Next Article in Journal
Remote Sensing Dynamics for Analyzing Nitrogen Impact on Rice Yield in Limited Environments
Previous Article in Journal
Local Development and LEADER Funding in Poland: Insights from the Wielkopolska Region
Previous Article in Special Issue
Supplemental Xylooligosaccharide Attenuates Growth Retardation and Intestinal Damage in Broiler Chickens Challenged by Avian Pathogenic Escherichia coli
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 14
Issue 10
10.3390/agriculture14101752
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Fermented Feed in Broiler Diets Reduces the Antinutritional Factors, Improves Productive Performances and Modulates Gut Microbiome—A Review

by
Nicoleta Corina Predescu
1,*,
Georgeta Stefan
2,
Mihaela Petronela Rosu
1 and
Camelia Papuc
3
1
Preclinical Sciences Department, Faculty of Veterinary Medicine of Bucharest, University of Agronomic Sciences and Veterinary Medicine of Bucharest, 105 Splaiul Independentei, District 5, 050097 Bucharest, Romania
2
Clinical Sciences 1 Department, Faculty of Veterinary Medicine of Bucharest, University of Agronomic Sciences and Veterinary Medicine of Bucharest, 105 Splaiul Independentei, District 5, 050097 Bucharest, Romania
3
Academy of Romanian Scientists (AOSR), 54 Splaiul Independentei, District 5, 050094 Bucharest, Romania
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(10), 1752; https://doi.org/10.3390/agriculture14101752
Submission received: 19 August 2024 / Revised: 23 September 2024 / Accepted: 3 October 2024 / Published: 4 October 2024
(This article belongs to the Special Issue Rational Use of Feed to Promote Animal Healthy Feeding)
Browse Figures
Versions Notes

Abstract

:
The aim of this review is to highlight the most beneficial effects of dietary fermented feed in correlation with decreasing the antinutrient concentration in vegetal matrices usually used for broiler nutrition. Rational feed formulation is critical for animals because it improves animal performance, and provides the animal with the necessary nutrients to develop strong bones, muscles and tissues, and a properly functioning immune system. Fermentation of animal feed is useful as compounds with high molecular mass are converted into energy and compounds with lower molecular mass in the presence of enzymes produced mainly by bacteria and yeasts. Fermentation products contain probiotic compounds with beneficial effects on the health of the animal microbiome. Feed fermentation has other roles such as converting antinutrients into beneficial substances for animal organisms, and some studies have shown that fermentation of feed decreases the risk of antinutrient components presence. For the bibliographic research, different platforms were used (PubMed, Science Direct, MDPI resources), and numerous words or combinations of terms were used to find the latest information. Fermented feed utilization has been shown to enhance growth performance while promoting a healthier gut microbiome in animals.

1. Introduction

Sustainable and physiological growth [1], improving meat quality and feed conversion efficiency of farm broilers represent the main directions of this sector [2,3]. Increased oxidative stress has a tremendous impact on the health status and well-being of the birds [4]. In fact, stress management presented a big concern for researchers all over the world, for the last ten years. In order to reduce the unintended side effects, many solutions were proposed and tested [2]. In European Union until 2006, for both therapeutic and non-therapeutic applications antibiotics were used in animal production [5], posing a threat to product safety due to antimicrobial residues and increasing the risk of microbial resistance development and spread in the poultry environment [3].
To mitigate this risk, alternative strategies are being explored to reduce antibiotic use in chicken farms [5,6]. Research has focused on finding natural agents that can serve as growth promoters while maintaining low mortality rates, high animal yield, and protecting the environment and consumer health [7].
Research has simultaneously explored the use of plant-derived antioxidant compounds [8], bacteriophage therapy [9], micronutrient supplementation, and fermented feed [10] in animal feed as strategies to alleviate various negative impacts on animal health, human health, and environmental sustainability.
In general, animal agricultural sectors and especially, poultry farms have grown more interested in using plants and their derivatives as feed additives throughout the past ten years to preserve or enhance their health and productivity [11]. Secondary plant metabolites, polyphenols, are responsible for most host health benefits [12]. Polyphenols are well known for their antioxidant [13], immunomodulatory [14], anti-mutagenic [15], and anti-inflammatory effects [16]. Despite these benefits, polyphenols have been shown to have poor gastrointestinal absorption as well as reduced quantities in target cells, limiting their effectiveness as antioxidants. Some polyphenols’ poor bioavailability necessitates additional research to fully realize their potential in poultry livestock rearing [17]. For example, tannins are plant polyphenols, known for their properties like binding to proteins to form large-molecular compounds, and complex metal ions, decreasing their availability for animals [18].
