that do not normally predominate’. Although the term dysbacteriosis is not commonly recognised in North America, shifts in intestinal MCs are known to play an integral role in avian intestinal health. Recently, Johnson (Reference JOHNSON2013) attempted to characterise the shift in intestinal MCs of turkey poults grown in the United States by following individual turkeys temporally. The researchers observed that although there were differences in timing, a predictable shift existed in the succession of turkey ileum microbiome. Microbiome diversity increased temporally until it reached a mature and stable state at eight weeks of age.

Shifts in intestinal microbiota of avian species may induce a cascade of reactions which result in reduced nutrient digestibility and impaired intestinal barrier function, increasing the risk of bacterial translocation, and inflammatory responses (Teirlynck et al., Reference TEIRLYNCK, GUSSEM, DEWULF, HAESEBROUCK, DUCATELLE and VAN IMMERSEEL2011). Typically, the syndrome is observed in birds between 20 and 30 days of age, and is characterised by symptoms including wet, greasy droppings with undigested feed particles, dirty feathers, reduced physical activity, increased water intake, and decreased feed intake and feed conversion. It has been hypothesised that both non-infectious and infectious factors are responsible for this syndrome. Non-infectious factors can be observed as feed interruptions or dietary changes, nutritional imbalance, dietary stressors such as non-starch polysaccharides (NSP), management issues, genetic factors, enzymatic dysfunction, and mycotoxins. Infectious agents thought to play a role in the development of dysbacteriosis can be from coccidia, C. perfringens and other unidentified bacterial infections which produce toxic metabolites. Despite this syndromes importance, there is a large knowledge gap and poor consensus of its aetiology, leading to incomplete characterisation. Teirlynck et al. (Reference TEIRLYNCK, GUSSEM, DEWULF, HAESEBROUCK, DUCATELLE and VAN IMMERSEEL2011) attempted to address this by researching the histological changes which occur in the intestinal mucosa in broilers diagnosed with dysbacteriosis. Results identified that dysbacteriosis coincided with an inflammatory reaction in the intestinal mucosa, causing weakening villus structures, an increase in T-lymphocyte penetration of intestinal mucosa and larger goblet cells.

Viruses and runting and stunting syndrome

Although it was first described in the 1940's, the exact aetiology of runting and stunting syndrome (RSS) remains unknown. Therefore, descriptive terms such as malabsorption syndrome and broiler stunting syndrome, among others, are relied upon for the identification of this multifactorial disease (Kang et al., Reference KANG, EL-GAZZAR, SELLERS, DOREA, WILLIAMS, KIM, COLLETT and MUNDT2012; Oamar et al., Reference OAMAR, ASLAM and JAHAN2013). Small, round and non-enveloped viruses are believed to the most likely etiologic agents (Kang et al., Reference KANG, EL-GAZZAR, SELLERS, DOREA, WILLIAMS, KIM, COLLETT and MUNDT2012). Efforts to address this knowledge gap have resulted in the isolation of reovirus, rotavirus, parvovirus, and astrovirus in various combinations from clinically infected chickens (Kang et al., Reference KANG, EL-GAZZAR, SELLERS, DOREA, WILLIAMS, KIM, COLLETT and MUNDT2012). These combinations of different infectious agents may give rise to a spectrum of clinical signs reported for this syndrome (Guy, Reference GUY1998).

Rotavirus infections in avian species are known to vary from severe to subclinical (Guy, Reference GUY1998). Economic losses as a result of RSS are caused by decreased flock uniformity and body weight, increased mortality and feed conversation efficiency and increased susceptibility to secondary diseases (Oamar et al., 2013). Various histopathological changes which interfere with normal digestive processes were observed by Oamar et al. (Reference OAMAR, ASLAM and JAHAN2013) in broiler chickens diagnosed with RSS, including: lesions, degradation of villi, crypts, and epithelial cells. Mucosal damage and resulting malabsorption leading to nutritional deficiencies are likely factors responsible for common clinical impacts associated with RSS. This is associated with growth retardation, ruffled feathers, and diarrhoea (Kang et al., Reference KANG, EL-GAZZAR, SELLERS, DOREA, WILLIAMS, KIM, COLLETT and MUNDT2012). Mucosal damage induced by viral infection may present an opportunity for entry of pathogens including E. coli and Salmonella spp. (Guy, Reference GUY1998).

