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. 2024 Feb 7;103(4):103500. doi: 10.1016/j.psj.2024.103500

Unraveling frontiers in poultry health (part 1) – Mitigating economically important viral and bacterial diseases in commercial Chicken and Turkey production

Yewande O Fasina *,1, David L Suarez †, George D Ritter ‡, Elise C Gerken §, Yuhua Z Farnell #, Ross Wolfenden ǁǁ, Billy Hargis
PMCID: PMC10907857  PMID: 38417326

Abstract

This symposium offered up-to-date perspectives on field experiences and the latest research on significant viral and bacterial diseases affecting poultry. A highlight was the discussion on the use of enteroids as advanced in vitro models for exploring disease pathogenesis. Outcomes of this symposium included identifying the urgent need to improve the prevention and control of avian influenza by focusing research on vaccine effectiveness. In this regard, efforts should focus on enhancing the relatedness of vaccine antigen to the field (challenge) virus strain and improving immunogenicity. It was also revealed that gangrenous dermatitis could be controlled through withholding or restricting the administration of ionophores during broiler life cycle, and that administration of microscopic polymer beads (gel) based-live coccidia vaccines to chicks could be used to reduce necrotic enteritis-induced mortality. It was emphasized that effective diagnosis of re-emerging Turkey diseases (such as blackhead, fowl cholera, and coccidiosis) and emerging Turkey diseases such as reoviral hepatitis, reoviral arthritis, Ornithobacterium rhinotracheale infection, and strepticemia require complementarity between investigative research approaches and production Veterinarian field approaches. Lastly, it was determined that the development of a variety of functionally-specific enteroids would expedite the delineation of enteric pathogen mechanisms and the identification of novel vaccine adjuvants.

Key words: highly pathogenic Avian influenza, gangrenous dermatitis, necrotic enteritis, re-emerging Turkey disease, Avian enteroids

HIGHLY PATHOGENIC AVIAN INFLUENZA IN THE AMERICAS. IS IT TIME FOR A PARADIGM SHIFT IN CONTROL?

David Suarez

Avian influenza is an economically important disease that plagues poultry species, and is caused by viruses that belong to the species Alphainfluenzavirus influenzae (International Committee on Taxonomy of Viruses, 2022; Carnegie et al., 2023). Clinical signs of the disease typically include severe depression, neurological signs, and swollen heads which frequently culminate in a high mortality (up to 100%) within 36 to 48 h postinfection (Spackman, 2020; Swayne, 2020).

The current outbreak of goose/Guangdong H5 highly pathogenic is unprecedented in both geographic scope and the endemic nature of the virus in wild birds (Youk et al., 2023). Our current control strategy in poultry continues to be to rapidly diagnosis outbreaks and to rapidly respond through depopulation programs to limit spread. This approach has been largely effective with little evidence of farm to farm spread, but because of the widely endemic nature in wild birds, the number of outbreaks in both commercial and backyard poultry has exceeded over 950 affected premises as of November, 2023. The number of cases in commercial poultry have decreased in 2023 compared to 2022, but outbreaks continue in backyard poultry and wild birds. It is unclear why a decrease in cases is occurring in both poultry and wild birds, but increased biosecurity hopefully is contributing to that reduction in poultry. Experimental studies of recent outbreak viruses, particularly in comparison with the 2014-15 HPAI outbreak, shows that the current viruses are more infectious in chickens and Turkeys. The virus transmitted in Turkeys more efficiently than it did in chickens. Because of the cost of the test and eradication approach, interest in vaccination continues to grow. Vaccine use is not approved in the U.S. because of the negative ramifications to trade, but we do have several vaccines that are licensed for potential use. These include reverse genetics adjuvanted inactivated vaccines, Turkey herpes virus vectored vaccines, and an alphavirus vectored RNA particle vaccine. Although all of these vaccines are expected to protect against clinical disease, concern about the antigenic relatedness of available vaccines in protection against viral shedding remains. A recently completed study shows that matching the vaccine to the current outbreak strain provides the best protection, based on virus shedding (Mo et al., 2023; Spackman et al., 2023). Despite the evidence for protection from vaccines, there is reluctance to use this option because it will affect trade of poultry and poultry products (Radin et al., 2017; Swayne et al., 2017). Efforts to improve our ability to differentiate vaccinated from vaccinated and exposed birds (DIVA) strategy are ongoing to mitigate trade concerns (Suarez, 2012). Because of the importance of U.S. exports, the future of control remains uncertain.