So, researchers are looking for solutions to increase the accessibility and bioavailability of proteins, metal ions, tannins, and other molecules [19]. A brief search on the main platforms for scientific journals (MDPI, PubMed, and Science Direct) revealed an increased number of articles related to the use of fermented feed for broilers reared in the farm system, to improve the bioavailability of the healthy molecules.
Indeed, feeds are the most important instruments used to achieve the mentioned goals (rapid growth, enhanced meat quality, and increased feed conversion efficiency in farms raising broiler chickens).
The use of fermented feeds in broiler nutrition has gained attention due to its potential impact on growth performance [20]. Also, many studies proved that fermented feed has a salutary effect on the broiler gut microbiome [21]. In general, the fermentation process results in the breakdown of complex compounds in the presence of microorganisms, leading to the production of smaller and more beneficial metabolites [21], that have a positive impact on the health and antioxidant status of the broiler [20]. Also, fermentation reduces the antinutrient components (ANC) in the feed, conducting to increase of food-beneficial nutrient bioavailability [19,20,21].
Healthy fermented feed alternatives include probiotics, prebiotics, enzymes, organic acids, immunostimulants, bacteriocins, bacteriophages [9], or feed additives [8]. Probiotics used in fermentation become the main microorganisms delivered by feed; the probiotic’s metabolites lower the pH of the feed and help reduce harmful microorganisms [22]. Probiotics like Lactobacillus, Bacillus subtilis, and yeast can improve immunological, antioxidant, and production function as well as remodel gut microbiota and alleviate intestinal dysbiosis and inflammation [23]. Probiotics are added to a feed substrate and fermented under controlled conditions to make fermented feed. Probiotics take over in the feed during fermentation, generating metabolites that raise crude protein content, lower pH, limit mycotoxin synthesis, reduce dangerous microbes, and remove allergens and antinutritional factors. Some studies recommend fermented feed for better tastes thanks to the production of acids, alcohols, ketones, and esters during the process [24,25].
The aim of the present review is to emphasise and discuss the most beneficial effects of using fermented feed for broilers in the context of achieving the expected growth performance in connection with gut microbiome health. Notably, for the present review, the most beneficial effects of feed fermentation are presented in correlation with decreasing the concentration of ANC in vegetal matrices usually used for broiler nutrition.
Feed of vegetal origin, that undergone microbial fermentation, usually with the aid of lactic acid bacteria (LAB), is referred as fermented feed. Through this method, the feed’s nutritional profile changes, its digestibility is increased, and the broilers’ gastrointestinal health is improved [20]. Probably the most important fact is that fermented feed contains live probiotics, organic acid (like lactic acid), lowering the pH, which can inhibit harmful pathogens, naturally preserves the feed, and reducing the risk of spoilage [25].

2. Fermentation Used in Feed Processing

Fermented feeds have been gaining attraction in poultry farming as a potential way to improve both growth performance and gut health in broilers [24,26]. It is known that fermentation is a complex process, and lately, it gained more and more application from the food industry to the feed industry. The fermentation process is based on the breaking down of complex compounds in feedstuffs, making nutrients more digestible for animals. This can lead to improved growth performance and feed efficiency. Fermentation can preserve feedstuffs and extend their shelf life by reducing spoilage caused by moulds and bacteria [27]. Moreover, fermentation allows for the utilization of non-conventional feed sources, such as industrial waste products, which can help reduce reliance on traditional feed ingredients. The use of probiotics (live microorganisms) and prebiotics (fibres that promote beneficial gut bacteria) in conjunction with fermentation can further enhance the benefits for animal health [24].
There are various techniques for making fermented feeds from vegetal matrices, such as liquid fermentation, solid fermentation, and ensiling, which are the most used over the last couple of decades [20]. Fermented liquid feed provides not only water and digestible nutrients, but also organic acids and beneficial microorganisms such as lactic acid bacteria and yeasts. Solid-state fermentation, as opposed to liquid fermentation, has advantages such as reduced wastewater generation, increased product stability, reduced energy consumption and easier transportation [22]. In general, the fermentation substrate used for ensiling consists of fresh, water-rich plant material that supports a high number of active microorganisms [28]. For instance, mechanical chopping during harvesting may lead to an increase in lactic acid bacteria (LAB) counts, followed by Enterobacteriaceae and yeasts. Whatever type of fermentation is used, most of the research studies suggest a concentration of live microorganisms in the biomass between 105 and 109 CFU/g [28].