Economic impacts

The success of the broiler industry worldwide relies on effective feed conversion (Cooper et al., Reference COOPER, SONGER and UZAL2013). The presence of pathogenic organisms and occurrence of enteric disease can cause competition for nutrients, intestinal mucosal damage, and a subsequent reduction in surface area for nutrient absorption, increased susceptibility to other diseases, immune system stimulation and resulting diversion of nutrients, and other effects which lead to reduced performance and feed conversion efficiency (Yegani and Korver. 2008). As feed is the major component of production cost (up to 70%) in broiler production, poor feed efficiency translates into large economic losses. In addition, costs associated with morbidity and mortality, decreased weight gain, increased time to slaughter, condemnations at slaughter and preventative and treatment costs associated with enteric disease contributes to economic losses. Van der Sluis (Reference VAN DER SLUIS2000) estimated that the occurrence of NE results in a loss of $0.05 per bird. Similarly, a survey by Lovland and Kaldhusal (2001) estimated that subclinical clostridial disease lead to losses of $0.05 per bird annually, although this was likely a gross underestimation due to uncertainties in diagnosing mild forms of infection. Skinner et al. (Reference SKINNER, BAUER, YOUNG, PAULING and WILSON2010) estimated that subclinical NE results in a loss to producers ranging from $878 - $1481 USD per flock. An original economic model performed by Williams (Reference WILLIAMS1999) determined that the loss from coccidiosis to the UK poultry industry in 1995 was £38,588,795, of which 98.1% was estimated to involve broiler chickens. For losses in broilers, 80.6% was estimated to be due to effects of coccidiosis on mortality, weight gain, and feed conversion, and 17.5% due to the cost of chemoprophylaxis and therapy.

To date, no economic models have been developed to assess the economic impact of coccidiosis on the poultry industry in North America, or on a global scale due to complexities identified by Williams (Reference WILLIAMS1999). A thorough understanding of the economic impact of viral induced gastrointestinal disease in poultry is lacking (Guy, Reference GUY1998). It is likely that viral infections negatively impact production, with the greatest proportion of economic losses attributed to reduced gain, feed efficiency, and flock uniformity (Guy, Reference GUY1998). Administration of antimicrobials and alternative products to broiler chickens have been demonstrated to alleviate symptoms associated with intestinal health associated diseases, thereby minimising the economic impacts of enteric diseases to the broiler industry. Assessing the economic impact of enteric illness in a broiler flock is an important component of the diagnostic procedure of enteric disease in poultry flocks.

Diagnosis and prevention

Differential diagnosis of enteric diseases in poultry is important when suitable treatment options and control recommendations may differ amongst them (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005; Cooper et al., Reference COOPER, SONGER and UZAL2013). Diagnosis should be based on several criteria (Cooper et al., Reference COOPER, SONGER and UZAL2013). Initially, a thorough history of the affected flock should be collected, including past disease occurrences, flock condemnation, and performance measures (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). A careful assessment of the individual flock health status should be performed, involving an evaluation of clinical signs, such as the occurrence of diarrhoea, huddling, anorexia, feed intake, and performance measures. Evaluation of litter quality is a useful indicator for identifying diarrhoea (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). If a severe clinical form of a named enteric disease is present, it may be possible to obtain a differential diagnosis based on clinical features. However, diagnosis of clostridial and subclinical forms of enteric disease may be challenging (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005; Cooper et al., Reference COOPER, SONGER and UZAL2013). For example, many clostridial species can be normal inhabitants of the poultry GIT, and therefore detection of these species and/or their toxins is not useful for confirming disease, as these have both been previously found in healthy birds (Cooper et al., Reference COOPER, SONGER and UZAL2013). Subclinical forms of enteric disease are challenging to differentiate due to non-specific nature of presenting clinical signs and lesions (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). Additionally, dysbacteriosis has proven difficult to diagnose due to incomplete characterisation of this syndrome to date (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). Necropsies and histology may further differentiate enteric disease through gross and microscopic lesions. Cultures to detect named diseases can then be performed to verify presence of disease depending on results from earlier steps. To diagnose emerging microbial ecology issues, a variety of microbial technologies and laboratory tests should be utilised.

Management of intestinal health should be the focus of control of enteric disease, including appropriate general management practices to prevent infectious gastrointestinal disease. However, when prevention methods fail, early detection and treatment are necessary (Wilson et al., Reference WILSON, TICE, BRASH and St. HILAIRE2005). If there is evidence of a named disease present in a flock, known risk factors for that disease should be immediately eliminated. When a subclinical form of enteric disease is present, what is known about the severe form of the disease should be extrapolated to controlling and treating the mild form of disease. Prudent use of antimicrobials or alternatives with known efficacy can then be used to control an outbreak of a gastrointestinal disease. Alternatively, emerging, non-traditional therapies can be used to prevent and/or resolve intestinal health issues while avoiding issues of antimicrobial resistance and residues.