GANGRENOUS DERMATITIS AND NECROTIC ENTERITIS: APPLIED RESEARCH AND PRACTICAL INTERVENTIONS IN COMMERCIAL BROILERS

Don Ritter

Gangrenous dermatitis (GD) and Necrotic enteritis (NE) are significant disease challenges in commercial broilers despite many years of basic and applied research into pathogenesis and control methods. Economic losses from these conditions are high, especially in broilers raised for No Antibiotics Ever (NAE) marketing programs (Fancher et al., 2020, Fancher et al., 2021). Field experiences and perspectives from broiler production veterinarians related to practical ways to reduce losses from these diseases may shed light on possible pathways for new research opportunities.

GD is primarily a bacterial translocation disease of chickens and Turkeys caused by Clostridium perfringens (CP) and Clostridium septicum (CS, Popoff et al., 2016; Prescott et al., 2016). In broiler chickens the disease occurs from 35 to 50 d of age characterized by low morbidity and high mortality in affected flocks. GD is correctly classified as a “gut disease” of poultry resulting from a bloom in numbers of CP/CS in the gut lumen with subsequent translocation from the gut to target tissues including muscle, skin, and liver. GD has an “inside – out” pathogenesis (Gornatti-Churria et al., 2018). Bacterial toxins are then produced at target sites which quickly kill the affected birds (Criollo et al., 2023). To demonstrate this effect under field conditions, the intestinal microflora of live birds with clinical GD were compared to microflora from clinically normal birds from the same broiler house. Over 30 pairs of birds were compared in this manner and all pairs showed an identical microflora dichotomy: clinical GD birds had high levels of CP and Escherichia coli and low levels of Lactobacillus bacteria compared to bacterial community patterns observed in clinically normal birds. Antibiotics, including ionophores, create powerful shifts in gut microflora patterns (Zou et al., 2022). Sequential analysis of microflora patterns showed that such shifts occur within 7 d of feeding the antibiotic. Conversely, chemical coccidiostats do not have antibacterial properties and thus do not disturb gut bacterial communities. Lu et al. (2008) demonstrated that the gut microflora community matures over time, and that ionophores greatly increase the relative abundance of Clostridium species (both good and bad) in the gut (Figure 1).

Figure 1.

Figure 1

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Effects of different diets on GIT bacterial community. Adapted from Lu et al. (2008).

Broiler production veterinarians have noted that GD has a seasonal pattern of severity, with peak incidence occurring in May and lowest incidence in October. This is illustrated in a GD disease tracking graph from a Delmarva broiler producer for 2005. This graph shows the number of clinically diagnosed GD houses per week when a continuous ionophore program was fed from 0 to 36 d for the entire year (Figure 2). Based on these learnings, it was hypothesized that using ionophores in later feeds during the age when clinical dermatitis occurred may increase the incidence of GD in a broiler complex located in a region with naturally high clostridial challenge such as Delmarva. This theory was tested the following year in a Delmarva broiler complex when half of the birds were fed a STR: Chemical GRO: Ionophore coccidial control program and half of the birds were fed the same products in reverse order: STR: Ionophore GRO: Chemical. The effect on the incidence of GD was striking, and both feed mills were then changed to the ionophore/chemical program which greatly reduced the overall incidence of GD observed (Figure 3). This strategy proved to be increasingly successful when later in the 2000s, coccidial vaccine programs were added to the annual cocci control program rotation in the Delmarva complex to almost eliminate use of ionophores, reducing annual levels of observed GD cases even further. To reduce the risk of GD, broilers should either not receive ionophores at all, or not consume them after 28 d of age. This is also true if ionophores are used in conjunction with live coccidial vaccines as part of a bio-shuttle program – the ionophore inclusion should stop at 28 d to minimize GD incidence.