Spontaneous fermentation, although possible in all types of fermentation, should be avoided because of the risk of growth of harmful microorganisms and toxic metabolites. The development of harmful microorganisms is reduced under normal production conditions and can be effectively controlled by applying good quality control practices as well as by optimizing fermentation parameters [21,22]. These parameters include composition of raw materials used, starter culture formulation, fermentation conditions, and post-fermentation processes. For instance, the selection of enzymes and microorganisms depends on the characteristics of the substrate, and pretreatments (mechanical, thermal, chemical) can facilitate fermentation. The choice between enzymatic treatments and fermentation varies depending on the properties of the feed and enzymes used. Finally, nutritional assessments are essential to determine both feed improvement and nutritional value [24,25,26,28].
All the three fermentation processes described above, can help reduce ANC in feedstuffs, such as tannins and phytates, which can interfere with nutrient absorption [29]. In Figure 1 are presented the most basic ingredients of the fermentation process of milled vegetal material with the addition of water (chlorine-free water is preferred to avoid killing fermentation sensitive microorganisms) and substances to stimulate bacteria and yeast for multiplication and fermentation of matrices. Reduced ANC, increased feed shelf life, alternative feed source utilization and enhanced probiotic and probiotic delivery are probably some of the most important reasons to use fermented feed for broiler chickens’ nutrition.
Legumes and cereals are part of the base diet for all farm animals including broilers. Because they provide significant amounts of carbs, protein, vitamins, and dietary fibre, these grains are vital to the broiler chicken diet [24]. To promote growth and maintain health, these nutrient sources are necessary for daily nourishment. However, a lot of research regarding the plant composition in proteins, lipids, carbohydrates, vitamins, and minerals provide evidence and debate the issue regarding the presence of ANC, which reduce the bioavailability of good nutrients [30].
In Table 1 are presented a few of the most used vegetal matrices of basal diet of broiler corelated with ANC and ways to mitigate their effects.
Worldwide, soybean (Glycine max) is the primary source of protein and amino acids utilized in animal feed formulations, especially for monogastric animals. High inclusion rates of high-quality vegetable protein, particularly in diets for chicken, can be found in soybeans, which have a less changeable chemical makeup than other protein sources. In addition to their high protein content, soybeans also include a variety of variable amounts of substances that are generally regarded as antinutritional. Phytic acid, saponins, isoflavones, and trypsin inhibitors are a few examples [31]. Nowadays, it is believed that eating controlled concentration of these substances can have positive biological effects on blood cholesterol levels and cancer prevention [33]. Most of the scientific results addressed the variations in the concentrations of phytic acid, saponins, isoflavones, and trypsin inhibitors. Soybean processing alters the levels of these minor elements in a variety of ways. During the processing of soybeans by fermentation is created conventional protein components, flours, isolates, and concentrates, without ANC [32].
Corn or maize (Zea mays) provides an affordable and easy-to-access source of protein and energy, being utilized as an important ingredient in commercial chicken feed. The high carbohydrate content, and amino acid profile of corn protein give chickens the energy they need to thrive and regulate their body temperature. Also, corn contains higher levels of ANC, phytate and polyphenols, that form complexes with metal ions [34,35]. With the help of the enzymes produced during fermentation, ANC are reduced, making fermentation an effective technique for enhancing the macro, trace, and total minerals levels of corn genotypes. Tannase and phytase, two enzymes produced during fermentation by microorganisms, are thought to be responsible for reducing antinutrients (polyphenols and phytate) in corn genotypes [36]. This likely explains the increase in trace minerals after corn fermentation. One possible mechanism for releasing minerals from phytate could be dephosphorylation, whereby the removal of phosphate groups from the inositol ring reduces phytate’s ability to bind minerals, increasing the bioavailability of vital dietary minerals. Fermenting grains flour for 14 days resulted in significant increases in total and extractable zinc, manganese, copper, and cobalt levels [29].
Both ruminant and nonruminant farming systems can use sorghum (Sorghum bicolor L.) as a source of protein and energy. Sorghum can be a good source of grain in an animal’s diet if it is processed properly and combined with other feed ingredients in a balanced manner [38]. Further research is required to fully comprehend important antinutritive characteristics of sorghum, such as tannin (phenolic compounds), phytic acid, and dhurrin [37]. Apart from its application in the food animal industry, the problem lies in the high tannin content of sorghum, a water-soluble polyphenolic metabolite that inhibits poultry growth. Increased tannin concentrations slow down protein digestion and form chelate, which makes them ANC [39]. Tannins negatively affect the growth, feed intake, digestion of protein, egg production, and deformities of the legs of broiler chickens. Dhurrin, a cyanogenic glucoside, by a specific enzyme pathway generate hydrogen cyanide (HCN), toxic for organisms [40]. It decreases the broilers’ apparent nutritional digestibility, promotes cytochrome oxidase system inactivation causing anoxia of the central nervous system, which can lead to death in a matter of seconds. To inhibit the antinutritive effects, processing in the presence of microorganism like lactic acid bacteria (LAB) is used [37,41].
Research has shown that the inclusion of barley (Hordeum vulgare L.) with β-glucan in the diets of young chicks can hinder growth and lead to problems such as sticky droppings. However, these negative effects can be mitigated either by fermenting the barley or by adding β-glucanase producing microorganisms to barley-rich diets [42]. The adverse effects appear to be associated with nutrient digestion and bowel transit problems, but there is no conclusive evidence that treatments aimed at removing β-glucan can improve nutrient digestibility in barley-based diets. Although there is a substantial amount of literature on this topic, very few studies have made significant advances for a certain answer [42]. Some recent research has looked at the antinutritive effects of pentosans present in other cereals, but there have been no direct tests on β-glucan isolated from barley in poultry diets, nor examinations of its impact on nutrient uptake by poultry. Probably, further research on the biochemistry and molecular biology of fermentation microorganisms with glucan-degrading enzymes could provide a deeper insight into their role in poultry nutrition [43].
Antinutritional factors are harmful compounds in wheat (Triticum aestivum) that interfere with the absorption and bioavailability of nutrients in monogastric animals like pigs and poultry, so impact its nutritional quality. Wheat, a key source for energy and protein, contains several ANC like phytate, protease inhibitors, tannins, lectins, alkaloids, and oxalate. Phytate, for instance, reduces the bioavailability of essential micronutrients such as iron and zinc [44]. Various strategies, including fermentation as well as genetic engineering, aim to mitigate these effects. Enzyme degradation of tannins—proteins complex in seed provide an efficient solution (this network being responsible for trapping metal ions). Rather than germination, processing by fermentation increases the content of iron and zinc, with the highest iron content observed in fermented samples (5.52 mg/100 g) [45].
Oats (Avena sativa L.) stand out among cereals because of their high dietary fiber content and nutritional value, which includes proteins, balanced amino acids, minerals, unsaturated fatty acids, vitamins, antioxidants, and phenolic compounds [46]. Their high soluble and insoluble fiber level is especially sought because it has been associated with several health advantages. Also, important concentrations of ANC are present in oats, it can disrupt the stomach’s normal functioning and prevent nutrients from being absorbed [47]. Also, rough texture, tough hull removal, low digestibility, and antinutrient elements, limit the use of oats in animal diet. To lower ANC, several processing methods, including fermenting, grinding and boiling, can help address these problems by increasing the availability of minerals, protein, and carbohydrates [47].
The rye grain (Secale cereale) contains several nutritionally beneficial dietary components. Poultry should not receive more than 5–7% of their diet, according to zootechnical requirements. The primary cause of rye grain’s restricted use as animal feed is its high level of antinutrient ingredients, like water-soluble pentosans [48]. Water-soluble pentosans’ capacity to absorb water and create a very dense solution gives their negative feeding characteristics. Animals’ digestive tracts are clogged with a viscous pentosan solution that prevents food nutrients from being absorbed. High rye grain consumption causes indigestion, weakens farm animals, and slows down the forage’s passage through the digestive system [49]. Poultry may experience oesophageal and gastric blockages. The immune systems of the birds will be impacted by the addition of rye to their diet. To prepare rye grain for feeding animals, there are several methods. Winter rye grain is currently subjected to enzymatic treatments to counteract its antinutritional qualities and improve its nutritional digestibility. Studies indicate that applying enzyme preparations to the aqueous grain extract of winter rye can considerably lower its viscosity [50].
Because it has a high protein content and a high dry matter yield, alfalfa (Medicago sativa L.) is an essential livestock feed crop in both developed and developing countries. This plant’s primary ANC are saponins, and because of their detrimental effects on animal performance, its high protein content has not been able to be used to its full potential as animal feed [51]. Saponins are glycosides that have a polycyclic aglycone moiety connected to a carbohydrate. These moieties can be either of the C27 steroid or the C30 triterpenoid, which are together referred to as sapogenins [52]. The flavor of saponins is unpleasant, and they have foaming qualities. For non-ruminant animals (pigs and chicks), the most important negative effect is growth rate retardation, which is mainly caused by a decrease in feed intake [6]. To fully detoxify the seeds of this antinutrient, the dry (raw) bean requires a long cooking time. Alternatively, fermentation with LAB microorganism, dramatically eliminates the majority of these antinutrients with a significantly lower energy cost than cooking [53].
Fermentation increases feed digestibility because fermentation break down lipids, complex carbohydrates and proteins into their simple biochemical units (e.g., fatty acids, monosaccharides or amino acids), making them easier for broilers to digest and absorb nutrients [20]. According to another study, the enhanced digestibility of fermented feeds may be responsible for the beneficial effects observed in the gastrointestinal environment/condition (e.g., the reduction of gastric pH and pathogenic microbial activity as well as the increase in the production of short chain fatty acids [SCFA]), which in turn enhances the growth performance of chickens [54].
Fermentation of fresh vegetal nutrients reduces the size of the complex molecules, with anti-nutritional characteristics, to easily absorbable structures in the digestive tract. Some of these molecules (Figure 2A), like protein-tannin complex, metal—starch—phytate complex or inhibitor–enzyme complex. After fermentation process (Figure 2B) of vegetal feed, the complex molecules are degraded, reducing the concentration of ANC, increases the concentration of beneficial compounds (antimicrobial peptides, metal ions, antioxidants, vitamins, short chain fatty acids, and amino acids) released from the complex networks and acting as prebiotics in the broiler gastrointestinal tract (GIT). Additionally, fermentation brings beneficial microorganisms, probiotics, to the digestive tract of the broiler improving the health status of the birds (Figure 2C). Broilers ingest fermented feed with decreased concentration of antinutritional compounds and enhanced prebiotics and probiotics levels, elevate the meat nutritional value. The human consumer, as the final link in the chain, is the beneficiary of the positive consequences of feeding fermented feed to broilers (Figure 2D).
Tannins have been shown to bind proteins via hydrogen bonding and hydrophobic interactions, resulting in protein-tannin complexes [55]. They impact the digestibility of proteins and carbohydrates, adding to the diet’s lower calorie value. Tannins interact with digestive enzymes such as trypsin and amylase, leaving them unavailable for digestion reactions. Tannins can form a complex compound with vitamin B, making it inaccessible for body needs [31,56].
Phytic acid is present in many plants and is also called inositol hexa-phosphate or IP6. It forms salts of the mono or/and divalent cations K+, Ca2+, and Mg2+. In this way, phytates serve as reservoirs of cations, with high-energy phosphoryl groups [56]. Because they can act as chelators of free iron are considered efficient natural antioxidant. Phytates are powerful anions in a broad pH range, impacting the bioavailability of divalent and trivalent mineral ions such as Ca2+, Cu2+, Mn2+, Zn2+, Mg2+, Fe2+, or Fe3+ in diet [57]. The effect of increasing phytate intake on mineral deficiency is dependent on what else is consumed. It has been claimed that the interaction between phytate and polysaccharides like starch, lowers carbohydrate bioavailability and breakdown, and influences starch metabolism as the development of the phytate-carbohydrate complex [31].
Protease inhibitors are found in many plants, including legume and cereal seeds used for broiler nutrition. Protease inhibitors function as competitive inhibitors, binding to the enzyme’s active site and forming a complex with a low dissociation constant at neutral pH [57]. The inhibitor imitates the substrate, resulting in an inhibitor-enzyme complex that cannot be removed using the usual process [55]. This blocks the enzyme’s active site and effectively silences its activity. For instance, amylase inhibitors are thought to have two functions: they protect the seeds from microbial diseases and pests while also inhibiting endogenous amylase [31,56].
Nutrient digestibility is a measurement of feed nutritional processes related to capacity and intestinal function. Beneficial microorganisms in fermentation produce metabolites like lactic acid, bacteriocin, antibacterial substances, and alcohols, which can lower digestive tract pH, inhibit harmful bacteria like Escherichia coli, and improve intestine digestion and absorption [55]. Addition of fermented material, broilers’ apparent calcium metabolic rates increased. Adding 20% fermented feed enhanced the apparent metabolic rate of Calcium. This is because the lactic acid produced by fermentation lower the feed pH, creating a favourable acidic environment in digestive system for calcium absorption [58].
In the same time, research suggests that fermented feeds can be a promising strategy for enhancing growth performance and gut health in broilers. However, the specific effects can vary depending on factors like the type of fermentation, the ingredients used, and the inclusion level in the diet. Furthermore, improved growth in birds is attributed to elevated activity of digestive enzymes such lipases, amylases, trypsin, and proteases in broilers fed fermented diets [59].
Enhanced nutrient availability by previously subject to fermentation of row vegetal matrices or plant byproducts. Beneficial microbes in fermented feeds can produce enzymes and organic acids that further improve nutrient utilization. While there is evidence linking fermentation to enhanced palatability and nutrient digestibility, fermentation resulted in a decrease in the amount of feed consumed by broilers throughout the starter and grower phases [60]. The hens’ growth rates were slowed down as a result during these stages, but surprisingly not during the finishing phase.
The ability of animals to convert feed into muscle tissues is shown by their slaughter performance [61]. The two main indicators used to assess carcass yield and meat quality in broilers are muscle and visceral (abdominal) fat. The addition of FTLM to the broiler diets raised the weights of the thigh and breast muscles [62]. Also, Yang et al. (2008) noted a rise in the weights of the cut parts (thighs and breast) of broilers given fermented herbal items [63].

3. Effects of Fermented Feeds on Broilers Growth Performance and Gut Microbiome

3.1. Improved Growth Performance

Resources like cereals, different vegetal beans, and agricultural by-products are insufficient to improve growth performance in broiler? It was shown previously that ANC in the feed, reduce digestibility and have an impact on survival rates. To reduce ANC, fermentation is the most used method [24]. Fermentation feed can stimulate growth, take the place of antibiotics, recycle waste (use byproducts to cut waste), and alleviate feed scarcity [22].
To evaluate the growth performance of an animal, in this case, broiler, considered parameters are feed conversion ratio (FCR), body weights gaining (BW) and feed intake (FI) [24]. Those tree parameters are linked by a mathematical relationship. FCR represents the ratio between FI and BW. The research indicate that the microorganisms used for feed fermentation influence the balance [64].
It’s crucial to increase broiler feed conversion rate, and for broilers feed with fermented feed, FCR is between 1.35–1.70 g feed/g gain, depending on the concentration of fermented feed added to the basal ratio and the age of the broilers [24]. The most recommended solution by the researchers is represented by feed fermentation. Indeed, probiotic fermentation of different materials produces fermented feed, which increases the beneficial nutrients and decreases the ANC [65].
According to the study [21], corn, soy-bean, and wheat, 6:2:2 (w:w:w), fermented with Lactobacillus casei (L. casei) was used as fermented feed additive. Four groups of chickens were investigated as follows NC (negative control received basal diet), PC (positive control received basal diet +antibiotic 15 ppm), FFL (fermented feed low received basal diet + 0.3 kg/t FFA), and FFH (fermented feed additive high received 3 kg/t FFA). The results of the study [21] indicated that FFL and PC diets had a higher FCR than the NC from 0–42 days, and the FFH and FFL groups gained greater BW (1–21 days). Also, microorganisms with beneficial properties, such as Lactobacillus aviarus genus, Lactobacillus spp., and Lactobacillus phylum Delsulfobacterota and class Desulfovibriona, were also tended to increase in the FFH and FFL fermented feed groups compared to the PC and NC groups. Pathogenic microorganisms were also significantly reduced in the group treated with FFH and PC [21].
Irawan et al., [62] investigated the effect of fermented soybean meal (FSBM) in the presence of Lactic acid bacteria and yeast on chickens’ performance. Comparing broiler trials fed with and without FSBM revealed that replacing SBM with FSBM had a substantial favorable effect on the BW of broiler chickens [66]. Except for the feed fermentation in the presence of Aspergillus niger, the majority of microbial fermentation (Lactic acid bacteria and yeast) resulted in a considerable rise of broiler BW. In the same research, positive correlation was found between broiler average daily gain and the diet supplementation with FSBM fermented in the presence of Aspergillus oryzae, mixed probiotics + bromelain, Bacillus subtilis, and Lactobacillus microorganisms. Also, fermented feed seems to be responsible for increasing the FI [66].
The most important microorganisms used to obtain fermented feed are belong to Ruminococcaceae, