Rancidity in fats and oils: Considerations for analytical testing
by Ajay Bhoyar, Global Technical Manager – Poultry, EW Nutrition
Rancidity testing is essential in the feed industry, as a key indicator of product quality and shelf life. It is conducted to determine the level of oxidation in samples of feed or feed ingredients and it can be performed through a number of analytical methods.
Rancidity is the process by which fats and oils in food become degraded, resulting into off-odor/flavor, taste, and texture. This process is caused by the oxidation of unsaturated fatty acids and can be accelerated by factors such as exposure to light, heat, and air. Rancidity can occur naturally over time, but it can also be accelerated by improper storage or processing of animal products. Fats are highly susceptible to degradation due to their chemical nature.
How does oxidative rancidity occur?
Oxidation occurs when an oxygen ion replaces a hydrogen ion within a fatty acid molecule and higher numbers of double bonds within the fatty acid increase the possibility of autoxidation. Oxidative rancidity results from the breakdown of unsaturated fatty acids in the presence of oxygen. Light and heat promote this reaction, which results in the generation of aldehydes and ketones – compounds which impart off-odors and flavors to food products. Pork and chicken fat demonstrate a higher degree of unsaturated fatty acids compared with beef fat and are therefore more prone for rancidity.
Oxidation: a three-step process
Fat/oil oxidation is a three-step process (Initiation, Propagation and Termination). Therefore, the oxidation products depend on the time. In the first phase, called Initiation, the formation of free radicals begins and accelerates.
Once the initial radicals have formed, the formation of other radicals proceeds rapidly in this second phase called Propagation. In this part of the process, a chain reaction of high energy molecules, which are variations of free radicals and oxygen, are formed and can react with other fatty acids. These reactions can proceed exponentially, if not controlled. Also in this phase, the rate of peroxide radical formation will reach equilibrium with the rate of decomposition to form a bell-shaped curve.
In the final phase, called Termination, the starting material has been consumed, and the peroxide radicals, as well as other radicals decompose into secondary oxidation by-products such as esters, short chain fatty acids, polymers, alcohols, ketones and aldehydes. It is these secondary oxidation by-products, which can negatively affect the growth and performance of animals.
Fig. 1: Oxidation: a three-phase series of reactions
Antioxidants preserve the quality of rendered products
Chemical antioxidants are used in the rendering industry to help preserve the quality of animal by-products. Synthetic antioxidants, such as BHA, BHT, and ethoxyquin, can help prevent the oxidation of these by-products, which can cause them to become rancid. These chemical antioxidants are added in small amounts to the raw materials prior to rendering or can be incorporated into the finished products to help extend their shelf life and maintain their nutritional value. It is important to note that the use of antioxidants in the rendering industry must be done in compliance with regulations and guidelines set forth by the FDA and other governing bodies.
Natural antioxidants like tocopherols, rosemary extract, ascorbyl palmitate, etc. are also used to prevent oxidation and maintain the freshness of rendered products, if the chemical antioxidants cannot be used.
Rancidity testing is the process of determining the level of rancidity in a product. Testing for level of rancidity is used widely as an indication of product quality and stability.
There are several methods used for rancidity testing, including:
Organoleptic rancidity testing
Oxidation of fats and oils leads to a change in taste, smell, and appearance. Organoleptic testing involves using the senses (sight, smell, taste) to determine the level of rancidity. Trained testers will examine the product for visual signs of spoilage, such as discoloration or the presence of crystals, and will also smell and taste the product to detect any off-flavors or odors.
Chemical & instrumental rancidity testing
Chemical testing involves using chemical methods to measure the level of rancidity. One common method is the peroxide value test, which measures the amount of peroxides (indicators of rancidity) in the product. Another method is the p-anisidine test, which measures the level of aldehydes (another indicator of rancidity) in the product.
Peroxide Value (PV) testing determines the amount of peroxides in the lipid portion of a sample through an iodine titration reaction targeting peroxide formations. Peroxides are the initial indicators of lipid oxidation and react further to produce secondary products such as aldehydes. Because peroxide formation increases rapidly during the early stages of rancidification but subsequently diminishes over time, it is best to pair PV testing with p-Anisidine Value to obtain a fuller picture of product quality.
Fig.2: Oxidation products changes with time
p-AV is a determination of the amount of reactive aldehydes and ketones in the lipid portion of a sample. Both compounds can produce strong objectionable flavors and odors at relatively low levels. The compound used for this analysis (p-Anisidine) reacts readily with aldehydes and ketones and the reaction product can be measured using a colorimeter. Samples that are particularly dark may not be the most applicable for this analysis as the colorimeter may not be able to adequately measure the wavelength required.
Thiobarbituric acid reactive substances (TBARS) are a byproduct of lipid peroxidation (i.e. as degradation products of fats). This can be detected by the TBARS assay using thiobarbituric acid as a reagent. TBA Rancidity (TBAR) also measures aldehydes (primarily malondialdehyde) created during the oxidation of lipids. This analysis is primarily useful for low-fat samples, as the whole sample can be analyzed rather than just the extracted lipids.
The Instrumental testing involves using instruments to measure the level of rancidity.
One common method is the use of a gas chromatograph, which can detect the presence of volatile compounds that indicate rancidity.
FTIR method can detect changes in the chemical makeup of the product that indicate rancidity.
Free Fatty Acids (FFA)
FFA testing determines the fatty acids that have been liberated from their triglyceride structure. A titration is performed on the extracted fat from a specific sample. The FFA content is then determined through a calculation of the amount of titrant used to reach the final result. Knowing what type of fat or fat containing product is being tested is important for this analysis to ensure that the appropriate calculation is applied. As the test does not differentiate between fatty acid types, samples with high palmitic or lauric fatty acid composition should have a different calculation factor applied so as to accurately represent the free fatty acid result.
Oxidative Stability Index (OSI)
OSI indicates how resistant a sample is to oxidation. Samples are subjected to heat while air is injected – a process which accelerates oxidation reactions. The samples are monitored, and the time required for the sample to reach an inflection point is determined. This test is useful when testing the efficacy of an antioxidant added to a product. Antioxidants should inhibit free radical propagation and thus increase a samples ability to hold up under the stressing conditions imposed by the OSI analysis. The measuring instrument, the Rancimat.
Analytical testing considerations in rendering operations
It is common to perform regular analytical testing in a rendering operation as a part of quality control and quality assurance program. There are several methods for testing rancidity in rendering operations. It is important to choose the appropriate method based on the type of product and the desired level of accuracy.
The results of rancidity testing are used to monitor and control the rendering process to prevent or minimize rancidity. This may involve adjusting processing conditions, using antioxidants, or implementing other measures to reduce oxidation.
Current state of oxidation
Peroxide Value (PV)
Secondary Oxidatives (p-Anisidine, TBARS)
PV:< 5 meq/kg
Potential for future oxidation
Oxidative Stability Index (OSI)
Analyze the stability of oil/fats
Value decreases as the antioxidant gets sacrificed
Table. 1: Analytical testing considerations for rendering
Rancidity is a common problem in rendered animal products. It can have detrimental effects on both the quality and safety of the product. It is caused by the oxidation of fats and oils, leading to the formation of harmful compounds such as free radicals and hydroperoxides. The best way to prevent rancidity is through proper storage, packaging, and handling techniques, as well as the use of antioxidants to slow down the oxidation process. It is important for manufacturers and consumers to be aware of the potential for rancidity in rendered animal products and take the necessary precautions to ensure the safety and quality of the product.
Salmonella in poultry: What are the most effective natural solutions?
feedby Dr. Inge Heinzl, EW Nutrition
Salmonella infection in poultry is a problem for the producer because of the performance losses of his flock. At the same time, products of salmonella-contaminated animals pose a severe risk to human health. In the USA, Salmonellosis in poultry is estimated to cost $ 11.6 billion each year (Wernicki et al., 2017) and more than € 3 billion in the EU (Ehuwa, 2021). As the use of antibiotics needs to be reduced to keep them effective, Salmonella control in poultry requires new solutions. This article shows how organic acids and phytomolecules can help to fight this problematic disease.
Salmonellosis: what it is, how it works, and why it’s such a problem
Salmonellosis is a zoonosis, meaning that it can be easily transferred from animals to humans. The transfer can occur via different routes:
Direct contact with an infected animal
Handling or consuming contaminated animal products such as eggs or raw meat from pigs, turkeys, and chicken
Contact with infected vectors (insects or pets) or contaminated equipment
Frozen or raw chicken products, as well as the eggs of backyard hens, are the most frequent causes of animal-mediated Salmonella infections in humans. The following graphic shows a clear relationship between the occurrence of Salmonella in layer flocks and the event of disease in humans:
The impact of Salmonella on poultry depends on the bird’s age
Within the poultry flock, there are two ways of spreading: the fecal-oral way (horizontal infection) or the infection of the progeny in the egg (vertical infection). The effects of the disease depend on the age of the birds: the younger the animals, the more severe the impact.
If the brood eggs already carry salmonellae, the hatchability dwindles. During their first month of life, infected chicks show ruffled downs and higher temperatures. Diarrhea leads to fluid losses and frequently to the chicks’ death.
Adult animals usually do not die from Salmonellosis; often, the infection remains unnoticed. During a substantial acute salmonella outbreak, the animals show weakness and diarrhea. They lose weight, resulting in decreased egg production in layers and worse growth performance in broilers. The birds need more water to compensate for the fluid losses, and their crowns and jowls appear pale.
Salmonella protects itself through an intelligent infection style
Salmonellae have developed a clever way to protect themselves. After they arrive in the gut, they attach to the epithelial cells and form small molecular “syringes” to inject divers substances into the gut cells (Type-3-injection system). These signaling substances make the gut cells bulge their membranes and enclose the bacterium. Finally, the manipulated gut cell absorbs the Salmonella, the host “allows” the bacterium to enter, and it can proliferate in the gut cells (Fischer, 2018).
When an antibiotic is attacking the bacterium, Salmonellae stop their cell division. Since many antibiotics are only effective against bacteria during cell division and growth, Salmonellae survive the attack by staying as dormant variants or persisters until the treatment stops (Fischer, 2018).
Salmonellae – a big “family”
The genus of Salmonella consists of more than 2600 serovars (Ranieri et al., 2015), of which less than 100 are relevant for humans (CDC, 2020). More than 1500 serovars belong to the Salmonella enterica subspecies that colonize the intestinal tract of warm-blooded animals. These serovars are responsible for 99 % of salmonella infections (Mendes Maciel et al., 2017). The main serovars relevant for poultry are S. Gallinarum and S. Pullorum, but also S. Enteritidis, Typhimurium, and in recent years, S. Kentucky, S. Heidelberg, S. Livingstone, and S. Mbandaka (Guillén et al., 2020).
The zoonosis Salmonellosis must be controlled
Several Salmonella serovars are critical for animals and humans. Since more than 91,000 salmonellosis cases are reported for Europe and more than 1.35 million for the USA every year (EFSA, 2022; FDA, 2020), their spread must be prevented by all means. Governments have enacted some laws to curtail this disease. The EU, for example, implemented extended control programs for zoonotic diseases, with Salmonella set as a priority. These programs include the provision of scientific advice, targets for reducing Salmonella in poultry flocks, and restrictions on the trade of products from infected flocks.
For farmers and vets, this means the obligation to notify the occurrence of the disease to the authorities. Depending on the country, it also entails compulsory vaccination and the documentation of hygienic measures. In the EU, due to the risk of developing resistances, the EFSA recommends limiting the use of antimicrobials to individual cases, e.g., to prevent inordinate suffering of animals.
Prevention of Salmonella infection is the key
The best strategy for salmonella control is prevention based on three key points (Visscher, 2014):
Preventing the introduction of Salmonella into the farm/flock through effective hygiene measures
Preventing the spread of the pathogens within a flock/farm
Prophylactic measures to recover immune resistance of the animals against Salmonella infection
For this purpose, the following steps are requested/recommended:
1. Keeping the litter dry
The use of well-absorptive material such as wood shavings, straw pellets, or straw granulates and regular removal of the used litter is recommended. The animals must be controlled for diarrhea to avoid wet droppings. The water supply must be adequate; an excessive water supply wets the litter.
2. Providing a clean environment
To keep the poultry house clean, broken eggs and dead animals (potential sources of infection) must be removed. In general, the houses should be cleaned and disinfected before every restocking.
Clean feed and water are essential; therefore, feed should not be stored outside but be kept dry and protected from pests and rodents. The feeding of the animals should take place inside to avoid contamination by wild birds. Concerning the water for drinking, the flow rate must be high enough to provide the birds with sufficient water but not too high that the floor gets wet. The troughs must be clean from droppings.