Figure 2.

Figure 2

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Gangrenous dermatitis disease tracking graph from a Delmarva broiler producer for 2005.

Figure 3.

Figure 3

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Evaluation of the efficacy of 2 feed mill coccidial control programs for the control of Gangrenous dermatitis in a commercial broiler flock.

NE is caused when Clostridium pefringens (CP) numbers bloom in the midgut and produce toxins that lead to death. Cycling of Eimeria coccidial oocysts, especially E. maxima (EMx), causes intestinal damage and excess mucus production that provides an ideal environment for CP overgrowth (Fasina and Lillehoj, 2019; Fathima et al., 2022; Kulkarni et al., 2022). Thus, most cases of both subclinical and clinical NE in broilers are triggered by reproduction cycles of EMx, and controlling this coccidial pathogen is critical to successful control of NE. Broiler producers struggle with controlling NE more often when using live oocyst coccidial vaccines to control coccidiosis, especially when raising broilers in No Antibiotics Ever (NAE) marketing programs. This is because of the unpredictable and uneven cycling of EMx due to the uneven application of coccidial vaccines of varying viability in the hatchery.

A series of applied research experiments were conducted in a Delmarva complex over several years to investigate this problem. Various dose and administration methods of coccidial vaccination were compared. The initial experiment was designed to find out which birds died from NE in the field: were the dead birds underdosed or overdosed with cocci vaccine? Ten percent of the birds in several broiler houses received either no coccidial vaccine or a full dose via oral gavage, while the balance of the birds received coccidial vaccine in ovo. The resulting differences in natural NE mortality revealed that unvaccinated chicks died at 3 to 8 times the rate of fully vaccinated chicks. Subsequent trials then focused on improving hatchery application of live coccidial vaccines to reduce the variability in EMx cycling to reduce NE risk. After many experiments, it was concluded that applying coccidial vaccine in a 2-phase gel resulted in the most coverage and individual bird volume uptake versus other methods. When compared to the more common application method of coarse water spray, it was demonstrated using microscopic polymer beads as a proxy for oocysts that chicks receiving the same dose of beads via 2-phase gel consumed 7 times more beads (Figure 4). The gel method of hatchery vaccine administration successfully reduced the incidence of NE and improved adjusted feed conversion when using live coccidial vaccines in several commercial broiler complexes. Lastly, the genetic relatedness of CP isolates from cases of GD or NE was studied. It was determined that CP isolates are diverse but group together according to disease condition and geographic origin (Figure 5).

Figure 4.

Figure 4

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Comparative efficacy of live coccidia vaccine administered as coarse water spray or as microscopic polymer beads (in a 2-phase gel) in a commercial broiler flock.

Figure 5.

Figure 5

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Genetic relatedness of C. perfringens isolates from cases of Gangrenous dermatitis or Necrotic enteritis.

EMERGING AND RE-EMERGING DISEASES OF COMMERCIAL TURKEYS

Elise C. Gerken

The emerging and re-emerging diseases currently facing the commercial Turkey industry in the USA were explored. In addition, the field veterinarian's approach to identifying and diagnosing emerging and re-emerging diseases was discussed. Furthermore, the impact of changes in management and housing systems on disease progression and prevalence over the years were highlighted.

In the United States, production veterinarians in the Turkey industry are responsible for the health and welfare of millions of commercial hens or toms annually. Because of the distribution of responsibility, these veterinarians focus their time trying to diagnose disease and identify causes and treatments as efficiently as possible to maintain performance and cost as well as ensuring wholesome products reach consumers. Emerging and re-emerging diseases are inherent to animal agriculture and are often identified in commercial Turkey production. While common diseases occur commonly and the ability to diagnose them quickly provides the speed and efficiency required to maintain performance, it is critical that as Turkey veterinarians, we are able to keep an open mind allowing for discovery of these rarer and newly emerging diseases. It is important to understand that over history, the bird has changed genetically, the diets have improved, and management systems have been altered, all of which provide an excellent platform for emergence of new diseases or recrudescence of older less frequently seen diseases. History of diseases in Turkey production as well as the diagnostic approach, and other factors influencing the changing landscape of diseases in commercial Turkey production in the USA were discussed. Supporting evidence found in literature was used to confirm when certain diseases were first discovered as well as progression of diseases will help supplement this discussion.

The type of Turkey production system utilized directly influences disease pressures which creates opportunities for emerging and re-emerging diseases in commercial Turkeys. Often consumers drive the housing systems utilized and this leads to changes in disease pressures. The reverse is sometimes the case when diseases are the reasoning behind shifts in production systems. An example of this dynamics was when commercial Turkeys were traditionally reared outdoors in ranges, and this consequently led to a high prevalence of diseases such as blackhead and fowl cholera. In response, the Turkey industry moved these birds indoors to reduce exposure to these diseases. However, increasing consumer demand in recent years for birds to be raised organically or without antibiotics has resulted in an increased prevalence of certain diseases such as coccidiosis and secondary enteric challenges. Furthermore, relatively newly diagnosed (i.e., emerging) diseases have been reported in the Turkey industry across the USA. These diseases in part include reoviral hepatitis, reoviral arthritis, Ornithobacterium rhinotracheale infection, and strepticemia. It is critical for the research approach and the field approach to be in synch and complimentary to one another in order to effectively and efficiently diagnose newly emerging pathogens in commercial poultry production.

ENTEROIDS AS A NOVEL TOOL FOR STUDYING THE AVIAN INTESTINAL SYSTEM

Yuhua Farnell

The avian intestine consists of villi and crypts and is a critical site for food digestion, nutrient absorption, and immune response. Intestinal crypts, which are invaginations at the base of villi, host crucial intestinal stem cells and Paneth cells (Cheng and Leblond, 1974). The crypt's spatial arrangement protects stem cells from the direct connection to the luminal environment containing digestive enzymes and microbial products (Kaiko et al., 2016; Gehart and Clevers, 2019). In the chicken, cells at the villus apex and are sloughed off into the intestinal lumen after 3 to 4 d (Uni et al., 2000). Stem cells within the crypt continuously differentiate into progenitor cells, replenishing worn-out matured cells in the villus. These stem cells have been used to establish the 3-dimensional (3D) multicellular intestinal organoids, also known as the enteroids, which recapitulate intestine epithelial structure and function and have been widely used for studying intestinal physiology, pathophysiology, molecular mechanisms of host-pathogen interactions and intestinal disease in mammals. Enteroids are defined as a mimic of an intestinal organ following 3 main capabilities, exhibiting multiple organ-specific cell types, recapitulating organ-specific functions, and organizing into a structure like an organ in vivo (Finkbeiner and Spence, 2013).

Recently studies on chicken enteroids were reported globally (Pierzchalska et al., 2012, 2017, Pierzchalska et al., 2019a, Pierzchalska et al., 2019b; Panek et al., 2018; Nash et al., 2021; Orr et al., 2021; Oost et al., 2022; Zhao et al., 2022). However, there remains a need to develop long-term cultures of avian enteroid biobank from various intestinal sections such as the duodenum, jejunum, ileum, and cecum, for comprehensive poultry research (Zhao et al., 2022). Stem cells isolated from the crypts of both broiler and layer chickens, were embedded in a basement membrane matrix and cultured using a custom-formulated enteroid growth media (Zhao et al.,2022). These crypt-derived enteroids were cultivated to form 3-dimensional sphere-like structures, which were successfully maintained and passaged up to 28 times. Additionally, enteroids that were cryopreserved for demonstrated the capability to continue growing and expanding. The standard techniques such as reverse transcription (RT)-PCR and immunoblotting were employed to characterize enteroids. These methods identified the gene marker indicative of specific cell types (E-cadherin for epithelial cells, leucine-rich repeat-containing G protein-coupled receptor 5 for stem cells, chromogranin A for enteroendocrine cells, lysozyme for Paneth cells, and mucin for goblet cells), thereby confirming the presence of a diverse array of intestinal epithelial cells within the enteroids.

