by Ajay Bhoyar, Global Technical Manager, EW Nutrition

Gut health is critical for profitable poultry production, as the gastrointestinal tract (GIT) plays a dual role in nutrient digestion and absorption while serving as a crucial defense against pathogens. A healthy gut enables efficient feed conversion, robust immune function, and resilience against diseases, reducing reliance on preventive and therapeutic antibiotics. Optimum gut health has become increasingly important in poultry production to combat antimicrobial resistance (AMR), a pressing global challenge threatening animal agriculture and public health.

AMR arises when bacteria develop antibiotic resistance, often due to overuse or misuse in human and animal settings. Predictive models suggest that by 2050, AMR could result in 10 million annual deaths and a 2.0%–3.5% reduction in global gross domestic production, amounting to economic losses between 60 and 100 trillion USD. In poultry, AMR compromises flock health, leading to higher mortality, reduced growth performance, and elevated treatment costs, directly impacting profitability. Additionally, resistant pathogens increase the risk of zoonotic disease transfer, posing serious food safety concerns.

Stricter regulations and rising consumer demand for antibiotic-free poultry products drive a shift toward sustainable, antibiotic-free production systems. However, A lack of understanding about strategies to replace AMU and their effectiveness under field conditions hampers change in farming practices (Afonso et al., 2024). Addressing AMR requires a holistic approach, encompassing enhanced biosecurity, innovative health-promoting strategies, and sustainable management practices. This paper explores practical dietary interventions to support poultry gut health while reducing dependency on antimicrobials, offering solutions for the long-term sustainability of poultry production.

Gut Mediated Immunity in Chickens

The gut is a critical component of the immune system, as it is the first line of defense against pathogens that enter the body through the digestive system. Chickens have a specialized immune system in the gut, known as gut-associated lymphoid tissue (GALT), which helps to identify and respond to potential pathogens. The GALT includes Peyer’s patches, clusters of immune cells in the gut wall, and the gut-associated lymphocytes (GALs) found throughout the gut. These immune cells recognize and respond to pathogens that enter the gut.

The gut-mediated immune response in chickens involves several mechanisms, including activating immune cells, producing antibodies, and releasing inflammatory mediators. GALT and GALs play a crucial role in this response by identifying and responding to pathogens and activating other immune cells to help fight off the infection.

The gut microbiome is a diverse community of microorganisms that live in the gut. These microorganisms can significantly impact the immune response. Certain beneficial bacteria, for example, can help stimulate the immune response and protect the gut from pathogens.

Overall, the gut microbiome, GALT, and GALs work together to create an environment hostile to pathogens while supporting the growth and health of beneficial microorganisms.

Key Factors Affecting Poultry Gut Health

The key factors affecting broiler gut health can be summarized as follows:

1. Early gut development: Gut-associated immunity responds to early feeding and dietary nutrients and is critical for protecting against exogenous organisms during the first week of life post-hatch.
2. Feed and Water Quality: The form, type, and quality of feed provided to broilers can significantly impact their gut health. Consistently available cool and hygienic drinking water is crucial for optimum production performance.
3. Stressors: Stressful conditions, such as high environmental temperatures or poor ventilation, can lead to an imbalance in the gut microbiome and an increased risk of disease.
4. Infections and medications: Exposure to pathogens or other harmful bacteria can disrupt the gut microbiome and lead to gut health issues. A robust immune system is important for maintaining gut health, as it helps to prevent the overgrowth of harmful bacteria and promote the growth of beneficial bacteria.
5. Biosecurity: Keeping the poultry environment clean and free of pathogens is crucial for maintaining gut health, as bacteria and other pathogens can quickly spread and disrupt the gut microbiome.
6. Management practices: Best practices, including proper litter management, can help maintain gut health and prevent gut-related issues.

Dietary Interventions for Optimum Gut Health

Gut health means the absence of gastrointestinal disease, the effective digestion and absorption of feed, and a normal and well-established microbiota (Bischoff, 2011). Various dietary measures can be taken to support the healthy functioning of the GIT and host defense. Water and feed safety and quality, feeding management, the form the feed is provided in (e.g., pellets), the composition of the diet, and the use of various feed additives are all tools that can be used to support health (Smits et al., 2021).

Various gut health-supporting feed additives, including organic acids, probiotics, prebiotics, phytochemicals/essential oils, etc., in combination or alone, have been explored as an alternative to antimicrobials in animal production. There were differences in the impacts of the strategies between and within species; this highlights the absence of a ‘one-size-fits-all’ solution. Nevertheless, some options seem more promising than others, as their impacts were consistently equivalent or positive when compared with animal performance using antimicrobials (Afonso et al., 2024). Including insoluble fibers, toxin binders, exogenous enzymes, and antioxidants in the feed formulations also play a crucial role in gut health optimization, which goes beyond their primary functions to combat AMR challenges.

Fig. 1: Multifactorial approach to gut health management in reduced antimicrobial use

Organic Acids

The digestive process extensively includes microbial fermentation, and as a result, organic acids are commonly produced by beneficial bacteria in the crop, intestines, and ceca (Huyghebaert et al., 2010). Organic acids’ inclusion in the poultry diet can improve growth performance due to improved gut health, increased endogenous digestive enzyme secretion and activity, and nutrient digestibility. Butyrate is highly bioactive in GIT. It increases the proliferation of enterocytes, promotes mucus secretion, and may have anti-inflammatory properties (Bedford and Gong, 2018; Canani et al., 2011; Hamer et al., 2008). These effects suggest that it supports mucosal barrier function. Butyrate is becoming a commonly used ingredient in diets to promote GIT health.

Including organic acids in the feed can decontaminate feed and potentially reduce enteric pathogens in poultry. Alternately, the formaldehyde treatment of feed is highly effective at a relatively low cost (Jones, 2011; Wales, Allen, and Davies, 2010).

Organic acids like formic and citric acid are also used in poultry drinking water to lower the microbial count by lowering the water’s pH and preventing/removing biofilms in the water lines. By ensuring feed and water hygiene, producers can minimize pathogen exposure, enhance bird health, and significantly reduce their reliance on antibiotics.

Probiotics, Postbiotics, Prebiotics and Synbiotics

Probiotics and prebiotics have drawn considerable attention to optimizing gut health in animal feeds. Probiotic supplementation could have the following effects: (1) modification of the intestinal microbiota, (2) stimulation of the immune system, (3) reduction in inflammatory reactions, (4) prevention of pathogen colonization, (5) enhancement of growth performance, (6) alteration of the ileal digestibility and total tract apparent digestibility coefficient, and (7) decrease in ammonia and urea excretion (Jha et al., 2020). Certain Lactobacilli or Enterococci species may be used with newly hatched or newborn animals; single or multi-strain starter cultures can be used to steer the initial microbiota in a desired direction (Liao and Nyachoti, 2017). Apart from using probiotics in feed and drinking water, probiotic preparations can be sprayed on day-old chicks in the hatchery or immediately after placement in the brooding house. This way, the probiotic strains/beneficial bacteria gain access to the gut at the earliest possible time (early seeding). Postbiotics are bioactive compounds produced by probiotics during fermentation, such as short-chain fatty acids, peptides, and bacterial cell wall components. Unlike live probiotics, postbiotics are stable, safer, and provide consistent health benefits.

Prebiotics like mannan-oligosaccharides (MOS), inulin, and its hydrolysate (fructo-oligosaccharides: FOS) play an important role in modulating intestinal microflora and potential immune response. Prebiotics reduce pathogen colonization in poultry and promote selective stimulation of beneficial bacterial species. Synbiotics are a combination of probiotics and prebiotics. This synergistic approach offers dual benefits by promoting the growth of beneficial bacteria and directly combating pathogens.

Dietary Fibers (DF)

The water-insoluble fibers are regarded as functional nutrients because of their ability to escape digestion and modulate nutrient digestion. A moderate level of insoluble fiber in poultry diets may increase chyme retention time in the upper part of the GIT, stimulating gizzard development and endogenous enzyme production, improving the digestibility of starch, lipids, and other dietary components (Mateos et al., 2012). The insoluble DF, when used in amounts between 3–5% in the diet, could have beneficial effects on intestinal development and nutrient digestibility.

Dietary fibers influence the development of the gizzard in poultry birds. A well-developed gizzard is a must for good gut health. Jiménez-Moreno & Mateos (2012) noted that coarse fiber particles are selectively retained in the gizzard, ensuring a complete grinding and a well-regulated feed flow. Secretion of digestive juices regulates GIT motility and feed intake. Including insoluble fibers in adequate amounts improves the gizzard function and stimulates HCl production in the proventriculus, thus helping control gut pathogens.

Toxin Risk Management

Mycotoxins may have a detrimental impact on the mucosal barrier function in animals (Akbari et al., 2017; Antonissen et al., 2015; Basso, Gomes and Bracarense, 2013; Pierron, Alassane-Kpembi and Oswald, 2016). Mycotoxins like Aflatoxin B1, Ochratoxin A, and deoxynivalenol (DON) not only suppress immune responses but also induce inflammation and even increase susceptibility to pathogens (Yuhang et al., 2023). To avoid intestinal health problems, poultry producers need to emphasize avoiding levels of mycotoxins in feedstuffs and rancid fats that exceed recommended limits (Murugesan et al., 2015; Grenier and Applegate, 2013).

Bacterial lipopolysaccharides (LPS), also known as endotoxins, are the main components of the outer membrane of all Gram-negative bacteria and are essential for their survival. In stress situations, the intestinal barrier function is impaired, allowing the passage of endotoxins into the bloodstream. When the immune system detects LPS, inflammation sets in and results in adverse changes in gut epithelial structure and functionality. Dietary Intervention to bind these endotoxins in the GIT can help mitigate the negative impact of LPS on animals. Given this, toxin risk management with an appropriate binding agent able to control both mycotoxins and endotoxins appears to be a promising strategy for reducing their adverse effects. Further, adding antioxidants and mycotoxin binders to feed can reduce the effects of mycotoxins and peroxides and is more necessary in ABF programs (Yegani and Korver, 2008).

Essential oils/Phytomolecules

Essential oils (EOs) are important aromatic components of herbs and spices and are used as natural alternatives for replacing antibiotic growth promoters (AGPs) in poultry feed. The beneficial effects of EOs include appetite stimulation, improvement of enzyme secretion related to food digestion, and immune response activation (Krishan and Narang, 2014)

Essential oils (EOs), raw extracts from plants (flowers, leaves, roots, fruit, etc.), are an unpurified mix of different phytomolecules. The raw extract from Oregano is a mix of various phytomolecules (Terpenoids) like carvacrol, thymol and p-cymene. Whereas the phytomolecules are active ingredients of essential oils or other plant materials. Phytomolecule is clearly defined as one active compound.

These botanicals have received increased attention as possible growth performance enhancers for animals in the last decade via their beneficial influence on lipid metabolism, and antimicrobial and antioxidant properties (Botsoglou et al., 2002), ability to stimulate digestion (Hernandez et al., 2004), immune enhancing activity, and anti-inflammatory potential (Acamovic and Brooker, 2005). Many studies have been reported on supplementing poultry diets with some essential oils that enhanced weight gain, improved carcass quality, and reduced mortality rates (Williams and Losa, 2001). The use of some specific EO blends has been shown to have efficacy towards reducing the colonization and proliferation of Clostridium perfringens and controlling coccidia infection and, consequently, may help to reduce necrotic enteritis (Guo et al., 2004; Mitsch et al., 2004; Oviedo-Rondón et al., 2005, 2006a, 2010).

Antimicrobial properties of phytomolecules hinder the growth of potential pathogens. Thymol, eugenol, and carvacrol are structurally similar and have been proven to exert synergistic or additive antimicrobial effects when combined at lower concentrations (Bassolé and Juliani, 2012). In in-vivo studies, essential oils used either individually or in combination have shown clear growth inhibition of Clostridium perfringens and E. coli in the hindgut and ameliorated intestinal lesions and weight loss than the challenged control birds (Jamroz et al., 2006; Jerzsele et al., 2012; Mitsch et al., 2004). One well-known mechanism of antibacterial activity is linked to their hydrophobicity, which disrupts the permeability of cell membranes and cell homeostasis with the consequence of loss of cellular components, influx of other substances, or even cell death (Brenes and Roura, 2010; Solórzano-Santos and Miranda-Novales, 2012; Windisch et al., 2008; O’Bryan et al., 2015).

Apart from use in feed, the liquid phytomolecules preparations for drinking water use can prove to be beneficial in preventing and controlling losses during challenging periods of bird’s life (feed change, handling, environmental stress, etc.).  Liquid preparations can potentially reduce morbidity and mortality in poultry houses and thus the use of therapeutic antibiotics. Barrios et al. (2021) suggested that commercial blends of phytomolecule preparations may ameliorate the impact of Necrotic Enteritis on broilers. Further, they hypothesized that the effects of liquid preparation via drinking water were particularly important in improving overall mortality.