3. Limiting contacts
To limit the spread of Salmonella, only a restricted number of persons can have access to the flocks. They must wear clothes, and instruments should be exclusively used for the respective poultry house.
Knowing the optimal growth conditions for Salmonella facilitates control
Salmonellae are a genus in the family of Enterobacteriaceae. They are gram-negative, rod-shaped (size: approx. 2 µm), glucose-fermenting facultative anaerobes that are motile due to peritrichous flagella. Since Salmonellae do not form spores, they can be easily destroyed by heating them to 60°C for 15-20 min (Forsythe, 2001), especially in food/feed with higher water content.
For the storage of food, Bell and Kyriakis (2002) found that most serovars of Salmonella will not grow at temperatures lower than 7°C and a pH lower than 4.5. Wessels et al. (2021) showed optimal growth conditions for Salmonella: temperatures between 5 and 46°C (optimum 38°C), a water activity of 0.94-0.99, and a pH of 3.8-9.5.
A high fat content in the feed or food increases the likelihood of infection with Salmonella because the fat protects the bacteria during the passage through the stomach. Doses of 10 to 100 Salmonella cells can already pose a severe risk (University of Georgia, 2015).
Natural alternatives to antibiotics: effective Salmonella control?
To reduce the incidence of Salmonella while simultaneously lowering the use of antibiotics in animal production, there are different possibilities. On the one hand, veterinary medicine offers vaccines. On the other hand, the feed industry provides additives that strengthen the immune system, improve gut health, or support the animals in another manner. Other than pro- and prebiotics, the main active ingredient categories for such additives are organic acids and phytomolecules.
Organic acids worsen the conditions for Salmonella
Already in ancient Egypt, the method of fermentation and the generated acids have been used for the conservation of food (Ohmomo et al., 2002). Nowadays, it is a standard tool to protect feed (silage) and food from spoilage. Also for animals, organic acids added to the feed or the water have proven helpful against pathogens. These modes of action can be combined against Salmonella: reducing the pathogen load in the feed to limit the intake of bacteria and fighting against these pathogens in the animal.
Organic acids reduce Salmonella in feed materials
In general, the antimicrobial activity of organic acids in feed is based on lowering the pH (Pearlin et al., 2019). pH-sensitive bacteria such as Salmonella minimize their proliferation at a pH <5. Additionally, the organic acids attack bacteria directly. The acid’s undissociated and more lipophilic form penetrates the bacterial cell membrane. At the neutral pH within the cell, the acid dissociates, releases protons, and lowers the pH, leading to the impediment of metabolic processes in the cell. The cell spends a lot of energy trying to get the pH back to neutral (Mroz et al., 2006). Additionally, the anions become toxic for the cell metabolites and disrupt the membrane (Russel, 1992).
Depending on the acid, the efficacy against Salmonella varies (see figure 3). Formic acid shows the highest effect, followed by fumaric acid. Then, lactic, butyric, and citric acid follow, showing lower efficacy.
Trials prove the efficacy of organic acids
An in-vitro trial was conducted at a commercial research facility in the US to test the efficacy of Acidomix AFL, a liquid mixture of propionic and formic acid, against Salmonella. The bacterial strain used in these studies was nalidixic acid-resistant Salmonella typhimurium. The bacteria were maintained in broth cultures of tryptic soy broth.
They were added to 5 g of dry feed in a 50 ml tube to a final concentration of 40,000 CFU/g. Next, Acidomix AFL was added to the desired inclusion rate, and the samples were incubated at room temperature. After 18 to 72 hours of incubation, viable bacteria were counted using the plate count method.
Results: As shown in figure 4, the trial found that at an inclusion rate of 2.0 %, Salmonella inhibition was nearly 100 %. Already at a 0.4 % inclusion rate, Salmonella could be reduced by 45-60 %, showing a clear dose dependency.
Phytomolecules combat Salmonella through complex modes of action
Plants produce phytogenic substances to protect themselves from molds, yeasts, and bacteria, among others. After several purification steps, these phytomolecules can be used to fight Salmonella in poultry. They work through different modes of action, from attacking the cell wall (terpenoids and phenols) to influencing the genetic material of the pathogenic cells or changing the whole morphology of the cell.
Due to the different modes of action, it was long thought that there would be no resistance development. Still, Khan et al. (2009) found some microorganisms such as multidrug-resistant E. coli, Klebsiella pneumoniae, S. aureus, Enterococcus faecalis, Pseudomonas aeruginosa, and Salmonella typhimurium can show a certain – perhaps natural – resistance to some components of herbal medicines.
Gram-negative bacteria such as Salmonella are usually less attackable by phytomolecules because the cell wall only allows small hydrophilic solutes to pass; however, phytomolecules are hydrophobic. However, mixing the phytomolecules with an emulsifier facilitates the invasion into the cell. Their efficacy depends on their chemical composition. It is also decisive if single substances or blends (possible positive or negative synergies) are used.
The best-clarified mode of action is the one of thymol and carvacrol, the major components of the oils of thyme and oregano. They can get into the bacterial membrane and disrupt its integrity. The permeability of the cell membrane for ions and other small molecules such as ATP increases, decreasing the electrochemical gradient above the cell membrane and the loss of energy equivalents.
Trials show the efficacy of phytomolecules against Salmonella
Two different phytogenic compositions were tested for their efficacy against Salmonella.
Trial 1: Blend of phytomolecules and organic acids shows best results in an in-vitro assay
To evaluate its potential as a tool for antibiotic reduction, a trial was conducted to test the antimicrobial properties of Activo Liquid, a mixture of selected phytomolecules and an organic acid designed for application in water. The laboratory test was carried out at the Veterinary Diagnosis Department of Kasetsart University in Thailand. Standardized suspensions [1×104 CFU/ml] of three poultry-relevant Salmonella strains were incubated in LB medium, either without or with Activo Liquid. The tests were run at concentrations of 0.05%; 0.1%; 0.2% and 0.4%. After incubation at 37°C for 6-7 hours, serial dilutions of the cell suspensions were transferred onto LB agar plates and incubated for 18-22h at 37°C. Subsequently, colonies (CFU/ml) were determined.
Results: Activo Liquid was found to be growth-inhibiting to all Salmonella strains from a concentration of 0.1% onwards. At 0.2%, Activo Liquid already exhibited bactericidal efficacy against all tested Salmonella isolates, which was confirmed at a concentration of 0.4%.