Enteroid technology has already been developed over the past decade and is extensively utilized in mammalian studies to explore intestinal physiology (Schwank et al., 2013; Middendorp et al., 2014), facilitate understanding of cellular crosstalk (Sato et al., 2011), and perform functional assay (Dekkers et al., 2013). Its vital role extends to disease modeling, drug screening, and tissue transplantation (Yui et al., 2012; Drost and Clevers, 2017). Finkbeiner et al. (2012) pioneered using human enteroids to elucidate rotavirus infection mechanisms. Subsequent studies have broadened this research to enteroids derived from various mammalian species, examining infections by bacteria, parasites, and viruses.

Avian enteroids have a wide range of potential applications. These models are particularly valuable for understanding and managing enteric infections, enabling the development of more effective therapeutic and preventative strategies. They are also integral to nutritional research for improving avian gut health. Researchers can tailor diets to enhance poultry gut health by analyzing how nutrients are absorbed and metabolized. Additionally, enteroids provide a unique model for examining interactions among the gut microbiota, intestinal epithelium, and immune cells, essential for maintaining animal gastrointestinal health and ensuring the safety of animal food products. They play a crucial role in enhancing vaccine research by providing detailed insights into gut immunity, interactions between pathogens and the host's intestinal system, and the effects of vaccines on gut health, thereby significantly aiding in developing more effective veterinary vaccines. The use of avian enteroids, therefore, is pivotal in advancing our understanding of animal gastrointestinal physiology and pathology. Their role in enhancing the efficacy of vaccines, improving animal health, and ensuring food safety underscores their significance in veterinary and nutritional research.

CONCLUSIONS

Prevention and control of avian influenza in poultry flocks continue to be a priority for the poultry industry. Although rapid diagnosis of outbreaks and rapid response through depopulation continue to limit the spread of the virus, this symposium has brought to light the dire need to invest in research geared towards optimizing vaccine efficacy. In particular, emphasis should be placed on enhancing the relatedness of vaccine antigen and the field (challenge) virus strain, and ensuring that critical viral epitopes are incorporated into the vaccine formulation to enhance immunogenicity. Clostridial diseases, namely GD and NE constitute an economic burden of up to a tune of billions of dollars annually in the global poultry industry. A relatively new information deduced from this symposium was that the incidence of gangrenous dermatitis could be controlled through withholding or restrictive administration of ionophores during broiler life cycle. It was also highlighted that NE-induced mortality could be reduced by administering coccidia vaccines to chicks using microscopic polymer beads in a 2-phase gel, compared to administration by coarse water spray method. It was also determined that CP isolates are diverse but group together according to disease condition and geographic origin.

In the Turkey industry, the type of housing and rearing system influences the incidence of re-emerging diseases such as blackhead, fowl cholera, and coccidiosis. Emerging diseases of Turkey discussed included reoviral hepatitis, reoviral arthritis, Ornithobacterium rhinotracheale infection, and strepticemia. It was determined that effective diagnosis of emerging pathogens require complementarity between investigative research approaches and production Veterinarian field approaches. The possibility of using enteroids as ex-vivo models of the bird's intestinal epithelium for disease modeling, studying host-pathogen interactions, and drug screening was discussed. It was highlighted that the development of a variety of functionally-specific enteroids (e.g., goblet cell-rich enteroids) could expedite research geared toward the delineation of enteric pathogen mechanisms and the identification of novel vaccine adjuvants.

DISCLOSURES

Yewande Fasina reports financial support was provided by Poultry Science Association. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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