In modern, intensive poultry production, the imminent threat of resistant Eimeria looms large, posing a significant challenge to the sustainability of broiler operations. Eimeria spp., capable of developing resistance to traditional anticoccidial drugs, has become a pressing global issue for poultry operators. The resistance of Eimeria to traditional drugs, coupled with concerns over drug residue, has necessitated a shift towards natural, safe, and effective alternatives. It was found that if a drug to which the parasite has developed resistance is withdrawn from use for some time or combined with another effective drug, the sensitivity to that drug may return (Chapman, 1997).

Several phytogenic compounds, including saponins, tannins, essential oils, flavonoids, alkaloids, and lectins, have been the subject of rigorous study for their anticoccidial properties. Among these, saponins and tannins in specific plants have emerged as powerful tools in the fight against these resilient protozoa. Botanicals and natural identical compounds are well renowned for their antimicrobial and antiparasitic activity so that they can represent a valuable tool against Eimeria (Cobaxin-Cardenas, 2016). The mechanisms of action of these molecules include degradation of the cell wall, cytoplasm damage, ion loss with reduction of proton motive force, and induction of oxidative stress, which leads to inhibition of invasion and impairment of Eimeria spp. development (Abbas et al., 2012; Nazzaro et al., 2013). Natural anticoccidial products may provide a novel approach to controlling coccidiosis while meeting the urgent need for control due to the increasing emergence of drug-resistant parasite strains in commercial poultry production (Allen and Fetterer, 2002).

Role of Feed Enzymes Beyond Feed Cost Reduction

Feed enzymes have traditionally been associated with improving feed efficiency and reducing feed costs by enhancing nutrient digestibility. However, their role can extend well beyond economic benefits, profoundly impacting gut health and supporting reduced antimicrobial use in poultry production. Exogenous enzymes reduce microbial proliferation by reducing the undigestible components of feed, the viscosity of digesta, and the irritation to the gut mucosa that causes inflammation. Enzymes also generate metabolites that promote microbial diversity which help to maintain gut ecosystems that are more stable and more likely to inhibit pathogen proliferation (Bedford, 1995; Kiarie et al., 2013).

High dietary levels of non-starch polysaccharides (NSPs) can increase the viscosity of digesta. This leads to an increase in the retention time of the digesta, slows down the nutrient digestion and absorption rate, and may lead to an undesired increase in bacterial activity in the small intestine (Langhout et al., 2000; Smits et al., 1997). Further the mucosal barrier function may also be adversely affected. To solve this problem, exogenous enzymes, such as arabinoxylanase and/ or ß-glucanase, are included in feed to degrade viscous fibre structures (Bedford, 2000). The use of xylanase and ß-glucanase may also cause oligosaccharides and sugars to be released, of which certain, for example, arabinoxylan oligosaccharides, may have prebiotic properties (De Maesschalck et al., 2015; Niewold et al., 2012).

New generation xylanases coming from family GH-10 are known to effectively breakdown both soluble and insoluble arabinoxylans into a good mixture of smaller fractions of arabino-xylo-oligosaccharides (AXOS) and xylo-oligosaccharides (XOS), which exert a prebiotic effect in the GIT. Awati et.al. (2023) observed that a novel GH10 xylanase contributed to positive microbial shift and mitigated the anti-nutritional gut-damaging effects of higher fiber content in the feed. With a substantial understanding of the mode of action and technological development in enzyme technology, nutritionists can reliably consider new-generation xylanases for gut health optimization in their antibiotic reduction strategy.

 

Conclusions

The challenge of mitigating antimicrobial resistance (AMR) in poultry production necessitates a multidimensional approach, with gut health at its core. Dietary interventions, such as organic acids, probiotics, prebiotics, phytomolecules, toxin binders, and feed enzymes, promote gut resilience, enhance immune responses, and reduce reliance on antimicrobials. These strategies not only support the health and productivity of poultry but also address critical global issues of AMR and food safety.

While no single solution fits all circumstances, integrating these dietary tools with robust biosecurity measures, sound management practices, and continued research on species-specific and field-applicable strategies can pave the way for sustainable, antibiotic-free poultry production. The transition to such systems aligns with regulatory requirements and consumer expectations while contributing to global efforts against AMR.

Ultimately, embracing holistic and innovative dietary strategies ensures a resilient gastrointestinal environment, safeguarding poultry health and productivity while protecting public health and environmental sustainability for future generations.

 

References: The references can be made available upon request to the author.

 

by Dr. Vesna Jenkins, Global Product Manager, EW Animal Care

Making silage enables the farmer to store forage, providing a cost-effective feed when required. From silage making through to feeding out, however, the challenge is to ensure that valuable dry matter, energy and protein are not lost. Any losses would require supplementation from other sources at extra cost. In the case of protein, farmers would need to purchase additional soybean meal, for example, to maintain cow productivity.

Clostridia: The Main Villain

One of the greatest challenges to making good silage is the presence of Clostridia bacteria, which can negatively impact animal health, performance and profitability. These bacteria pose a health risk to both beef and dairy cattle and can negatively influence cheese quality through the late blowing defect.

During the ensiling process, Clostridia break down protein, reducing silage nutritional value, and produce butyric acid, which decreases silage palatability and affects feed intake. Clostridia can easily enter through soil contamination and thrive in forage with low dry matter, high buffering capacity, or lower levels of soluble carbohydrates and nitrate.

Negative impacts of Clostridia

• Health risk to cattle
• Reduced nutritional value of silage
• Declined feed intake, leading to diminished productivity
• Late blowing defect in cheese

Trial results

A recent scientific trial by the Swedish University of Agricultural Sciences (SLU) tested the effect of BioStabil Plus silage inoculant on difficult to ensile grass-clover forage (28% DM) challenged with Clostridia. The research demonstrated a clear effect of BioStabil Plus on multiple parameters.

The application of BioStabil Plus to glass-clover forage resulted in:

• Improved dry matter (DM) retention (Figure 1)
• Enhanced protein preservation (Figure 2)

Both outcomes contribute to feed cost savings.

 

Benefits of BioStabil Plus

Protection Against Nutrient Loss –  BioStabil Plus protects against dry matter, energy, and protein losses in the fermentation period. It contains the rapid-growing lactic-acid-producing homofermentative strain L. plantarum DSM 19457, ensuring sufficient lactic acid production for a rapid pH drop in ensiled forage (Figure 3).

 

Reduction of Clostridial Load – BioStabil Plus reduces the Clostridial load as evidenced by significantly lower butyric acid production (Figure 4). Lower butyric acid content maintains silage palatability, feed intake, and avoids final dairy product quality issues.

 

Enhanced Aerobic Stability –  BioStabil Plus contains heterofermentative strains L. buchneri DSM 19455 and L. brevis DSM 23231, producing an optimal level of acetic acid for enhanced aerobic stability during the feed-out phase. An EFSA scientific opinion on L. brevis DSM 23231 specifically outlines its ability to reduce Clostridia risk.

Protecting your profit margin

BioStabil Plus protects against the growth of undesirable bacteria such as Clostridia, yeasts and molds during and after ensiling, helping prevent loss of valuable dry matter, energy and protein from the silage.

Producing high-quality, palatable, well-preserved silage ensures that the investment in silage making is not wasted. Most importantly, the preserved energy and protein maximize profitability through higher production of milk or meat and generate feed cost savings that support producers’ margins.

Contact your local EW Nutrition representative to access valuable resources and advice on all aspects of optimized silage management.

by Ilinca Anghelescu, Global Director Marketing Communications, EW Nutrition

 

As the global demand for animal products continues to rise, so do various claims about the impact of agriculture on greenhouse gas emissions. A study commissioned by the United Nations’ Food and Agriculture Organization (FAO) concluded that, according to the most recent data, agri-food system emissions totaled 16.5 billion metric tons of CO₂ equivalent, representing 31% of global anthropogenic emissions.

Of these 31%, the most important trend highlighted by FAO was the “increasingly important role of food-related emissions generated outside of agricultural land, in pre- and post-production processes along food supply chains”. The food supply chain (food processing, packaging, transport, household consumption and waste disposal) is thus set to become the top GHG emitter, above farming and land use.

How bad is 31%?

While 31% is a large figure, even this estimate represents a significant decrease from the 1950s, when agri-food emissions constituted approximately 58% of total anthropogenic emissions: “From 1850 until around 1950, anthropogenic CO2 emissions were mainly (>50%) from land use, land-use change and forestry”, states the latest IPCC report.

Figure 1. Source: IPCC AR6 Report, 2023. LULUCF = Land Use, Land-Use Change and Forestry

As the IPCC graph in Figure 1 indicates, the percentage decrease is mostly due to the rising prevalence of oil and coal in CO₂ emissions over the recent decades, as shown in Figure 2 below.

Annual greenhouse gas (GHG) emissions worldwide from 1990 to 2022, by sector (in million metric tons of carbon dioxide equivalent)

Figure 2. Source: Statista

Total population and agri-food emission changes, 1950 – today

The global population increased by approximately 220%, from 2.5 billion in 1950 to 8 billion in 2023. In the meantime, estimates suggest that, in the 1950s, agri-food systems were responsible for approximately 2-3 billion metric tons of CO₂-equivalent (CO₂e) emissions per year. This figure includes emissions from livestock, rice paddies, fertilizer use, and land-use change (e.g., deforestation for agriculture).

Assessments generally agree that today’s agri-food systems contribute approximately 9-10 billion metric tons of CO₂e annually, a threefold increase from 1950. This includes emissions from agriculture (e.g., livestock, crop production), food processing, transportation, and land-use changes.

This increase is consistent with FAO’s new findings, of food chain climbing to the top of agri-food emitters.

But where did these increased emissions come from?

A look at the graph below gives us an indication: world poverty rate decreased massively between 1950 and today. While COVID brought a setback, the historical data would clearly indicate a correlation between the increased output in agri-food systems and the decreased rate of poverty.

How did poverty rates decline so steeply? The reasons lie, to a large extent, in technological innovation, especially in genetics and farm management, and in the increased apport of plentiful and affordable meat protein to the world. The numbers below build an image of an industry that produces better, more, and cheaper.

Global meat production: 1950 vs. Present

Then…

In 1950, the estimated total meat production was of approximately 45 million metric tons.

Key Producers: The United States, Europe, and the Soviet Union were the primary producers of meat.
Types of Meat: Production was largely dominated by beef and pork, with poultry being less significant.

…and now

Now, the total meat production lies somewhere around 357 million metric tons (as of recent data from FAO)., representing a 53% increase from 2000 and a staggering 690% increase from 1950.

Key Producers: Major producers include China, the United States, Brazil, and the European Union.
Types of Meat: Significant increases in poultry production, with pork remaining a leading source of meat, especially in Asia. Beef production has also increased, but at a slower rate than poultry and pork.

Factors contributing to increased meat production

Population Growth: The world population has grown from approximately 2.5 billion in 1950 to over 8 billion today, driving increased demand for meat.

Economic Growth and Urbanization: Rising incomes and urbanization have led to shifts in economic power and dietary preferences, with more people consuming higher quantities of meat, especially in developing countries.

Technological Advancements: Improvements in animal breeding, feed efficiency, and production systems have increased the efficiency and output of meat production.

Intensification of Livestock Production: The shift from extensive to intensive livestock production systems has allowed for higher meat yields per animal.

Global Trade: Expansion of global trade in meat and meat products has facilitated the growth of production in countries with comparative advantages in livestock farming.

Livestock yield increase, 1950 to the present

The increase in livestock yield for cattle, pigs, and chickens between 1950 and the present has been significant due to advances in breeding, nutrition, management practices, and technology.

Beef

1950s

• Average Carcass Weight: In the 1950s, the average carcass weight of beef cattle was about 200 to 250 kilograms (440 to 550 pounds).
• Dressing Percentage: The dressing percentage (the proportion of live weight that becomes carcass) was typically around 50-55%.

Present Day

• Average Carcass Weight: Today, the average carcass weight of beef cattle is approximately 300 to 400 kilograms (660 to 880 pounds).
• Dressing Percentage: The dressing percentage has improved to about 60-65%.

Increase in Beef Cattle Yield

• Increase in Carcass Weight: The average carcass weight has increased by about 100 to 150 kilograms (220 to 330 pounds) per animal.
• Improved Dressing Percentage: The dressing percentage has increased by about 5-10 percentage points, meaning a greater proportion of the live weight is converted into meat.

Dairy

1950s

• Average Milk Yield per Cow: Approximately 2,000 to 3,000 liters per year, depending on the region.

Present Day

• Average Milk Yield per Cow: Approximately 8,000 to 10,000 liters per year globally, with some countries like the United States achieving even higher averages of 10,000 to 12,000 liters per year.

Increase in Milk Yield:: Milk yield per cow has increased about 4-5 times due to genetic selection, improved nutrition, technological advancements, and better herd management.

Chickens (Layers)

1950s

• Average Egg Production per Hen: In the 1950s, a typical laying hen produced about 150 to 200 eggs per year.

Present Day

• Average Egg Production per Hen: Today, a typical laying hen produces approximately 280 to 320 eggs per year, with some high-performing breeds producing even more.

Increase in Egg Yield: The average egg production per hen has increased by approximately 130 to 170 eggs per year.

Chickens (Broilers)

1950s

• Average Yield per Bird: In the 1950s, broiler chickens typically reached a market weight of about 1.5 to 2 kilograms (3.3 to 4.4 pounds) over a growth period of 10 to 12 weeks.

Present Day

• Average Yield per Bird: Today, broiler chickens reach a market weight of about 2.5 to 3 kilograms (5.5 to 6.6 pounds) in just 5 to 7 weeks.

Increase in Yield: The average weight of a broiler chicken has increased by approximately 1 to 1.5 kilograms (2.2 to 3.3 pounds) per bird. Additionally, the time to reach market weight has been nearly halved.

Factors contributing to yield increases

Genetic Improvement:

• Selective Breeding: Focused breeding programs have developed chicken strains with rapid growth rates and high feed efficiency, significantly increasing meat yield.

Nutrition:

• Optimized Feed: Advances in poultry nutrition have led to feed formulations that promote faster growth and better health, using balanced diets rich in energy, protein, and essential nutrients.

Management Practices:

• Housing and Environment: Improved housing conditions, including temperature and humidity control, have reduced stress and disease, enhancing growth rates.

Technological Advancements:

• Automation: Automation in feeding, watering, and waste management has improved efficiency and bird health.
• Health Monitoring: Advances in health monitoring and veterinary care have reduced mortality rates and supported faster growth.

Feed Conversion Efficiency:

• Improved Feed Conversion Ratios (FCR): The amount of feed required to produce a unit of meat has decreased significantly, making production more efficient.

Why Feed Conversion Ratio is a sustainability metric

Feed Conversion Ratio (FCR) is a critical metric in livestock production that measures the efficiency with which animals convert feed into body mass. It is expressed as the amount of feed required to produce a unit of meat, milk, or eggs. Advances in nutrition and precision feeding allow producers to tailor diets that optimize FCR, reducing waste and improving nutrient uptake. Also, breeding programs focused on improving FCR can lead to livestock that naturally convert feed more efficiently, supporting long-term sustainability.

Poultry (Broilers): From the 1950s, improved from approximately 4.75 kg/kg to 1.7 kg/kg.

Pigs: From the 1950s, improved from about 4.5 kg/kg to 2.75 kg/kg.

Cattle (Beef): From the 1950s, improved from around 7.5 kg/kg to 6.0 kg/kg.

Figure 4. Evolution of FCR from 1950

FCR is crucial for livestock sustainability for several reasons, as shown below.

1. Resource efficiency

– Feed Costs: Feed is one of the largest operational costs in livestock production. A lower FCR means less feed is needed to produce the same amount of animal product, reducing costs and improving profitability.

– Land Use: Efficient feed conversion reduces the demand for land needed to grow feed crops, helping to preserve natural ecosystems and decrease deforestation pressures.

– Water Use: Producing less feed per unit of animal product reduces the water needed for crop irrigation, which is crucial in regions facing water scarcity.

2. Environmental impact

– Greenhouse Gas Emissions: Livestock production is a significant source of greenhouse gases (GHGs), particularly methane from ruminants and nitrous oxide from manure management. Improved FCR means fewer animals are needed to meet production goals, reducing total emissions.

– Nutrient Runoff: Efficient feed use minimizes excess nutrients that can lead to water pollution through runoff and eutrophication of aquatic ecosystems.

3. Animal welfare

– Health and Growth: Optimizing FCR often involves improving animal health and growth rates, which can lead to better welfare outcomes. Healthy animals grow more efficiently and are less susceptible to disease.

4. Economic viability

– Competitiveness: Lowering FCR improves the economic viability of livestock operations by reducing input costs and increasing competitiveness in the global market.

Livestock emissions

Livestock emissions can be direct (farm-gate) or indirect (land use). Pre- and post-production emissions are considered separately, since they refer to emissions from manufacturing, processing, packaging, transport, retail, household consumption, and waste disposal.

Farm-gate emissions

Global farm-gate emissions (related to the production of crops and livestock) grew by 14% between 2000 and 2021, to 7.8 Gt CO2 eq, see below. 53% come from livestock-related activities, and the emissions from enteric fermentation generated in the digestive system of ruminant livestock were alone responsible for 37 percent of agricultural emissions (FAOSTAT 2023).

Land use for livestock

Land use emissions contribute a large share to agricultural emissions overall, especially through deforestation (~74% of land-use GHG emissions). The numbers have declined in recent years, to a total of 21% reduction between 2000 and 2018.

The other side of the coin is represented by the increased land usage for livestock, either directly for grazing or indirectly for feed crops.

1. Pasture and grazing land

1950: Approximately 3.2 billion hectares (7.9 billion acres) were used as permanent pastures.

Present: The area has increased to around 3.5 billion hectares (8.6 billion acres).

Change: An increase of about 0.3 billion hectares (0.7 billion acres).

2. Land for Feed Crops

1950: The land area dedicated to growing feed crops (such as corn and soy) was significantly less than today due to lower livestock production intensities and smaller scale operations. Feed crops likely accounted for about 200-250 million hectares of the cropland, although figures are evidently difficult to estimate.

Present: Of the approx. 5 billion hectares of land globally used for agriculture, about 1.5 billion hectares are dedicated to cropland.

The increase in cropland hectares is a direct consequence of the intensification of demand for livestock production. To keep these numbers in check, it is essential that producers strive to use as little feed as possible for as much meat yield as possible – and this directly relates to a key metric of the feed additive industry: Feed Conversion Ratio, mentioned above.

The role of food loss in livestock sustainability

The Food and Agriculture Organization (FAO) of the United Nations defines food loss as the decrease in quantity or quality of food resulting from decisions and actions by food suppliers in the chain, excluding retail, food service providers, and consumers. Food loss specifically refers to food that gets spilled, spoiled, or lost before it reaches the consumer stage, primarily taking place during production, post-harvest, processing, and distribution stages.

Food loss is currently estimated to be relatively stable over the last decades, at around 13%.

Key aspects of food loss

1. Stages of Food Loss:
   • Production: Losses that occur during agricultural production, including damage by pests or diseases and inefficiencies in harvesting techniques.
   • Post-Harvest Handling and Storage: Losses that happen due to inadequate storage facilities, poor handling practices, and lack of proper cooling or processing facilities.
   • Processing: Losses during the processing stage, which may include inefficient processing techniques, contamination, or mechanical damage.
   • Distribution: Losses that occur during transportation and distribution due to poor infrastructure, inadequate packaging, and logistical inefficiencies.
2. Quality and Quantity:
   • Quality Loss: Refers to the reduction in the quality of food, affecting its nutritional value, taste, or safety, which may not necessarily reduce its quantity.
   • Quantity Loss: Refers to the actual reduction in the amount of food available for consumption due to physical losses.
3. Exclusions:
   • Retail and Consumer Level: Food loss does not include food waste at the retail or consumer levels, which is categorized as food waste. Food waste refers to the discarding of food that is still fit for consumption by retailers or consumers.

Importance of reducing food loss

Every step along the production chain, each action taken to preserve feed, increase yield, ensure stable and high meat quality, can contribute to reducing food loss and ensuring that animal protein production stays sustainable and feeds the world more efficiently.

• Food Security: Reducing food loss can help improve food availability and access, particularly in regions where food scarcity is a concern. Where we thought we were on our way to eradicate world hunger, recent upticks in several regions show us that progress is not a given.
• Economic Efficiency: Minimizing food loss can improve the efficiency and profitability of food supply chains by maximizing the utilization of resources.
• Environmental Impact: Reducing food loss helps to decrease the environmental footprint of food production by lowering greenhouse gas emissions and minimizing land and water use. This is all the more important in regions where world hunger shows signs of going up. Perhaps not by coincidence are these regions some of the most affected by climate change.

By understanding and addressing the causes of food loss, stakeholders across the food supply chain can work towards more sustainable and efficient food systems.

What’s next?

Improving production practices and technology

Investment in research and development of new technologies that enhance livestock production efficiency and reduce environmental impact is vital for the future sustainability of the sector.

India is a good illustration of room to grow. If we look at cow milk alone, India, with a headcount of approximately 61 million animals, has a total milk production that is neck-and-neck with the United States, whose dairy cow headcount is in the neighborhood of 9.3 million. India’s milk yield sits around 1,600 liters/animal/year, compared to the US’s average of 10,700 liters.

Optimizing Feed Efficiency

Continued focus on improving FCR through genetic selection, optimized nutrition, and advanced management practices will be crucial for reducing the environmental footprint of livestock production.

Promoting Sustainable Land Use

Strategies to balance the need for increased livestock production with sustainable land use practices are essential. This includes adopting agroecological approaches and improving the efficiency of feed crop production.

Reducing Food Loss

Stakeholders across the food supply chain must prioritize reducing food loss through improved storage, transportation, and processing technologies. This will help ensure that livestock production contributes effectively to global food security.

Enhancing Emission Tracking and Reporting

There is a need for standardized methods for collecting and reporting data on GHG emissions in agriculture. This will enable more accurate assessments and the development of targeted strategies for emission reductions.

References

Bell, D. D. (2002). Laying hens in the U.S. market: An appraisal of trends from the beginning of the 20th century to present. Poultry Science, 81(5), 485-490. https://doi.org/10.1093/ps/81.5.485

CarbonWise. (2023). Global greenhouse gas emissions by sector. Retrieved from https://carbonwise.co/global-greenhouse-gas-emissions-by-sector/

Crippa, M., Solazzo, E., Guizzardi, D., Monforti-Ferrario, F., Tubiello, F. N., Leip, A., … & Janssens-Maenhout, G. (2022). Greenhouse gas emissions from food systems: building the global food system emissions database (GFED). Earth System Science Data, 14(4), 1795-1821. https://essd.copernicus.org/articles/14/1795/2022/essd-14-1795-2022.pdf

European Environment Agency (EEA). (2023). Improving the climate impact of raw material sourcing. Retrieved from https://www.eea.europa.eu/publications/improving-the-climate-impact-of-raw-material-sourcing

Food and Agriculture Organization of the United Nations (FAO). (2021). The State of Food and Agriculture 2021: Making agrifood systems more resilient to shocks and stresses. FAO. https://openknowledge.fao.org/server/api/core/bitstreams/6e04f2b4-82fc-4740-8cd5-9b66f5335239/content

Food and Agriculture Organization of the United Nations (FAO). (2021). Food Loss and Waste Database. FAO. https://www.fao.org/platform-food-loss-waste/food-loss/introduction/en

Food and Agriculture Organization of the United Nations (FAO). (2021). Greenhouse gas emissions from agrifood systems. Retrieved from https://www.fao.org/platform-food-loss-waste/food-loss/introduction/en

Goldewijk, K. K., & Verburg, P. H. (2013). Per-capita estimations of long-term historical land use and the consequences for global change research. Global Environmental Change, 23(4), 1166-1175. https://doi.org/10.1016/j.gloenvcha.2013.04.001

Intergovernmental Panel on Climate Change (IPCC). (2023). AR6 Synthesis Report: Climate Change 2023. IPCC. https://www.ipcc.ch/report/ar6/syr/

Kusuma, A. B., Laga, W. R., & Purnomo, H. (2022). Climate Change and Livestock Farming: Strategies for Mitigation and Adaptation. MDPI, 12(10), 1554. https://www.mdpi.com/2077-0472/12/10/1554

Matthews, D. (2023). Chicken, meat, and the future of global food: Forecasts and predictions for beef, pork, and more. Vox. https://www.vox.com/future-perfect/2023/8/4/23818952/chicken-meat-forecast-predictions-beef-pork-oecd-fao?mc_cid=d1a37e53b6&mc_eid=1b5c5e908a

Our World in Data. (2020). Milk yields per animal. Retrieved from https://ourworldindata.org/grapher/milk-yields-per-animal

Our World in Data. (2023). Grazing land use over the long-term, 1600 to 2023. Retrieved from https://ourworldindata.org/grazing-land-use-over-the-long-term

Ritchie, H., & Roser, M. (2020). Food greenhouse gas emissions. Our World in Data. https://ourworldindata.org/food-ghg-emissions

Roche, J. R., Friggens, N. C., Kay, J. K., Fisher, M. W., Stafford, K. J., & Berry, D. P. (2013). Invited review: Body condition score and its association with dairy cow productivity, health, and welfare. Animal Frontiers, 3(4), 23-29. https://doi.org/10.2527/af.2013-0032

Sharma, V. P., & Gulati, A. (2020). Changes in Herd Composition a Key to Indian Dairy Production. United States Department of Agriculture (USDA) Economic Research Service. https://www.ers.usda.gov/publications/pub-details/?pubid=99794

The Last Glaciers. (2023). Decarbonizing Food and Agriculture. Retrieved from https://thelastglaciers.com/decarbonising-food-and-agriculture/

Thoma, G., Jolliet, O., & Wang, Y. (2016). National Pork Board. (2016). Greenhouse gas emissions and the potential for mitigation from the pork industry in the U.S. Retrieved from https://www.porkcheckoff.org/wp-content/uploads/2021/05/16-214-THOMA-final-rpt.pdf

Thornton, P. K., & Herrero, M. (2015). Impacts of climate change on the livestock food supply chain; a review of the evidence. Frontiers in Veterinary Science, 2, 93. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4686767/

USDA – National Agricultural Statistics Service. (n.d.). Trends in U.S. Agriculture – Broiler Industry. U.S. Department of Agriculture. Retrieved from https://www.nass.usda.gov/Publications/Trends_in_U.S._Agriculture/Broiler_Industry/

Zuidhof, M. J., Schneider, B. L., Carney, V. L., Korver, D. R., & Robinson, F. E. (2014). Evolution of the modern broiler and feed efficiency. Annual Review of Animal Biosciences, 2(1), 47-71. https://doi.org/10.1146/annurev-animal-022513-114132

By Ilinca Anghelescu, Global Director Marketing Communications, EW Nutrition

Medications like GLP-1 receptor agonists, such as semaglutide (marketed as Ozempic, Wegovy, Zepbound etc.), have demonstrated startling efficacy in reducing body weight and are now at the forefront of obesity treatment. Since they work primarily by suppressing appetite, an obvious question is being considered across the entire food chain: will weight loss drugs significantly impact the future of agriculture?

More and more voices are answering “yes”. Not only are models showing a significant impact of these drugs over the medium- and long term, but the demand reduction triggered by weight loss drugs will hurt regions where population peak and shifting demand are already lowering the growth potential of certain segments of agriculture.

Changes are already seen in food consumption

Weight loss drugs like semaglutide work by mimicking the GLP-1 hormone, which regulates appetite and insulin secretion. By doing so, these medications reduce hunger and caloric intake, leading to weight loss. They also appear to reduce consumption of alcohol, tobacco, and junk food. While they have been around for more than a decade, they only recently started to be prescribed for the express purpose of weight loss. In the meantime, medical research is yielding increasingly better results at more affordable prices and with easier application, which will lead to much more widespread adoption around the world.

Currently, around 1.7% of the US population is officially prescribed such drugs, although it is hard to know how many people are actually taking this type of medication. Morgan Stanley expects the figure to grow to 7% within ten years – equivalent to well over 23 million people in the US alone. Even with this currently small percentage, retailers are claiming to see effects. Pepsi, Nestle and Walmart are among those preparing to pivot in the face of expected losses.

As more individuals adopt these drugs for weight management, dietary patterns are expected to shift even more, impacting food demand at both individual and population levels. With a 25% reduction in caloric intake for a considerable slice of the world’s over 1 billion obese people, not to mention overweight populations that might take these drugs off-label, the math speaks for itself.

Potential implications for agriculture

1. Crop Production Adjustments: Farmers might adjust crop production to align with changing consumer preferences. Increased demand for fruits, vegetables, and whole grains could lead to a shift in crop priorities, influencing agricultural planning and resource allocation.
2. Livestock Industry: A potential decrease in demand for high-fat meats and increase in demand for leaner meats could impact the livestock industry, leading to changes in breeding, feeding, and marketing strategies. Animal protein, however, remains much less impacted than industries supplying manufacturers of junk food, alcohol, and tobacco.

Changes in consumer demand will inevitably impact food prices and market dynamics, from the field to retail shelves. Increased demand for healthier food options might lead to industry shifts and higher prices initially, but as production scales up, prices could stabilize. This economic transition will require strategic adjustments across the supply chain.

Bonus problem: World population will peak and decline within two generations

To add insult to injury: United Nations demographic models suggest population growth will peak around 10.3 billion in the mid-2080s, then decline. Naturally, the distribution is unequal across the board, with some countries peaking this year and others growing at staggering speeds.

For instance, 63 countries and areas will already see population peaks in 2024 and are expected to decline by 14% over the next 30 years – including China, Russia, Germany, and Japan.

 

These new demographic models should already shape the long-term plans not just for companies, but for countries and alliances as well – and agriculture will represent a major point of impact. In its case, this map is consistent with FAO’s analysis of growth areas and lends even more credence to the idea of major shifts already felt within a generation. Growth in protein demand will move to what are now seen as developing nations, while developed countries should expect shrinking demand. It is, however, in these developed countries where obesity drugs will hit first and most strongly, lowering demand that is already nearing its peak.

Still: It’s not all bad news!

The emergence of weight loss drugs like semaglutide has the potential to influence dietary patterns significantly, thereby impacting agricultural demand and production. While this is undeniably a challenge, there is a major opportunity here as well: The industries that will be most severely hit do not include healthy protein production. A reduced food intake will likely require a higher quality of nutrition in general, with reduced demand for “empty” calories and increased demand for vitamin-, fiber-, and especially protein-packed meals, tasty as well as nutritionally rich.

 

Further reading

Wilding, J.P.H., et al. (2021). “Once-Weekly Semaglutide in Adults with Overweight or Obesity.” *New England Journal of Medicine*, 384(11), 989-1002. https://www.nejm.org/doi/full/10.1056/NEJMoa2032183

Astrup, A., et al. (2021). “Semaglutide for the treatment of overweight and obesity: A review.” *Diabetes, Obesity and Metabolism*, 23(S1), 39-49. https://dom-pubs.onlinelibrary.wiley.com/doi/full/10.1111/dom.14863

Garnett, T. (2011). “Where are the best opportunities for reducing greenhouse gas emissions in the food system (including the food chain)?” *Food Policy*, 36, S23-S32. https://www.sciencedirect.com/science/article/abs/pii/S0306919210001132

 

Antimicrobial resistance (AMR) poses a significant threat to global health, driven by the overuse and misuse of antibiotics in both human medicine and livestock farming. In livestock farming, antimicrobials are still used extensively for therapeutic and non-therapeutic purposes. However, estimates of the quantities used per species are notoriously hard to derive from fragmented, incomplete, or unstandardized data around the world.

A recent article (“Global antimicrobial use in livestock farming: an estimate for cattle, chickens, and pigs”, Animal, 18(2), 2024) attempts to update the figures by estimating global biomass at treatment of cattle, pigs, and chickens, considering distinct weight categories for each species in biomass calculation, and using the European Medicines Agency’s weight standards for the animal categories. With these more refined calculations, authors Zahra Ardakani, Maurizio Aragrande, and Massino Canali aim to provide a more accurate estimate of global antimicrobial use (AMU) in cattle, chickens, and pigs. Understanding these patterns is crucial for addressing AMR and developing strategies for sustainable livestock management.

Key Findings

The study estimates that the global annual AMU for cattle, chickens, and pigs amounts to 76,060 tons of antimicrobial active ingredients. This is a significant revision from previous estimates due to a more detailed evaluation of animal weights and categories:

1. Cattle: 40,697 tons (53.5% of total AMU)
2. Pigs: 31,120 tons (40.9% of total AMU)
3. Chickens: 4,243 tons (5.6% of total AMU)

Methodology

The study utilizes the concept of Population Correction Units (PCU) to estimate antimicrobial usage, taking into account the weight and category of livestock at the time of treatment. This method differs from previous approaches that relied on live weight at slaughter, providing a more accurate representation of AMU.

The PCU is calculated by multiplying the number of animals by their average weight during treatment. This approach allows for differentiation by age and sex, which is particularly important for species like cattle and pigs.

Figure 2: (a) Changes in global PCU (million tonnes), (b) changes in global antibiotic use in mg per PCU, and (c) changes in global AMU (thousand tonnes) for cattle, chickens, and pigs; between 2010 and 2020.  Abbreviations: PCU = Population Correction Unit; AMU = Antibiotic Use.

Study shows lower AMU than previous estimates

The study highlights a significant shift in AMU patterns, with chickens showing a remarkable decrease in antimicrobial use despite increased production. This is indicative of improved management and more responsible use of antibiotics in the poultry industry.

The lower AMU in cattle and pigs, compared to previous estimates, underscores the importance of considering animal age and weight at treatment. These findings align closely with World Organization for Animal Health (WOAH) estimates, validating the methodology.

However, the study also acknowledges limitations, including reliance on European standards for average weight at treatment, which may not reflect global variations. Additionally, the lack of comprehensive global data on veterinary antibiotics presents challenges in creating fully accurate estimates.

Corrected estimate highlights improved production advances

This study provides a revised and potentially more accurate estimate of global antimicrobial use in livestock. By accounting for the weight and treatment categories of animals, it offers insights that could guide policy and management practices to mitigate the spread of antimicrobial resistance.

The article also indicates that the industry may have over-estimated antimicrobial usage in livestock and, just as importantly, that antimicrobial use has been kept in check or even reduced, despite increases in farmed animal headcounts. The lower usage is likely due to regulatory oversight and improvements in alternative methods to control and mitigate health challenges.

 

Part 4: Paleness

By Dr. Inge Heinzl, Editor and Marisabel Caballero, Global Technical Manager Poultry

We already showed bad feathering, mouth and beak lesions, bone issues, and foot pad lesions as signs of mycotoxin contamination in the feed, but there is another indicator: paleness. Paleness can signify a low count of red blood cells resulting from blood loss or inadequate production of these cells. Other possibilities are higher bilirubin levels in the blood due to an impaired liver, leading to jaundice or missing pigmentation.

The mycotoxins mainly causing anemia are Aflatoxins, Ochratoxin, DON, and T-2 toxin

Anemia can be diagnosed using parameters such as red blood cell count, hemoglobin levels, and hematocrit/packed cell volume (PCV). Numerous studies have examined the impact of mycotoxins on hematological parameters. They reveal their propensity to affect red blood cell production by impairing the function of the spleen and inducing hematological alterations. On the other hand, anemia can be caused by blood loss. Due to affecting coagulation factors, mycotoxins can lead to internal hemorrhages. The gut wall damage, probably due to secondary infections such as coccidiosis and necrotic enteritis, can entail bloody diarrhea in various animal species.

Impact on the production of blood cells

Low values of blood parameters such as red blood cells, hemoglobin, and hematocrit can result from inadequate production due to impacted production organs. The World Health Organization (WHO, 1990) and European Commission (European Commission, 2001) have identified hematopoietic tissues as targets for necrosis caused by T-2 toxin. Chu (2003) even stated that “the major lesion of T-2 toxin is its devastating effect on the hematopoietic system in many mammals, including humans”. Pande et al. (2006) suggested that reduced hemoglobin values result from decreased protein synthesis due to mycotoxin contamination, a notion supported by Pronk et al. (2002), who described trichothecenes as potent inhibitors of protein, DNA, and RNA synthesis, particularly affecting tissues with high cell division rates. Additionally, the European Commission (2001) highlighted the sensitivity of red blood cell progenitor cells (in this trial, the cells of mice, rats, and humans) to the toxic effects of T-2 and HT-toxins. DAS also seems to attack the hematopoietic system, as shown in humans (WHO, 1990). A further cause for anemia might be low feed intake or nutrient absorption, which inhibits adequate iron absorption and leads to iron deficiency. In their case report, Bozzo et al. (2023) assumed that renal failure and a resulting impaired excretion capacity caused by OTA might even increase the half-life of the toxins. This would enhance their effects on their target organs, such as the liver and bone marrow, and lead to anemia.

Several studies utilizing different animal species and mycotoxin dosages have been conducted to assess the effects of Aflatoxins, Ochratoxin, and T-2 Toxin on hematological parameters. The following table provides a summary of some of these studies.

Animal species	Dosage	Impact	Reference
T-2 Toxin and other Trichothecenes
Broilers	T-2 – 0, 1, 2, and 4 mg T-2 toxin/kg n=30 per group	Significant reduction in hemoglobin at 1, 2, and 4 ppm; PCV significantly reduced at 4 ppm	Pande et al., 2006
Broilers	T-2 – 0 and 4 mg/kg diet n=60 per group	Decrease in hemoglobin, mean corpuscular volume, and mean corpuscular hemoglobin concentration	Kubena et al., 1989a
Broilers	4, 16, 50, 100, 300 ppm for seven days n=5-20 chickens per group	Anemia; significant reduction of hematocrit (50 and 100 ppm); survivors had atrophied lymphoid organs and were anemic	Hoerr et al., 1982
Yangzhou goslings	0, 0.2, 0.4, 0.6, 0.8, 1.0, 2.0 mg/kg; n=6 per group	Red blood cell count decreased in the 2.0 mg/kg group along with an increase in mean corpuscular hemoglobin (p<0.05) and reduced mean platelet volume (P<0.05)	Gu et al., 2023
Broilers	2 ppm; 32 birds per group	Anemia, as indicated by significantly (P<0.05) lower total erythrocyte count (TEC) values, lower hemoglobin levels, and packed cell volume; additional thrombocytopenia could be the cause of bleeding	Yohannes et al., 2013
DON
Broilers	5 and 15 mg/kg of feed for 42 days	Decrease in erythrocytes, mean corpuscular volume (MCV), and mean corpuscular hemoglobin concentration (MCHC) at 15 mg/kg; decrease in hematocrit and hemoglobin at both levels of DON.	Riahi, 2021
Piglets	0.6 mg/kg and 2.0 mg/kg	Significant decrease in mean corpuscular volume	Modrá et al., 2013
Broilers	16 mg/kg diet n=60 per group	Significant decrease in mean corpuscular volume	Kubena et al., 1989c
Ochratoxin
Broilers	2 mg/kg diet singly or combined with DAS 6 mg/kg	Reduced mean corpuscular hemoglobin values	Kubena et al., 1994
Broilers	2 mg/kg diet	Significant decrease in hemoglobin, hematocrit, mean corpuscular volume and mean corpuscular hemoglobin concentration	Kubena et al., 1989b
Aflatoxins
Broilers	2.5 µg/g	Decrease in red blood cell count	Huff et al., 1988
Broilers	≥1.25 µg/g	Significant decrease in hemoglobin and erythrocyte count	Tung et al., 1975
AFB1 + OTA
Laying hens	Natural feed contamination OTA – 31 ± 3.08 µg/kg and AFB1 – 5.6 ± 0.33 µg/kg dry weight	Anemia signs (pale appearance of combs and wattles), evidenced by the discoloration of the content of the femoral medullary cavity.	Bozzo et al., 2023

Table 1: The effects of different mycotoxins on hematological parameters – hematopoiesis

In their meta-analysis, Andretta et al. (2012) reported that the presence of mycotoxins in broiler diets decreased the hematocrit and the hemoglobin concentration by 5% and 15%, and aflatoxin alone decreased the parameters by 6% and 20%.

It should be evident that a simultaneous occurrence of several mycotoxins even aggravates the situation. In an experiment involving Sprague Dawley rats, administering T-2, DON, NIV, ZEA, NEO, and OTB decreased hematocrit and red blood cell counts across all mycotoxins. However, for DON, NIV, ZEN, and OTB, red blood cell values showed partial recovery after 24 hours (Chattopadhyay, 2013). Perhaps the organism learns to cope with the mycotoxins.

The examples show that Trichothecenes, such as T-2 toxin, DON, and others, as well as Ochratoxins and Aflatoxins, impact blood parameters such as hematocrit, hemoglobin, red blood cell count, and mean corpuscular volume. All these changes might lead to paleness of the skin and birds’ feet and combs.

Blood loss caused by bleeding or destruction of erythrocytes

The second possibility for anemia is blood loss due to injuries or lesions. In addition to directly causing hemorrhages, mycotoxins can promote secondary infections such as coccidiosis, which damages the gut and may produce bloody feces.

Parent-Massin (2004) e.g. reports on rapidly progressing coagulation problems after the ingestion of trichothecenes leading to septicemia and massive hemorrhages. Table 2 shows more examples of mycotoxins causing paleness due to blood loss.

Animal species	Dosage	Impact	Reference
T-2 Toxin and other Trichothecenes
Cats	T-2 toxin – 0.06-0.1 mg/kg body weight/day	Bloody feces, hemorrhages	Lutsky et al., 1978
Cats	T-2 toxin – 0.08 mg/kg BW every 48 h until death	Bloody feces	Lutzky and Mor, 1981
Pigeon	DAS in oat, sifting	Emesis and bloody stools	Szathmary (1983)
Calves	0.08, 0.16, 0.32, or 0.6 mg/kg BW per day for 30 days; 1 calf per treatment	Bloody feces at doses ≥0.32 mg/kg BW per day	Pier et al., 1976
Ochratoxin
Rats	Single dosages of 0, 17, or 22 mg/kg BW in 0.1 Mol/L NaHCO3, gavage	Multifocal hemorrhages in many organs	Albassam et al., 1987
DON
Broilers	0, 35, 70, 140, 280, 560, and 1120 mg/kg body weight	Ecchymotic hemorrhages throughout the intestinal tract, liver, and musculature; relationship to hemorrhagic anemia syndrome seems warranted	Huff et al., 1981
Sterigmatocystin (ST)
10-12-day old chicks (93-101 g)	10 and 14 mg/kg BW intraperitoneal	Hemorrhages and foci of necrosis in the liver	Sreemannarayana et al., 1987
Aflatoxins
Broiler chickens	100 µg/kg feed	Hemorrhages in the liver	Abdel-Sattar, 2019
Turkeys	500 and 1000 ppb in the diet	Bloody diarrhea, spleens with hemorrhages, petechial hemorrhages in the small intestine	Giambrone et al., 1984
Broilers	0, 0.625, 1.25, 2.5, 5.0, and 10.0 mg/kg of diet combined with Infectious Bursal Disease	Slight hemorrhages in the skeletal muscles; decreased hematocrit and hemoglobin due to hemolytic anemia.	Chang and Hamilton, 1981
Broilers	0, 1, and 2 mg AFB1/kg of diet	Downregulation of the genes involved in blood coagulation (coagulation factor IX and X) and upregulation of anticoagulant protein C precursor, an inactivator of coagulation factors Va and VIIIa, and antithrombin-III precursor with 2 mg/kg	Yarru, 2009
Pigs	1-4 mg/kg, 4 weeks 0.4-0.8 mg/kg, 10 weeks	Hemorrhages	Henry et al., 2001

Table 2: The effects of different mycotoxins on hematological parameters – blood loss

Poor pigmentation

The fourth reason for paleness can be inadequate pigmentation. According to Hy Line (2021), the so-called pale bird syndrome is characterized by poor skin and egg yolk pigmentation and is caused by reduced absorption of fat and carotenoid pigments in compromised birds. This is also the case when the diets contain pigment supplements. Tyczkowski and Hamilton (1986) observed in their experiment with chickens exposed to doses of 1-8 µg of Aflatoxins/g of diet for three weeks that aflatoxins can cause poor pigmentation in chickens, probably by impairing carotenoids absorption but also transport and deposition. Osborne et al. (1982) asserted that carotenoids were significantly (P<0.05) depressed by 2 ppm ochratoxin as well as by 2.5 ppm aflatoxin in the diet.

Another possibility is oxidative stress due to the mycotoxin challenge. As pigments also serve as antioxidants, they may be expended for this purpose and are no longer available for pigmentation.

Paleness in poultry – a reason to think about mycotoxins

Paleness can have different causes, some of which are influenced by mycotoxins. If your chickens or hens are pale, checking the feed concerning mycotoxins is always recommended. A feed analysis can give information about possible contamination (see our tool MasterRisk).

In the case of contamination, effective products binding the mycotoxins and mitigating the adverse effects of these harmful substances can help protect your birds. As paleness is usually not the only effect of mycotoxins but also a decrease in growth, toxin binders can help maintain the performance of your animals.

References:

Abdel-Sattar, Ward Masoud, Kadry Mohamed Sadek, Ahmed Ragab Elbestawy, and Disouky Mohamed Mourad. “The Protective Role of Date Palm (Phoenix Dactylifera Seeds) against Aflatoxicosis in Broiler Chickens Regarding Carcass Characterstics, Hepatic and Renal Biochemical Function Tests and Histopathology.” Journal of World’s Poultry Research 9, no. 2 (June 25, 2019): 59–69. https://doi.org/10.36380/scil.2019.wvj9.

Albassam, M. A., S. I. Yong, R. Bhatnagar, A. K. Sharma, and M. G. Prior. “Histopathologic and Electron Microscopic Studies on the Acute Toxicity of Ochratoxin a in Rats.” Veterinary Pathology 24, no. 5 (September 1987): 427–35. https://doi.org/10.1177/030098588702400510.

Andretta, I., M. Kipper, C.R. Lehnen, and P.A. Lovatto. “Meta-Analysis of the Relationship of Mycotoxins with Biochemical and Hematological Parameters in Broilers.” Poultry Science 91, no. 2 (February 2012): 376–82. https://doi.org/10.3382/ps.2011-01813.

Bhat, RameshV, Y Ramakrishna, SashidharR Beedu, and K.L Munshi. “Outbreak of Trichothecene Mycotoxicosis Associated with Consumption of Mould-Damaged Wheat Products in Kashmir Valley, India.” The Lancet 333, no. 8628 (January 1989): 35–37. https://doi.org/10.1016/s0140-6736(89)91684-x.

Bozzo, Giancarlo, Nicola Pugliese, Rossella Samarelli, Antonella Schiavone, Michela Maria Dimuccio, Elena Circella, Elisabetta Bonerba, Edmondo Ceci, and Antonio Camarda. “Ochratoxin A and Aflatoxin B1 Detection in Laying Hens for Omega 3-Enriched Eggs Production.” Agriculture 13, no. 1 (January 5, 2023): 138. https://doi.org/10.3390/agriculture13010138.

Chang, Chao-Fu, and Pat B. Hamilton. “Increased Severity and New Symptoms of Infectious Bursal Disease during Aflatoxicosis in Broiler Chickens.” Poultry Science 61, no. 6 (June 1982): 1061–68. https://doi.org/10.3382/ps.0611061.

Chattopadhyay, Pronobesh, Amit Agnihotri, Danswerang Ghoyary, Aadesh Upadhyay, Sanjeev Karmakar, and Vijay Veer. “Comparative Hematoxicity of Fusarium Mycotoxin in Experimental Sprague-Dawley Rats.” Toxicology International 20, no. 1 (2013): 25. https://doi.org/10.4103/0971-6580.111552.

European Commission. “Opinion of the Scientific Committee on Food on Fusarium Toxins Part 5: T-2 Toxin and HT-2 Toxin.” Food.ec.europa. Accessed May 30, 2001. https://food.ec.europa.eu/document/download/a859c348-a38e-404c-a2af-c3e29a3a8777_en?filename=sci-com_scf_out88_en.pdf.

Giambrone, J.J., U.L. Diener, N.D. Davis, V.S. Panangala, and F.J. Hoerr. “Effect of Purified Aflatoxin on Turkeys.” Poultry Science 64, no. 5 (May 1985): 859–65. https://doi.org/10.3382/ps.0640859.

Gu, Wang, Qiang Bao, Kaiqi Weng, Jinlu Liu, Shuwen Luo, Jianzhou Chen, Zheng Li, et al. “Effects of T-2 Toxin on Growth Performance, Feather Quality, Tibia Development and Blood Parameters in Yangzhou Goslings.” Poultry Science 102, no. 2 (February 2023): 102382. https://doi.org/10.1016/j.psj.2022.102382.

Henry, H., T. Whitaker, I. Rabban, J. Bowers, D. Park, W. Price, F.X. Bosch, et al. “Aflatoxin M1.” Aflatoxin M1 (JECFA 47, 2001). Accessed July 29, 2024. https://inchem.org/documents/jecfa/jecmono/v47je02.htm.

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Yohannes, T., A. K. Sharma, S. D. Singh, and V. Sumi. “Experimental Haematobiochemical Alterations in Broiler Chickens Fed with T-2 Toxin and Co-Infected with IBV.” Open Journal of Veterinary Medicine 03, no. 05 (2013): 252–58. https://doi.org/10.4236/ojvm.2013.35040.

Part 3: Bone disorders and foot pad lesions

By Dr. Inge Heinzl, Editor, and Marisabel Caballero, Global Technical Manager Poultry

 

Bone health is essential for animals and humans. Besides giving structural support, allowing movement, and protecting vital organs, the bones release hormones that are crucial for mineral homeostasis and acid balance and serve as reservoirs of energy and minerals (Guntur & Rosen, 2012; Rath, N.C. & Durairaj, 2022; Suchacki et al., 2017).

Bone disorders and foot pad lesions are considerable challenges in poultry production, especially for fast-growing birds with high final weights. Due to pain, the animals do not move, and dominant, healthy birds may restrict lame birds’ access to feed and water. In consequence, these birds are often culled. Moreover, processing these birds is problematic, and often, they must be discarded or downgraded.

Foot pad lesions, another common issue in poultry production, can also have significant economic implications. On the one hand, pain restricts birds from eating and drinking and reduces weight gain. On the other hand, for many producers, chicken feet constitute a substantial part of the economic value of the bird; therefore, discarding them represents a significant financial loss. Additionally, to push poultry production in the right direction concerning animal health and welfare, a foot pad scoring system at the processing plant is in place in European countries.

Mycotoxins affect bones in different ways

Mycotoxins, depending on their target organs, can have diverse effects on the skeleton of birds. For example, mycotoxins that target the liver can disrupt calcium metabolism, which in turn affects the mineralization of the bones (rickets) and the impairment of chondrocytes can slow down bone growth (e.g., tibial dyschondroplasia). When the kidneys are impacted, urate clearance decreases, plasma uric acid consequently increases, and urate crystals form in the synovial fluid and tendon sheaths of various joints, particularly the hock joints. These examples highlight the complex and varied ways mycotoxins can impact poultry bone health.

Inadequate bone mineralization and strength – Rickets and layer cage fatigue

Sufficient bone mineralization is essential for the stability of the skeleton. Calcium (Ca), Vitamin D, and Phosphorous (P) deficiency leads to inadequate mineralization, weakens the bone, and can cause soft and bent bones or, in the case of layers, cage fatigue – a collapse of the spinal bone- and paralysis. Inadequate bone mineralization can be caused in different ways, among them:

1. Decrease in the availability of the nutrients necessary for mineralization. This can occur if the digestibility of these nutrients deteriorates
2. Impact on the Ca/P ratio—A ratio of 1 – 2:1 is vital for adequate bone development (Loughrill et al., 2016). Mycotoxins can alter absorption and transporters for one or both elements, altering their ratio.
3. Impact on the Vitamin D receptor, affecting its expression or the transporters for Ca and P.

Aflatoxins can impair bone mineralization by different modes of action. An important one is the impairment of the digestibility of Ca and P: Kermanshahi et al. (2007) fed broilers diets with high levels of aflatoxins (0.8 to 1.2 mg AFB1/kg feed) for three weeks, which resulted in a significant reduction of Ca and P digestibility. Other researchers, however, did not find an effect on Ca and P digestibility with lower aflatoxin levels:  Bai et al. (2014) feeding diets contaminated with 96 (starter) and 157 µg Aflatoxins (grower) per kg of feed to broilers and Han et al. (2008) saw no impact on cherry valley ducks with levels of 20 and 40 µg AFB1/kg diet.

Indirectly, a decrease in the availability of Ca and P due to aflatoxin-contaminated feed can be shown by blood or tibia levels of these minerals, as demonstrated by  Zhao et al. (2010): They conducted a trial with broilers, resulting in blood serum levels of Ca and P levels significantly (P<0.05) dropped with feed contaminated with 2 mg/kg of AFB1. Another trial conducted by Bai et al. (2014) showed decreased Ca in the tibia and reduced tibial break strength.

To get more information about the effect of mycotoxins on bone mineralization and the utilization of Ca, P, and Vit. D in animal organisms, Costanzo et al. (2015) challenged osteosarcoma cells with 5 and 50 ppb of aflatoxin B1. They asserted a significant down-modulation of the expression of the Vitamin D receptor. Furthermore, they assumed an interference of AFB1 with the actions of vitamin D on calcium-binding gene expression in the kidney and intestine.  Paneru et al. (2024) could confirm this downregulation of the Vit D receptor and additionally of the Ca and P transporters in broilers with levels of ≥75 ppb AFB1. They also saw a significant reduction in tibial bone ash content at AFB1 levels >230 ppb, a decreased trabecular bone mineral content and density at AFB1 520 ppb, and a reduced bone volume and tissue volume of the cortical bone of the femur at the level of 230 ppb (see Figure 1). They concluded that AFB1 levels of already 230 ppb contribute to bone health issues in broilers.

Figure 1: Increasing doses of AFB1 (<2 ppb – 560 ppb) deteriorate bone quality (Paneru, 2024): Cross-sectional images of femoral metaphysis with increasing AFB1 levels (left to right). The outer cortical bone is shown in light grey, and the inner trabecular bone in blue. Higher levels of AFB1 (T4 and T5) show a disruption of the trabecular bone pattern (less dense blue pattern with thinner and more fragmented bone strands and with wide spaces between the trabecular bone) (shown in white).

All experiments strongly suggest that aflatoxins harm bone homeostasis. Additional liver damage, oxidative stress, and impaired cellular processes can exacerbate bone health issues.

Trichothecenes also negatively impact bone mineralization. Depending on the mycotoxin, they may affect the gut, decreasing the absorption of Ca and P and probably provoking an imbalance in the Ca/P ratio.

For instance, when T-2 toxin was fed to Yangzhou goslings at 0.4, 0.6, and 0.8 mg/kg of diet, it decreased the Ca levels (halved at 0.8 mg/kg) and increased the P levels in the blood serum, so the Ca/P ratio decreased from the adequate ratio of 1 – 2 to 0.85, 0.66, and 0.59 (P<0.05) (Gu et al., 2023). The alterations of the Ca and P levels, the resulting decreasing Ca/P ratio, and an additional increase in alkaline phosphatase (ALP) suggest that T-2 toxin negatively impacts Ca absorption, increases ALP, and, therefore, disturbs calcification and bone development.

Other studies show that serum P levels decreased in broilers fed DON-contaminated feed with levels of only 2.5 mg/kg (Keçi et al., 2019). One reason for the lower P level is probably the lower dry matter intake, affecting Ca and P intake. Ca serum level is not typically reduced, which can be explained by the fact that Ca plays many critical physiological roles (e.g., nerve communication, blood coagulation, hormonal regulation), so the body keeps the blood levels by reducing bone mineralization. Another explanation is delivered by Li et al. (2020): After their trial with broilers, they stated that dietary P deficiency is more critical for bone development than Ca deficiency or Ca & P deficiency. The results of the trial conducted by Keçi et al. with DON (see above) were reduced bone mineralization, affected bone density, ash content, and ash density in the femur and tibiotarsus with a stronger impact on the tibiotarsus than on the femur.

In line with trichothecenes effects in Ca and P absorption, Ledoux et al. (1992) suppose that diarrhea caused by intake of fumonisins leads to malabsorption or maldigestion of vitamin D, calcium and phosphorus, having birds with rickets as a secondary effect.

Ochratoxin A (OTA) impairs kidney function, negatively affects vitamin D metabolism, reduces Ca absorption, and contributes to deteriorated bone strength (Devegowda and Ravikiran, 2009). Indications from Huff et al. (1980) show decreased tibia strength after feeding chickens OTA levels of 2, 4, and 8 µ/g, and Duff et al. (1987) report similar results also in turkey poults.

A further mycotoxin possibly contributing to leg weakness is cyclopiazonic acid produced by Aspergillus and Penicillium. This mycotoxin is known for leading to eggs with thin or visibly racked shells, indicating an impairment of calcium metabolism (Devegowda and Ravikiran, 2009). Tran et al. (2023) also showed this fact with multiple mycotoxins.

The co-occurrence of different mycotoxins in the feed – the standard in praxis – increases the risk of leg issues. A trial with broiler chickens conducted by Raju and Devegowda (2000) showed a bone ash-decreasing effect of AFB1 (300 µg/kg), OTA (2 mg/kg), and T-2 toxin (3 mg/kg), fed individually but an incomparable higher effect when fed in combination.

Impairment of bone growth – tibial dyschondroplasia (TD)

In TD, the development of long bones is impaired, and abnormal cartilage development occurs. It is frequent in broilers, with a higher incidence in males than females. It happens when the bone grows, as the soft cartilage tissue is not adequately replaced by hard bone tissue. Some mycotoxins have been related to this condition: According to Sokolović et al. (2008), actively dividing cells such as bone marrow are susceptible to T-2 toxin, including the tibial growth plates, which regulate chondrocyte formation, maturation, and turnover.

T-2 toxin: In a study with primary cultures of chicken tibial growth plate chondrocytes (GPCs) and three different concentrations of T-2 toxin (5, 50, and 500 nM), He et al. (2011) found that T-2 toxin decreased cell viability, alkaline phosphatase activity, and glutathione content (P < 0.05). Additionally, it increased the level of reactive oxygen species and malondialdehyde in a dose-dependent way, which could be partly recompensated by adding an antioxidant (N-acetyl-cysteine). They concluded that T-2 toxin inhibits the proliferation and differentiation of GPCs and contributes, therefore, to the development of TD, altering cellular homeostasis. Antioxidants may help to reduce these effects.

Gu et al. (2023) investigated the closely bodyweight-related shank length and the tibia development in Yangzhou goslings fed feed with six different levels (0 to 2.0 mg/kg) of T-2 toxin for 21 days. They determined a clear dose-dependent slowed tibial length and weight growth (p<0.05), as well as abnormal morphological structures in the tibial growth plate. As tibial growth and shank length are closely related to weight gain (Gu et al., 2023; Gao et al., 2010; Ukwu et al., 2014; Yu et al., 2022), their slowdown indicates lower growth performance.

Fumonisin B1 is also a potential cause of this kind of leg issue. Feeding 100 and 200 mg/kg to day-old turkey poults for 21 days led to the development of TD (Weibking et al., 1993). Possible explanations are the reduced viability of chondrocytes, as found by Chu et al. (1995) after 48 h of exposure, or the toxicity of FB1 to splenocytes and chondrocytes, which was shown in different primary cell cultures from chicken (Wu et al., 1995).

Bacterial chondronecrosis with osteomyelitis lameness (BCO) can be triggered by DON and FUM

BCO presents a highly critical health and welfare issue in broiler production worldwide, and it is estimated that 1-2 % of condemnations in birds at the marketing age result from this disease. What is the reason? Today’s fast-growing broilers are susceptible to stress. This enables pathogenic bacteria to compromise epithelial barriers, translocate from the gastrointestinal tract or the pulmonary system into the bloodstream, and colonize osteochondrotic microfractures in the growth plate of the long bone. This can lead to bone necrosis and subsequent lameness.

In their experiment with DON and FUM in broilers, Alharbi et al. (2024) showed that these mycotoxins reduce the gut’s barrier strength and trigger immunosuppressive effects. They used contaminations of 0.76, 1.04, 0.94, and 0.93 mg DON/kg of feed and 2.40, 3.40, 3.20, and 3.50 mg FUM/kg diet in the starter, grower, finisher, and withdrawal phases, respectively. The team observed lameness on day 35; the mycotoxin groups always showed a significantly (P<0.05) higher incidence of cumulative lameness.

The increase in uric acid leads to gout

In general, mycotoxins, which damage the kidneys and, therefore, impact the renal excretion of uric acid, are potentially a factor for gout appearance.

One of these mycotoxins is T-2 toxin. With the trial mentioned before (Yangzhou goslings, 21 days of exposure), Gu et al. (2023) showed that the highest dosage of the toxin (2.0 mg/kg) significantly increased uric acid in the blood (P<0.05), possibly leading to the deposit of uric acid crystals in the joints and to gout.

Huff et al. (1975) applied Ochratoxin to chicks at 0, 0.5, 1.0, 2.0, 4.0, and 8.0 µg/g of feed during the first three weeks of life. They found ochratoxin A as a severe nephrotoxin in young broilers as it caused damage to the kidneys with doses of 1.0 µg/g and higher. At 4.0 and 8.0 µg/g doses, uric acid increased by 38 and 48%, respectively (see Figure 2). Page et al. (1980) also reported increased uric acid after feeding 0.5 or 1.0 mg/kg of Ochratoxin A to adult white Leghorn chickens.

Figure 2: Effect of Ochratoxin A on plasma uric acid (mg/100 ml) (according to Huff et al., 1975)

Foot pad lesions – a further hint of mycotoxicosis

Foot pad lesions often result from wet litter, originating from diarrhea due to harmed gut integrity. Frequently, mycotoxins impact the intestinal tract and create ideal conditions for the proliferation of diarrhea-causing microorganisms and, therefore, secondary infections. Some also negatively impact the immune defense system, allowing pathogens to settle down or aggravate existing bacterial or viral parasitic diseases. In general, mycotoxins affect the physical (intestinal cell proliferation, cell viability, cell apoptosis), chemical (mucins, AMPs), immunological, and microbial barriers of the gut, as reported by Gao et al. (2020). Here are some examples of the adverse effects of mycotoxins leading to intestinal disorders and diarrhea:

• Mycotoxins can modulate intestinal epithelial integrity and the renewal and repair of epithelial cells, negatively impacting the intestinal barrier’s intrinsic components; for instance, DON can significantly reduce the transepithelial electrical resistance (TEER)(Grenier and Applegate, 2013). A higher permeability of the epithelium and a decreased absorption of dietary proteins can lead to higher protein in the digesta in the small intestine, which serves as a nutrient for pathogens including perfringens (Antonissen et al., 2014; Antonissen et al., 2015).
• The application of Ochratoxin A (3 mg/kg) increased the number of S. typhimurium in the duodenum and ceca of White Leghorn chickens (Fukata et al., 1996). Another trial with broiler chicks at a concentration of 2 mg/kg aggravated the symptoms due to an infection by S. gallinarum (Gupta et al., 2005).
• In a trial by Grenier et al., 2016, feed contaminated with DON (1.5 mg/kg), Fumonisin B (20 mg/kg), or both mycotoxins aggravated lesions caused by coccidia.
• DON impacts the mucus layer composition by downregulating the expression of the gene coding for MUC2, as shown in a trial with human goblet cells (Pinton et al., 2015). The mucus layer prevents pathogenic bacteria in the intestinal lumen from contacting the intestinal epithelium (McGuckin et al., 2011).
• Furthermore, DON and other mycotoxins decrease the populations of lactic acid-producing bacteria, indicating a shift in the microbial balance (Antonissen et al., 2016).
• FB1 causes intestinal disturbances such as diarrhea, although it is poorly absorbed in the intestine. According to Bouhet and Oswald (2007), the main toxicological effect ascertained in vivo and in vitro is the accumulation of sphingoid bases associated with the depletion of complex sphingolipids. This negative impact on the sphingolipid biosynthesis pathway could explain other adverse effects, such as reduced intestinal epithelial cell viability and proliferation, modification of cytokine production, and impairment of intestinal physical barrier function.
• T-2 toxin can disrupt the immune response, enhance the proliferation of coli in the gut, and increase its efflux (Zhang et al., 2022).

All these mycotoxins can cause foot pad lesions by impacting gut integrity or damaging the gut mucosa. They promote pathogenic organisms and, thus, provoke diarrhea and wet litter.

Mitigating the negative impact of mycotoxins on bones and feet is crucial for performance

Healthy bones and feet are essential for animal welfare and performance. Mycotoxins can be obstructive. Consequently, the first step to protecting your animals is to monitor their feed. If the analyses show the occurrence of mycotoxins at risky levels, proactive measures must be taken to mitigate the issues and ensure the health and productivity of your poultry.

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Institut du Porc (IFIP), the French pork research and development institute and a key player in the French agricultural sector, has recently published its 2024 report, titled Porc par les Chiffres 2023-2024. The document provides a comprehensive overview of the global, European, and French pork industries and is a critical resource for all industry professionals.

The Global Pork Industry

The global pork industry has experienced significant changes over recent years. In 2021, global pork production reached approximately 108 million tons of carcass weight equivalent (CWE), largely driven by China’s recovery from African Swine Fever (ASF). By 2022, global production continued to rise, though at a slower pace due to the stabilization of China’s pig herd. However, the global landscape remains varied with notable regional differences.

Figure 1. Main pork exporters (in 1000 tons)*

Figure 2. Main pork importers (in 1000 tons)*

*Excluding intra-EU and intra-EUMCA-EU trade evolving: EU15 (2000-2003), EU25 (2004-2006), EU27 (2007-2013), EU28 (2014)

In Asia, China dominates pork production, contributing 47.5 million tons in 2021. Other significant producers include Vietnam, Japan, South Korea, and the Philippines. In Europe, the EU-28 collectively produced 24.6 million tons, with Germany, Spain, and France being the leading producers. In the Americas, the United States and Brazil are major contributors, with the U.S. producing 12.6 million tons and Brazil 4.4 million tons. The production in other regions like Africa and Oceania remains relatively small in comparison.

The global pork trade is equally dynamic. In 2022, the major exporters included the European Union, the United States, and Canada. Key importers were China, Japan, and Mexico. The shifting demands and production capacities have led to fluctuating trade patterns, impacting global pork prices and market stability.

Figure 3. Evolution of global pork production (GDP in 1000 tons)

Pork Industry in the European Union

The European pork industry faced a challenging year in 2022, marked by a decline in production and various economic pressures. The EU’s pork production fell by approximately 5%, equating to a loss of over 12.6 million pigs for slaughter. Germany, historically one of the largest producers, saw a significant 10% reduction in output due to ongoing economic and sanitary crises. Spain, while typically a growing market, experienced its first production decline since 2014 due to increased piglet mortality rates from health issues.

Despite these challenges, some regions showed resilience. France managed a relatively smaller production decrease of 2%, maintaining its position as a key player in the European market. The economic environment, characterized by rising inflation and high feed costs, pushed pork prices to record levels across the continent, with French pork prices ranking high in Europe, just behind Spain.

The consumption patterns within the EU also varied significantly. Countries like Denmark and Spain exhibited high per capita pork consumption rates, while others like the United Kingdom and Italy showed more moderate consumption levels. This disparity reflects both cultural preferences and economic conditions across the region.

Figure 4. Evolution of pork production in the main EU countries (tons, from a base of 100 in 2005)

The French Pork Industry

In France, the pork industry in 2022 faced a year of significant adjustments. The country produced 2.19 million tons of carcass weight equivalent, a 3% decrease from the previous year. This decline was attributed to reduced slaughter weights and lower export volumes of live pigs. Despite these challenges, France remained the third-largest pork producer in the EU, following Spain and Germany.

Regionally, pork production is concentrated in areas like Brittany and Pays de la Loire. Brittany alone accounts for a substantial portion of the national production. The distribution of pork farms across France highlights the regional specialization, with significant variations in production volumes from one region to another.

Figure 5. Suppliers to France (percentage of total imports)

French pork exports faced hurdles due to reduced demand from China, which saw a 35% drop in imports from France in 2022. However, increased sales to other Asian markets like the Philippines and Japan partially offset this decline. In terms of value, the higher pork prices helped mitigate the impact of lower export volumes, with total export values reaching 1.76 billion euros.

Figure 6. Export targets for France (percentage of total exports)

Economic and Production Challenges

The pork industry globally and within the EU faces several ongoing challenges. Rising feed costs, largely driven by global commodity price increases, have significantly impacted production costs. In Europe, the economic downturn and ongoing health crises like ASF and PRRS (Porcine Reproductive and Respiratory Syndrome) continue to challenge producers.

In France, inflation and high production costs have led to a tightening of profit margins for pig farmers. The high costs of feed and energy, coupled with lower production volumes, have made it difficult for many producers to remain profitable. The industry has responded with efforts to improve efficiency and sustainability, though these measures take time to implement and yield results.

Future Outlook

In Asia, China’s recovery from ASF will likely stabilize, but the focus will shift towards improving biosecurity and production efficiency. In Europe, the industry will need to navigate economic challenges and health crises while adapting to changing consumer preferences towards more sustainable and ethical production practices.

For France, the key to future success will lie in balancing production efficiency with market demands. Investments in technology, biosecurity, and sustainable practices will be crucial. Additionally, expanding export markets beyond traditional partners will help mitigate the risks associated with market fluctuations.

The pork industry, both globally and within the EU, is at a pivotal point. The combination of economic pressures, health challenges, and shifting market dynamics necessitates strategic adjustments. By focusing on efficiency, sustainability, and market diversification, the industry can navigate these challenges and continue to thrive in the coming years.

The report can be read in full here.

By Twan van Gerwe, DVM PhD Dipl ECPVS, Technical Director
Dr. Inge Heinzl, Editor

 

One of the biggest challenges in swine production is keeping the modern, hyperprolific sow healthy and in good shape so that she can wean large, healthy litters and maintain her high reproductive performance.

Unfortunately, sows often suffer from stress and increased systemic inflammation around farrowing and during lactation. This leads to impaired feed intake and disturbed endocrine homeostasis, negatively affecting reproductive and litter performance.

The key to increasing the efficiency of pig production is to reduce the metabolic burden of sows while maintaining the reproductive performance of high-yield sows. A deep understanding of the complex interplay between environmental factors, sow well-being, health, and productivity is necessary to implement enhanced nutritional regimens and meticulous management practices.

Why does oxidative stress occur in today’s sows?

Nowadays, hyperprolific sows produce between 30 and 40 weaned piglets per year and are at a higher risk of suffering from stress. What are the reasons?

A high number of piglets causes oxidative stress

Oxidative stress occurs when reactive oxygen species (ROS) are produced faster than the body’s antioxidant mechanisms can neutralize them and cause damage to lipids, proteins, and DNA. During gestation, the sow needs high amounts of energy to provide for the fetuses. This energy is produced in the placental mitochondria. The placenta, therefore, is a place of active oxygen metabolism during gestation and a source of oxidative stress. In hyperprolific sows, a higher number of fetuses need even more energy to grow. Consequently, ROS production and the risk for intrauterine growth retardation (IUGR) increases (Figure 1). Moreover, evidence shows that the body’s antioxidant potential is reduced in late gestation and after parturition (Szczubial, 2010), resulting in increased oxidative stress biomarkers (Yang, 2023). Increased milk production for large litters demands a substantial amount of energy, risking similar oxidative distress. Therefore, both the final phase of gestation and the subsequent lactation period are predestined for oxidative stress, which has been demonstrated by reduced TEAC (Trolox equivalent antioxidant capacity) levels during these phases (Lee et al., 2023).

Figure 1. Illustration of the effect of oxidative stress on the fetus: intrauterine growth retardation (IUGR) (adapted from Yang et al., 2023)

Heat and ambient stress also contribute

The reproductive sow produces lots of heat.  From the beginning of gestation, the sow’s thermoneutral zone decreases. This, however, does not always correspond with the ambient conditions. Especially during the last days of gestation, the discrepancy is exceptionally high as everything is prepared for the newborn piglets, which need a temperature of about 27-35°C. The sow, on the contrary, would be happy with 18-22°C. Additionally, changes around farrowing – moving to the farrowing unit, social stress, change of feed, and the preparation for parturition – exert additional stress for the sows.

Why does the inflammation level increase?

After parturition, systemic inflammation is a normal phenomenon: the reproductive organs have sustained injuries during the parturition process and require remodeling. Inflammation is a natural and desired process, to repair the tissues and return to a normal status. However, inflammation is increased in modern sows, adversely affecting their inflammatory balance. Some possible underlying reasons are:

1. The high numbers of piglets need a lot of space in the uterus, often leading to damage of the uterine tissue and an inflammatory response in the sows. Lee et al. (2023) found significantly (p<0.10) higher TNF-α concentrations in sows with litters of 15-20 piglets than in sows with 7-14 piglets. TNF-α is a biomarker of inflammation.
2. Pathogenic infections – particularly infections of the reproductive tract – can induce a prolonged or excessive inflammatory state. A further reason can be the need for more obstetric interventions in hyperprolific sows, which can injure the birth canal or the uterus.
3. Imbalanced nutrition: Excessive backfat is associated with a higher expression of proinflammatory cytokines, and feed contaminated with mycotoxins can impair the sow’s immunocompetence.

Biomarkers can inform us about the oxidative status

Biomarkers are naturally occurring molecules that help us identify diseases or physiological processes. They provide insights into the oxidative state and inflammatory processes.

Anti-oxidative biomarkers

To check the anti-oxidative capacity, the “beneficial” substances, or antioxidants, can be quantified. These substances can neutralize free radicals or be neutralized by them. Higher levels of antioxidants indicate better antioxidant capacity; when antioxidants are abundant, fewer oxidizable substances have undergone oxidation.

Examples of antioxidant biomarkers:

Total Antioxidant Capacity (T-AOC): represents the synergistic interaction effects of all antioxidants in a matrix (E.g., diet or body fluids). It’s a global measure of non-enzymatic antioxidant efficiency. Various assays, like Trolox Equivalent Antioxidant Capacity (TEAC), which measures a substance’s antioxidant capacity compared to Trolox, can measure T-AOC.

Glutathione Peroxidase (GSH-Px) belongs to the peroxidase family and converts hydrogen peroxide to water.

Catalase (CAT): scavenges ROS. Its activity can predict oxidative stress.

Superoxide Dismutase (SOD): catalyzes the dismutation of superoxide radicals to oxygen and hydrogen peroxide.

Oxidative biomarkers

Oxidative stress biomarkers, the ‘negative’ substances, can also serve as general biomarkers. These include free radicals with oxidant capacity or intermediate/final oxidation products. Ideally, their levels should be minimized.

Examples of oxidative stress biomarkers:

Thiobarbituric acid reactive substances (TBARS): to measure lipid peroxidation products in cells, tissues, and body fluids.

Reactive oxygen species (ROS) or free radicals: unstable, oxygen-containing molecules that react with other molecules in a cell. They might damage DNA, RNA, and proteins and cause cell death. Hydrogen Peroxide (H₂O₂) is a ROS produced during normal cellular metabolism, which causes oxidative damage at excessive levels.

Malondialdehyde (MDA): a final product of oxidative fat degradation and, therefore, a biomarker for lipid peroxidation.

Pro-inflammatory biomarkers

Like oxidative stress, the interplay between pro- and anti-inflammatory signals helps develop the proper immune response for the appropriate duration.

Examples of Pro-inflammatory biomarkers or molecules produced in the case of inflammation:

• Plasma Adenosine Deaminase (ADA-1 and ADA-2): involved in immune regulation, with ADA-1 inhibiting pro-inflammatory responses and ADA-2 supporting immune cell functions.
• Interleukins (IL-1α and IL-1β), IL-6: IL-1α and IL-1β are associated with inflammatory diseases, IL-6: is produced during inflammation and acute-phase response.
• Tumor Necrosis Factor α (TNF-α): endogenous pyrogen that induces fever and promotes inflammation.
• C-reactive Protein (CRP): liver-produced acute-phase protein responding to inflammation.

Procalcitonin (PCT) is produced by the liver during infections and helps detect bacterial infections.

Examples of anti-inflammatory substances – the “good ones”:

• Interleukines – IL-4, IL-10: inhibit the function of the macrophages and act, therefore, anti-inflammatory
• Cortisol: anti-inflammatory and immune-suppressive
• ACTH: stimulates the production and release of cortisol

Higher stress or infection level lowers performance in sows and piglets

As mentioned, hyperprolific sows suffer from higher oxidative stress, especially during late gestation, parturition, and lactation. Additionally, systemic inflammation occurs to repair the injured tissues to facilitate the healing of the birth canal and remodeling of the uterus to establish the subsequent pregnancy. To this purpose, an inflammatory cascade, triggered by the injuries due to gestation and parturition, involves the release of critical (pro-inflammatory) mediators such as TNF-α and IL-6, leading to the activation of acute phase proteins.

After triggering inflammatory pathways, anti-inflammatory pathways must also be activated to reestablish homeostasis in the reproductive organs (Serhan & Chiang, 2008). Alterations at the onset of anti-inflammatory pathways and exacerbated activation and maintenance of inflammatory pathways can lead to uncontrolled inflammation and the onset of reproductive disease in sows (Kaiser et al., 2018), as well as reduced feed intake and insufficient milk production, resulting in poorly growing piglets and lower weaning weights or piglets suffering from clinical infectious diseases such as diarrhea. If possibly homeostasis cannot be restored, the sow is at risk of contracting diseases like post-partum dysgalactia syndrome (PPDS), lameness, and impaired fertility.

Targeted use of polyphenols can mitigate inflammation and improve the oxidative status of sows

There are several experiments showing the beneficial effects of natural compounds. Especially polyphenols, disposing of phenyl rings and two or more hydroxyl substituents, are perfect radical scavengers and proven antioxidants (Chen, 2023). Phytogenic substances that have anti-inflammatory effects can be found in the families of polyphenols as well as terpenoids, flavonoids, saponins, and tannins (Bunte et al., 2019; Ge et al., 2022; Ginwala et al., 2019; Santos Passos et al., 2022; Ambreen and Mirza, 2020).

Here are some examples showing the beneficial effects of phytochemicals:

1. Primiparous sows fed with Moringa oleifera leaf meal, rich in polyphenols, saponins, and tannins, illustrate the potential of phytomolecules: serum levels of T-AOC (total anti-oxidative capacity), were increased in late gestation and during lactation, while MDA was reduced. Additionally, piglets that received Moringa oleifera meal showed the highest serum CAT and SOD activities. The meal significantly decreased the farrowing length and number of stillbirths, while there was an increasing trend in the number of live‐born piglets (Sun et al., 2020).
2. The polyphenol Daidzein, a member of the class of compounds known as isoflavones (200 mg/kg during gestation), increased the total antioxidant capacity (T-AOC) and the activities of glutathione peroxidase and superoxide dismutase. Additionally, it elevated the level of immunoglobulin G and increased the number of piglets born and born alive per litter (Li et al., 2021).
3. Glycitein, a polyphenol occurring in the isoflavone fraction of soy products, applied during late gestation and lactation increased the total antioxidant capacity and SOD activity during the first 18 days of lactation and the CAT and GSH-Px activity in mid-lactation. Plasma MDA level was reduced from late gestation to the 18^th day of lactation. The enhanced oxidative status of the sow resulted in a higher daily gain of the piglets and a higher weaning weight of the litter (Hu et al., 2015).
4. Meng et al. (2018) tested Resveratrol (300 mg/kg), a stilbenes polyphenol, in sows from day 20 of gestation until farrowing. They saw noticeably higher GSH-Px, SOD, and CAT activities, as well as lower contents of MDA and H₂O₂ in the placental tissue, improving the antioxidant status of sows and piglets.
5. Xu et al. (2022) fed silymarin to sows in late gestation. They observed that IL-1ß concentration in the blood sample on the 18^th day of lactation was reduced in the supplemented group. The altered fecal microbiota was associated with variations in inflammatory factors, suggesting that silymarin modulates microbiota in the gut and may improve the health of lactation sow.

Phytochemicals support sows against oxidative and inflammatory stress

The above-presented examples show that phytochemicals, particularly those developed to have a potent anti-inflammatory and anti-oxidative capacity, have a high potential to alleviate oxidative stress in pregnant and lactating sows and reduce inflammation when applied in sow diets. Consequently, a broader use of these natural substances should be considered to reduce the metabolic burden of sows and increase the efficiency of pig production.

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by Madalina Diaconu, Global Manager Gut Health, EW Nutrition

Coccidiosis, caused by Eimeria spp., is a major challenge in poultry production, leading to significant economic losses. Historically, control strategies have relied on chemical anticoccidials and ionophores. However, the emergence of drug-resistant Eimeria strains and consumer concerns about chemical residues necessitate alternative solutions. Phytogenics, especially tannins and saponins, offer promising natural solutions to be included in programs for coccidiosis control. More and more independent research highlights the potential of these natural compounds to enhance poultry health and productivity.

Efficacy of Tannins and Saponins in Coccidiosis Control

Phytogenics are plant-derived bioactive compounds known for their antimicrobial, antioxidant, and immunomodulatory properties. Among these, tannins and saponins have shown particular promise in supporting coccidiosis control.

The challenge: Preventing the spread of infections and mitigating subclinicial coccidiosis before it reaches this stage.

Tannins

Tannins are polyphenolic compounds found in various plants. They exhibit strong antimicrobial activity by binding to proteins and metal ions, disrupting microbial cell membranes, and inhibiting enzymatic activity.

Anticoccidial Activity: Tannins have been shown to interfere with the life cycle of Eimeria. Studies demonstrate that tannins can reduce oocyst shedding and intestinal lesion scores in infected birds (Abbas et al., 2017).

Immune Modulation: Tannins enhance immune responses by promoting the proliferation of lymphocytes and the production of antibodies, which help in the clearance of Eimeria infections (Redondo et al., 2021).

Saponins

Saponins are glycosides with surfactant properties, capable of lysing cell membranes of pathogens. They also stimulate immune responses, enhancing the host’s ability to fight infections.

Membrane Disruption: Saponins disrupt the cell membranes of Eimeria, leading to reduced parasite viability and replication (Githiori et al., 2004).

Immune Enhancement: Saponins stimulate the production of cytokines and enhance the activity of macrophages, improving the overall immune response against coccidiosis (Zhai et al., 2014).

Independent Research Evidences Phytogenics’s Role in Supporting Programs for Coccidiosis Control

Numerous studies have evaluated the efficacy of phytogenics in coccidiosis control. Here, we highlight key findings from peer-reviewed research:

Abbas et al. (2012): This study reviewed various botanicals and their effects on Eimeria species in poultry. The authors concluded that tannins and saponins significantly reduce oocyst shedding and lesion scores, comparable to conventional anticoccidials.

Allen et al. (1997): The authors investigated the use of dietary saponins in controlling Eimeria acervulina infections. The study found that saponin-treated birds exhibited lower oocyst counts and improved weight gain compared to untreated controls.

Masood et al. (2013): This study explored the role of natural antioxidants, including tannins, in controlling coccidiosis. The results indicated that tannins reduced oxidative stress and improved intestinal health, leading to better performance in broiler chickens.

Idris et al. (2017): The researchers assessed the potential of saponin-rich plant extracts against avian coccidiosis. The findings demonstrated significant reductions in oocyst output and lesion severity, highlighting the potential of saponins as effective anticoccidials.

Hailat et al. (2023): The researchers studied three phytogenic formulations against a control group with chemical drugs. The study concluded that phytogenic blends can be safely used as alternatives to the chemically synthesized drugs, either alone or in a shuttle program, for the control of poultry coccidiosis.

El-Shall et al. (2021): This review article highlights research findings on phytogenic compounds which showed preventive, therapeutic, or immuno-modulating effects against coccidiosis.

Despite initial skepticism, the growing body of evidence supports the efficacy of phytogenics in supporting coccidiosis control. Tannins and saponins, in particular, have shown significant potential in reducing parasite load, improving intestinal health, and enhancing immune responses. These natural compounds offer several advantages over traditional chemical treatments, including lower risk of resistance development and absence of harmful residues in meat products.

Challenges and Promises

While the efficacy of phytogenics is well-supported, challenges remain, especially with lower-quality products that may display variability in plant extract composition, in their standardization of doses, and in ensuring consistent quality. At the same time, these compounds are not silver bullets, and no producer should make unreasonable claims.

As far as the mode of action is concerned, the evidence is becoming clear: phytogenics, particularly tannins and saponins, are effective in mitigating gut health challenges and supporting bird performance when challenged. Their natural origin, coupled with potent antimicrobial and immunomodulatory properties, makes them suitable for sustainable poultry production. As the poultry industry seeks to reduce reliance on chemical drugs, phytogenics represent a viable and promising solution.

References

Abbas, R. Z., Iqbal, Z., Blake, D., Khan, M. N., & Saleemi, M. K. (2011). “Anticoccidial drug resistance in fowl coccidia: the state of play revisited”. World’s Poultry Science Journal, 67(2), 337-350. https://doi.org/10.1017/S004393391100033X

Allen, P. C., Danforth, H. D., & Levander, O. A. (1997). “Interaction of dietary flaxseed with coccidia infections in chickens”. Poultry Science, 76(6), 822-828. https://doi.org/10.1093/ps/76.6.822

El-Shall, N.A., El-Hack, M.E.A., et al. (2022). “Phytochemical control of poultry coccidiosis: a review”. Poultry Science, 101(1) 101542. https://doi.org/10.1016/j.psj.2021.101542

Idris, M., Abbas, R. Z., Masood, S., Rehman, T., Farooq, U., Babar, W., Hussain, R., Raza, A., & Riaz, U. (2017). “The potential of antioxidant rich essential oils against avian coccidiosis”. World’s Poultry Science Journal, 73(1), 89-104. https://doi.org/10.1017/S0043933916000787

Hailat, A.M., Abdelqader, A.M., & Gharaibeh, M.H. (2023). “Efficacy of Phyto-Genic Products to Control Field Coccidiosis in Broiler Chickens”. International Journal of Veterinary Science, 13(3), 266-272. https://doi.org/10.47278/journal.ijvs/2023.099

Masood, S., Abbas, R. Z., Iqbal, Z., Mansoor, M. K., Sindhu, Z. U. D., & Zia, M. A. (2013). “Role of natural antioxidants for the control of coccidiosis in poultry”. Pakistan Veterinary Journal, 33(4), 401-407.

Redondo, L. M., Chacana, P. A., Dominguez, J. E., & Miyakawa, M. E. (2021). “Perspectives in the use of tannins as alternative to antimicrobial growth promoter factors in poultry”. Frontiers in Microbiology, 12, 641949. https://doi.org/10.3389/fmicb.2021.641949

Zhai, H., Liu, H., Wang, S., Wu, J., & Kluenter, A. M. (2014). “Potential of essential oils for poultry and pigs”. Animal Nutrition, 2(4), 196-202. https://doi.org/10.1016/j.aninu.2016.12.004