Trial 2: Blend of nature-identical phytomolecules inhibits Salmonella
On Mueller Hinton agar plates where Salmonella enterica were spread uniformly, small disks containing 0 (control, only methanol), 1, 5, and 10 µl of Ventar D were placed and incubated at 37 °C for 16 hours. The presence of clearing zones indicates antimicrobial activity.
Additionally, a motility test was performed in tubes with a motility test medium containing 0 (control) and 750 µL Ventar D. For this purpose, one colony of Salmonella enterica grown on the agar was stuck in the middle of the medium and incubated at 37 °C for 12-16 hours. Growth can be visualized through the formation of red color.
Result: Ventar D inhibited S. enterica in a dose-dependent manner. Clearing zones were visible within the lowest tested concentration. At its inhibitory concentration, Ventar D suppressed S. enterica motility (figures 5 and 6).
Let’s fight Salmonella through effective and sustainable natural tools
The zoonosis Salmonella generates high costs in the poultry industry. As Salmonellosis can be transferred to humans, it must be kept under control by all means. Antibiotics are one tool to fight Salmonella, but they have their “side effects”: they are no longer well respected by the consumer, and, even more critically, they create resistance. To help keep antibiotics effective, poultry producers seek to use effective but not resistance-creating natural solutions against Salmonella.
As shown with the reviewed trials, organic acids and phytomolecules are highly active against diverse Salmonella serovars. Accordingly, feed additives based on these active ingredients offer effective tools for controlling Salmonella in poultry while also contributing to the overarching aim of reducing antibiotic use in poultry production.
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Water Hygiene: The missing ingredient for successful ABF poultry
by T.J. Gaydos
Water quality is a frequently overlooked part of animal production and it becomes even more important when producing animals in an antibiotic-free (ABF) system. Chickens drink almost twice as much water as they consume feed, and water hygiene is often a second-level priority. Microbes present in water can be primary or secondary pathogens or non-pathogenic. Consuming impure water can add a challenge to the immune system, negatively impacting performance.
Water hygiene is essential for achieving antibiotic-free poultry production
Significant resources are spent on the correct nutrients in the diet and the correct additives for bird health. Water quality should be a priority, and a water quality monitoring program is essential for success in an ABF program. All things being equal, animals will perform better if they have access to high-quality water.
The variability of water quality in the grow-out region should determine how many water quality samples are taken. In highly variable areas, water quality should be measured at every season change on enough farms in every region to know if the solutes are changing. If the water quality is good and consistent, monitoring may be reduced significantly. Water quality should be a part of a “problem farm” work up or related to otherwise unexplained poor performance.
Water-soluble additives: Prevent biofilm
The use of water-soluble products is common in ABF production systems and their frequent use may provide a carbon source for bacteria. This, along with warm temperatures and slow water flow in enclosed water systems, makes the perfect environment for biofilm development.
It is important to frequently flush lines, give birds access to fresh water between additives, and sanitize water lines after using a product that can provide nutrients to bacteria in the line. The biofilm is a perfect location to harbor and protect pathogens from acids and mild or under-dosed disinfectants.
Designing a water quality program
The first step to building a water quality program is to understand the challenge on every farm. Correct sample collection is critical to achieving good results. Take a water sample from as close to the well as possible and submit for water quality analysis: pH, hardness, and minerals. This sample should also be submitted for bacterial load: total aerobic plate count (CFU) per mL and total coliforms per mL.
Monitor bacterial load
A drip sample should be collected from the end of the line for bacterial load analysis as well. This will help determine if the bacterial challenge begins at the source or is limited to the house. Additionally, a swab from the inside of the end of the water line should be taken to determine the level of biofilm. The total bacterial count should be less than 1,000 CFU/mL without fecal coliforms in a free-flowing sample, and total bacteria should be less than 10,000 CFU/mL on a biofilm swab.
Monitor water pH
Water should have a pH between 5 and 8. Water with a pH consistently lower than 5 can be damaging to equipment, while a pH over 8 reduces the efficacy of many disinfectants and can have a bitter taste to birds. Hard water can increase scaling of lines and equipment, leading to leaking seals. Scale also provides a matrix for biofilm formation, making cleaning and disinfection more difficult.
Clean and disinfect water lines
Cleaning water lines between flocks is the minimum program for ABF production. Stabilized hydrogen peroxide products are excellent for disinfecting water lines between flocks. The levels needed for proper disinfection of lines are generally too strong for birds, and the lines must be flushed prior to bird placement.
Water lines are often only cleaned in the house; it is important to periodically clean the lines that transport water from the well or water source to the poultry house as this may be a significant reservoir for bacteria. If the well is identified as a source of contamination, it is essential to seek the help of a qualified technician before adding any sanitizing product to a wellhead.
Ideally, water should be continuously disinfected with a product that is approved for poultry consumption. One of the best products for continuous disinfection is chlorine dioxide, which is effective at reducing bacteria and also reducing the concentrations of some mineral components. High levels of iron in the water can create a favorable environment for E. coli and other bacteria such as C. perfringens.
In addition to disinfection, chlorine dioxide is an effective treatment to reduce soluble iron levels. High sodium and chloride levels can lead to flushing and promote the growth of some bacteria. If high levels of sodium and chloride are consistent across a grow-out region, it may be possible to decrease the levels in the feed to reduce flushing. If the levels of sodium and chloride are considerably high, reverse osmosis should be considered to improve water quality.
Bottom line: invest in high-quality water
Another effective product is stabilized hydrogen peroxide at an appropriate residual level for bird consumption. There are other options for water line sanitation that can be explored on a case-by-case basis.
There are excellent online resources [link] for poultry water quality. The important message remains, in any case, that investment in high-quality water is a critical step for success in ABF poultry production.
Austin, B.J., J. Payne, S.E. Watkins, M. Daniels, and B.E. Haggard. 2016. How to Collect Your Water Sample and Interpret the Results for the Poultry Analytical Package. Arkansas Water Resources Center, Fayetteville, AR, FS-2017-01: 8 pp.
Scantling, M. and Watkins, S. 2013. Identify Poultry Water System Contamination Challenges. FSA8011. University of Arkansas Division of Agriculture Research and Extension.
Watkins, S. 2008. Water: Identifying and correcting challenges. Avian Advice 10(3):10-15. University of Arkansas Cooperative Extension Service, Fayetteville, AR
Want to reduce antibiotic use? Biosecurity and sanitation are crucial
by T.J. Gaydos
Biosecurity may not sound like an exciting topic at first, but it is a critical component of responsible poultry production. It is not enough to devise a strong biosecurity program; that program must also be followed by all people that interact within the system. It only takes one dirty boot or tire to ruin months of hard work.
Achieving good results with a flock largely depends on protecting the birds from biosecurity risks
Antibiotic reduction in poultry requires biosecurity
In a poultry operation, feed, people, and equipment constantly need to go in and out of farms and mills. Thus, no biosecurity program can be perfect. The intensity of the program needs to balance the realities of farming and the current disease pressure. The best program takes all of those into account, additionally considers local weather, availability of supplies, and company/farm staff. It is simple enough to be done even when no one is watching and should be easily scalable in case of increased disease pressure.
The rigorousness of a program must be in due proportion to the local circumstances. Having a biosecurity program that is too strict for the perceived disease pressure may result in people taking the path of least resistance. They probably will not follow instructions, especially if there is not enough monitoring and training to reinforce the value of biosecurity. On the other hand, a program with too lax guidelines will not have the desired effect.
The discrepancy between care requirements and separation
Unfortunately, the most valuable animals in an operation are often the most frequently visited by the most people. Pullets need closely monitored feedings, vaccines, and deworming. Breeders need eggs collected and shipped. Hatcheries require a labor force and maintenance. The feed mill and hatchery are central and overlapping points for all areas of the operation. The human and vehicle traffic at these locations must be closely monitored to reduce the risk of rapid disease transmission.
Feed mills are critical sites for biosecurity measures in poultry production
A physical barrier or sign indicating a biosecurity area on a farm or building entrance can help remind people of the program. Of course, these signs will not stop a disease from entering, nor a person determined to enter a site, but they will cause well-trained people to pause and reflect if they are making a sound decision.
Hygiene is a critical factor
It is well documented that hands and feet are significant transmitters of human and animal pathogens. Several studies have shown that hand washing can reduce absenteeism in school-aged children by 29-57%, thanks to a decrease in gastrointestinal diseases (Wang et al., 2017). Hand washing also reduces the incidence of respiratory illness in human populations by up to 21% (Aiello et al., 2008). Mycoplasmas can survive for one day in a person’s nose, for up to three days in hair, and up to 3-5 days on cotton or feathers (Christensen et al., 1994). Influenza viruses endure 1-2 days on hard surfaces (Bean et al., 1982) and more than a month in pond water (Domanska-Blicharz et al., 2010).
When building a biosecurity program, it is essential to consider the relevant pathogens of concern and the practical ways to reduce their risk of transmission.
How to establish an effective biosecurity program
Generally, biosecurity comprises two important parts:
Physical biosecurity, being the combination of all the physical barriers such as boot washes, signs, and disinfection
Operational biosecurity, covering the processes that protect an operation. This includes downtime, visiting birds in age order, time out for birds from people visiting sick flocks, and respect for physical biosecurity measures. Operational biosecurity starts with training, not only regarding the tasks required to be secure, but also the importance of disease prevention.
Establish several zones
When designing a program, consider four zones of increasing cleanliness: off-farm, on-farm, transition zone, and the animal housing area (Figure 1). Each zone should have a control point to reduce the pathogen load coming in, with exact measures depending on current disease status and bird value. These measures include vehicle sanitation and movement restrictions, footwear cleaning and disinfection, and use of personal protective equipment (PPE).
Figure 1: the four “cleanliness zones” in a farm
Increasing cleanliness from off-farm (red) to on-farm (orange) separated by a physical barrier. The entrance to the facility (transition zone; yellow) and the animal housing area (green).
Cleaning and disinfection are two of the core measures
As hands and feet are the main transmitters of pathogens, washing and sanitizing them is a priority. The outside of the house must be left outside, meaning that hands should be washed frequently and shoes sanitized between sites. Shoe covers should be put on when entering the house.
Cleanliness of the cell phone is often overlooked as a source of disease transmission (Olsen et al., 2020). It is a powerful tool: camera, notebook, light… and notoriously hard to clean. Cleaning and disinfection also apply to all shared tools and equipment that enter farms.
Prevent undesired “cohabitants”
Another critical point in biosecurity is the control of undesired pests and farm animals. Baits must be rotated, available where rodents are frequent, appropriately spaced, and secured from non-target animals. Habitats for pests need to be removed, the perimeter of the buildings must be clear of vegetation and debris, feed and grain spills picked up, and equipment stored away from the facilities. Pets and other farm animals should be kept away from the perimeter of the house and should under no circumstance be allowed to enter the facilities.
Tailored biosecurity programs keep your flock healthy
It is impossible to design a blanket biosecurity program for every operation. Understanding microbiology and disease transmission along with the risk points in a production system will allow a comprehensive plan to be developed. It is important to consider biosecurity as an investment in health and not an optional expense. No program is perfect, but small changes can significantly reduce the risk of pathogens entering the system and leading to major economic and animal welfare issues.
Aiello, Allison E., Rebecca M. Coulborn, Vanessa Perez, and Elaine L. Larson. “Effect of Hand Hygiene on Infectious Disease Risk in the Community Setting: A Meta-Analysis.” American Journal of Public Health 98, no. 8 (2008): 1372–81. https://doi.org/10.2105/ajph.2007.124610
Bean, B., B. M. Moore, B. Sterner, L. R. Peterson, D. N. Gerding, and H. H. Balfour. “Survival of Influenza Viruses on Environmental Surfaces.” Journal of Infectious Diseases 146, no. 1 (1982): 47–51. https://doi.org/10.1093/infdis/146.1.47.
Christensen, N. H., Christine A. Yavari, A. J. McBain, and Janet M. Bradbury. “Investigations into the Survival of MYCOPLASMA GALLISEPTICUM, Mycoplasma Synoviae And Mycoplasma Iowae on Materials Found in the Poultry House Environment.” Avian Pathology 23, no. 1 (1994): 127–43. https://doi.org/10.1080/03079459408418980.
Domanska-Blicharz, Katarzyna, Zenon Minta, Krzysztof Smietanka, Sylvie Marché, and Thierry van den Berg. “H5n1 High Pathogenicity Avian Influenza Virus Survival in Different Types of Water.” Avian Diseases 54, no. s1 (2010): 734–37. https://doi.org/10.1637/8786-040109-resnote.1.
Olsen, Matthew, Mariana Campos, Anna Lohning, Peter Jones, John Legget, Alexandra Bannach-Brown, Simon McKirdy, Rashed Alghafri, and Lotti Tajouri. “Mobile Phones Represent a Pathway for Microbial Transmission: A Scoping Review.” Travel Medicine and Infectious Disease 35 (2020): 101704. https://doi.org/10.1016/j.tmaid.2020.101704.
Wang, Zhangqi, Maria Lapinski, Elizabeth Quilliam, Lee-Ann Jaykus, and Angela Fraser. “The Effect of Hand-Hygiene Interventions on Infectious Disease-Associated Absenteeism in Elementary Schools: A Systematic Literature Review.” American Journal of Infection Control, 2017. https://doi.org/10.1016/j.ajic.2017.01.018.
Stop feed spoilage: How organic acids can preserve feed quality
by Daniela Vega Sampedro, Product Manager Organic Acids, EW Nutrition
Feed spoilage is a significant issue for the feed industry, leading to loss of nutrients, feed waste, and substantial economic issues for feed and animal producers worldwide (Leyva Salas et al., 2017). Fungal growth is one of the main causes of feed spoilage; it can occur at any stage of the feed production chain, including grain pre- and post-harvest processes, during feed production or storage. Organic acids and their salts are globally used in animal nutrition for microbial preservation and supporting animal health.
Organic acids help preserve animal feed and prevent spoilage through molds, yeasts, and mycotoxins
The threat of molds and yeasts in animal feed
Yeasts and molds can have both positive and negative effects on products consumed by animals and humans. On the one hand, yeasts are used to produce fermented products, such as bread, wine, and beer. On the other hand, yeasts and molds promote the spoilage of raw materials, food, and feeds (Lowes et al., 2000). Molds are among the most potent food and feed spoilers. They can be very resilient to environmental stress, which is a concern in climate change scenarios (Perrone et al., 2020) and enables them to withstand feed preservation measures (Punt et al., 2020).
Several hundred species of molds and yeasts can invade a large variety of raw materials and feeds. They show an easy adaptation to different environments; for instance, they can grow and reproduce in media with pH levels ranging from 2 to above 9 (Tournas et al., 2001). However, the majority of yeasts and molds require free oxygen to grow and thrive.
Excess moisture, high water activity, and high temperatures in feedstuffs are the main mold growth factors that concern the feed industry (Mohapatra et al., 2017). At storage, grains’ moisture content should not exceed 13%, and the water activity of raw materials, feedstuffs, and finished feed should be maintained below 0.8 (Dijksterhuis et al., 2019). Controlling these points contributes to preventing the growth of most pathogens and undesirable microorganisms.
Mold growth reduces the nutritional value of feed, which affects animal health and performance
The microbiology of molds and how they affect the feed
The microbial growth dynamic of grain storage depends on several factors, including the harvest season, grain temperature and moisture content, as well as the type of facility and its environment. For instance, in some areas, grains are harvested at the beginning of the cold season and stored through the following warm season. Storage molds constitute a significant threat to the quality of these raw materials, especially during the warm months, when the stored grains may become hotter than the surrounding environment. This leads to condensation, which increases moisture and water activity. Molds easily thrive in these conditions.
Storage molds reduce the nutritional and commercial value of grains and feeds. For grains, their commercial value decreases when the appearance of kernels changes in a manner recognized by the grain industry as kernel damage. The chemical composition of feeds may deteriorate due to enzymatic actions, resulting in a loss of nutrients (energy, vitamins) and the production of free fatty acids and other unwanted by-products (Reed et al., 2007).
Extensive research has established the factors that influence mold-induced deterioration during grain storage and which management strategies are required:
Moisture content and water activity (a function of the temperature, moisture content, and substrate) – Microorganisms have a limiting water activity below which they cannot grow; therefore, drying the grains below that critical level is part of an effective mold control strategy (Mannaa & Kim, 2017).
Temperature – Grain-contaminating molds thrive in tropical regions, where high temperature and humidity conditions predominate. In general, molds are inactive if the grains are stored below 20 °C (Mousa et al., 2013). However, the temperature of stored grains increases as molds begin to grow in the warmer and/or wetter parts of the grain/feed mass and feed, and heat is generated due to respiration, accelerating the deterioration rate. Moreover, the presence of a temperature gradient in the feedstuffs causes air to move, accelerating the transfer of moisture to cooler grain (Mannaa & Kim, 2017).
Grain quality, including previous storage conditions, insect infestation, presence of broken kernels, and impurities – When grain is too warm, the rate of insects’ breeding is higher (they respond to higher temperatures), the grain contains more humidity and may carry fungal spores. Broken kernels are an easier target for mold and insect infestations than whole ones, increasing the possibility of spoilage (Marcos Valle et al., 2021).
Duration of storage, management, and aeration influence the oxygen and carbon dioxide concentration in the grain mass, which plays a role in mold growth (Marcos Valle et al., 2021).
The consequences of storage deterioration include:
worse organoleptic properties (aspect, texture, taste, and aroma) of grains and feeds
more kernel damage,
higher fat acidity,
slight increase in protein content as non-protein constituents are consumed by mold respiration, causing
Molds and mycotoxins: a toxic relationship for animal health
Beyond their negative impact on feed quality, some fungal genera such as Aspergillus, Penicillium, Alternaria, and Fusarium can produce mycotoxins, secondary metabolites that have toxic effects on humans and animals (Greco et al., 2015). Roughly 60% of raw materials produced for agriculture purposes worldwide are estimated to be contaminated by fungi and mycotoxins (Eskola et al., 2020). Mycotoxins can induce toxic, carcinogenic, and mutagenic reactions even at low concentrations. Their presence in the final feed is a sign of alert as, usually, these metabolites are resistant to technological treatments. Thus, it is important to stop them from entering the feed production chain (Leyva Salas et al., 2017).
Feed-contaminating Fusarium species produce mycotoxins such as trichothecenes, zearalenone, and Fumonisin.
Organic acids: Unrivaled in preventing feed spoilage
It is crucial to reduce the feed losses and improve animal health by controlling fungal contamination at all stages of the feed production chain: from pre-harvest strategies on the field to post-harvest management during storage and even at feed processing. Throughout these processes, producers can apply different management practices. For instance, in field crops, fungal growth can be prevented through crop rotation and tillage; the use of fungicides is a later measure when mold presence exceeds critical levels.
Post-harvest management of grains and their by-products includes drying and storage management through moisture and temperature monitoring and aeration programs. Other spoilage-prevention measures include good hygiene practices and thermal treatments in feed production. However, feed producers and farmers face limitations in applying and linking such measures to tackle the occurrence of these undesirable pathogens (Dijksterhuis et al., 2019).
Pro-Stabil BSL is a product that harnesses the feed preservation effects of organic acids and combines them with surfactants. This means that it can offer a strong yeast and mold inhibition while maintaining the moisture in feed, thus reducing the risk of microbial challenges while prolonging the shelf life of feedstuffs and compound feeds.
Trial results: Pro-Stabil BSL is a great tool to reduce mold growth and manage moisture
Pro-Stabil BSL contains a synergistic blend of organic acids and a surfactant that leads to
» Improved moisture dispersion in the feed
» Increased water retention (reduced water activity)
» Improved anti-mold agent dispersion in the feed and grain
Trial results show a significant decrease in mold growth when Prostabil BSL was added to compound feed. In addition, when moisture was added at 2%, moisture from the environment was also observed, but the mold counts still decreased (Figure 1).
Figure 1: Effects of Pro-Stabil BSL with addition of 2 % moisture on feed quality indicators
When adding Pro-Stabil BSL to animal feed, the following benefits can be expected:
Reduction and prevention of mold growth and recontamination
Improved moisture management
Improved feed mill efficiency production
Improved microbiological quality of grains and feed
Shrinkage management by increasing moisture in feed with no risk of mold development
Reduced water dissipation
Mold growth can lead to sensory defects in feed and reduce its nutritional value. It can also harm animals through the production of mycotoxins. Pro-Stabil BSL offers a safe solution that is also easy to handle. Using the preservative properties of organic acids, Pro-Stabil BSL helps to reduce feed spoilage and its associated effects on animal health and performance.
Dijksterhuis, Jan, Martin Meijer, Tineke van Doorn, Jos Houbraken, and Paul Bruinenberg. “The Preservative Propionic Acid Differentially Affects Survival of Conidia and Germ Tubes of Feed Spoilage Fungi.” International Journal of Food Microbiology 306 (2019): 108258. https://doi.org/10.1016/j.ijfoodmicro.2019.108258.
Eskola, Mari, Gregor Kos, Christopher T. Elliott, Jana Hajšlová, Sultan Mayar, and Rudolf Krska. “Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%.” Critical Reviews in Food Science and Nutrition 60, no. 16 (2020): 2773-2789. https://doi.org/10.1080/10408398.2019.1658570
Greco, Mariana, Minna Kemppainen, Graciela Pose, and Alejandro Pardo. “Taxonomic Characterization and Secondary Metabolite Profiling Of Aspergillus Section Aspergillus Contaminating Feeds And Feedstauffs.” Toxins 7, no. 9 (2015): 3512–37. https://doi.org/10.3390/toxins7093512.
Harein, P., & Meronuck, R. (1995). Stored grain losses due to insects and molds and the importance of proper grain management. In V. Krischik, G. W. Cuperus, & D. Galliart (Eds.), Stored product management (pp. 29e31). Oklahoma Cooperative Extension Service Publication. E-912.
Leyva Salas, Marcia, Jérôme Mounier, Florence Valence, Monika Coton, Anne Thierry, and Emmanuel Coton. “Antifungal Microbial Agents for Food Biopreservation—a Review.” Microorganisms 5, no. 3 (2017): 37. https://doi.org/10.3390/microorganisms5030037.
Lowes, K. F., C. A. Shearman, J. Payne, D. MacKenzie, D. B. Archer, R. J. Merry, and M. J. Gasson. “Prevention of Yeast Spoilage in Feed and Food by the Yeast Mycocin Hmk.” Applied and Environmental Microbiology 66, no. 3 (2000): 1066–76. https://doi.org/10.1128/aem.66.3.1066-1076.2000.
Mannaa, Mohammed, and Ki Deok Kim. “Influence of temperature and Water activity on Deleterious fungi AND Mycotoxin production during grain storage.” Mycobiology 45, no. 4 (2017): 240–254. https://doi.org/10.5941/myco.2017.45.4.240.
Marcos Valle, F. J., Castellari, C., Yommi, A., Pereyra, M. A., & R. Bartosik. “Evolution of grain microbiota during hermetic storage of corn (zea mays l.).” Journal of Stored Products Research 92 (2021): 101788. https://doi.org/10.1016/j.jspr.2021.101788.
Mohapatra, D., Kumar, S., Kotwaliwale, N., and K. K. Singh. “Critical factors responsible for fungi growth in stored food grains and non-Chemical approaches for their control.” Industrial Crops and Products 108 (2017): 162–182. https://doi.org/10.1016/j.indcrop.2017.06.039.
Mousa, W., Ghazali, F. M., Jinap, S., Ghazali, H. M., and S. Radu. “Modeling growth rate and assessing AFLATOXINS production by Aspergillus flavusas a function of Water activity and temperature on polished and brown rice.” Journal of Food Science 78, no. 1 (2013). https://doi.org/10.1111/j.1750-3841.2012.02986.x.
Perrone G, Ferrara M, Medina A, Pascale M, and N. Magan. “Toxigenic Fungi and Mycotoxins in a Climate Change Scenario: Ecology, Genomics, Distribution, Prediction and Prevention of the Risk.” Microorganisms 8, no. 10 (2020): 1496. https://doi.org/10.3390/microorganisms8101496.
Punt, Maarten, Tom van den Brule, Wieke R. Teertstra, Jan Dijksterhuis, Heidy M.W. den Besten, Robin A. Ohm, and Han A.B. Wösten. “Impact of Maturation and Growth Temperature on Cell-size Distribution, Heat-Resistance, Compatible Solute Composition and Transcription Profiles of Penicillium Roqueforti Conidia.” Food Research International 136 (2020): 109287. https://doi.org/10.1016/j.foodres.2020.109287.
Reed, Carl, Stella Doyungan, Brian Ioerger, and Anna Getchell. “Response of Storage Molds to Different Initial Moisture Contents of Maize (Corn) Stored AT 25°C, and Effect on Respiration Rate and Nutrient Composition.” Journal of Stored Products Research 43, no. 4 (2007): 443–58. https://doi.org/10.1016/j.jspr.2006.12.006.
Feed hygiene in animal nutrition is vital – and organic acids help achieve it
by Vinil Samraj Padmini, Global Category Manager, EW Nutrition
Feed safety is essential for animal health and performance – and food safety. Inadequate feed sanitization is still a problem across the globe. It impacts not only the feed industry and animal producers but also puts workers and consumers at risk of being exposed to harmful substances.
Developing a hygiene program for the whole feed chain needs to include proper monitoring of microbial growth, as well as feed processing methods that prevent feed contamination and enable decontamination. This article outlines the importance of feed hygiene and focuses on how organic acids help reduce contamination from “farm to fork”.
Corn is often contaminated with Aspergillus fungi that can produce poisonous mycotoxins
How to achieve feed hygiene
Feed hygiene requires the control of microorganisms throughout the feed production chain. However, producers or retailers can rarely certify or verify feedstuffs’ safety due to the wide range of potential microbial contamination agents and hazards encountered in different feed environments (den Hartog, 2003). The relationship between feed and microorganisms varies, depending on the conditions: feed can transport pathogenic microorganisms and thus directly transmit disease; likewise, microorganisms can also be responsible for feed spoilage and thereby indirectly cause issues (Baer, Miller, and Dilger, 2013).
Since its foundation, the World Organization for Animal Health (OIE) has established standards, guidelines, and recommendations for toxin risk management, including for microorganisms that are transmissible via feed. Recurring outbreaks of Salmonella, Escherichia coli, and other familiar Enterobacteriaceae are a key concern for animal health professionals and the feed industry (Elsayed et al., 2021). However, as factors ranging from climate change to genetic mutations come into play, feed producers are working with moving targets; some of the most significant issues they might face tomorrow are unknown today. There are no easy solutions to these multifactorial problems – but in any case, corrective measures need to include quality control and quality assurance for assessing and managing the pathogenic and microbial risk situation.
To improve animal productivity sustainably, producers regularly experiment with modifying production techniques, innovating feed formulations, but also exploring new ingredients. The inclusion of new ingredients such as animal proteins, oils, and fermented products, among others, heightens the need for strict feed quality monitoring (Truelock et al., 2020). New ingredients come with causative agents of feedborne illnesses, some of which might be unknown (Goodarzi Boroojeni et al., 2016). Therefore, feed and animal producers need to consider how feed changes impact feed safety and include these hazards in their planning and risk assessments.
Better feed hygiene is crucial
For any animal production, feed processing constitutes the most crucial part of feed hygiene management, as it covers all treatments of the feed before ingestion. It is referred to as “hydrothermal processing” due to the use of heat that is required to kill most of the pathogens in raw materials, feedstuffs, and compound feed (Jones, 2011). However, whether or not hydrothermal processing will effectively eliminate a given pathogen depends on its heat resistance. Moreover, factors such as the type of feed components involved and water activity levels also need to be considered to reduce microbial pressure (Doyle and Mazzotta, 2000).
The new generation of feed milling equipment – besides elevating feed costs – can also improve feed quality (Truelock et al., 2020). These technologies tend to enhance feed stability and hygiene by modifying the physicochemical properties of the ingredients. This improves the absorption of nutrients, thereby enabling a higher feed intake efficiency with positive results for animal performance (Abdollahi, Svihus, and Ravindran, 2013). However, while increasing processing time at a given temperature can lead to a better decontamination process, it can also negatively affect some nutrients’ dynamics. This includes enzymes, proteins, minerals, vitamins, fiber and starch, and especially non-starch polysaccharides (Goodarzi Boroojeni et al., 2014).
Organic acids as a solution of feed hygiene risk management
Hence, while significant progress in feed science and feed production technology has already been made, researchers and the industry are still searching for alternative approaches to supporting feed hygiene (Goodarzi Boroojeni et al., 2016). Organic acids are a central research field as they offer promising antimicrobial properties. In combination with feed mill techniques, they already play an essential role in feed preservation (Brul et al., 2002). Despite their efficacy in inhibiting microbial growth, weak organic acids are safe to handle (especially when they are buffered) compared to inorganic acids.
In addition to their preservative effect in feed, it has been shown that organic acids can support gut health. They are not just antimicrobial agents but also acidifiers that display their impact in the stomachs of monogastric animals (Tugnoli et al., 2020).
A combined solution for microbial contamination challenges
To support the feed industry and animal production in light of feed safety challenges in AGP-free production, EW Nutrition focuses research efforts on maximizing the beneficial effect of organic acids. The ACIDOMIX® range of products supports the stabilization of the gastrointestinal microflora, inhibiting pathogenic bacterial growth in feed and water. Acidomix is an efficient acidifier specially formulated to have strong antimicrobial effects applicable in feed hygiene programs. Various powder and liquid solutions offer a wide range of benefits:
Strong antimicrobial effect, supporting the prevention of bacterial infections
Reducing the incidence of dysbiosis
Acidifying the feed and digestive tract
Supporting the improvement of production performance
Preventing feed re-contamination
Feedstuffs and compound feed are at risk of contamination and re-contamination throughout the feed production chain: processing, transportation, delivery, storage, and on-farm. Thus, a holistic and integrated approach that includes optimized feed mill processing and customized organic acids is required to improve the feed’s hygiene status. The positive effects are clear: feed producers benefit economically, animal producers reap the effects of improved animal health and performance, and people get to enjoy producing and consuming safe and nutritious food.
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Goodarzi Boroojeni, Farshad, Birger Svihus, Heinrich Graf von Reichenbach, and Jürgen Zentek. 2016. “The Effects of Hydrothermal Processing on Feed Hygiene, Nutrient Availability, Intestinal Microbiota and Morphology in Poultry—A Review.” Animal Feed Science and Technology 220: 187–215. https://doi.org/10.1016/j.anifeedsci.2016.07.010.
Truelock, Courtney N, Mike D Tokach, Charles R Stark, and Chad B Paulk. 2020. “Pelleting and Starch Characteristics of Diets Containing Different Corn Varieties.” Translational Animal Science 4 (4): txaa189. https://doi.org/10.1093/tas/txaa189.
Tugnoli, Benedetta, Giulia Giovagnoni, Andrea Piva, and Ester Grilli. 2020. “From Acidifiers to Intestinal Health Enhancers: How Organic Acids Can Improve Growth Efficiency of Pigs.” Animals 10 (1): 134. https://doi.org/10.3390/ani10010134.
Goodarzi Boroojeni, F., W. Vahjen, A. Mader, F. Knorr, I. Ruhnke, I. Röhe, A. Hafeez, C. Villodre, K. Männer, and J. Zentek. “The Effects of Different Thermal Treatments and Organic Acid Levels in Feed on Microbial Composition and Activity in Gastrointestinal Tract of Broilers.” Poultry Science 93, no. 6 (June 1, 2014): 1440–52. https://doi.org/10.3382/ps.2013-03763.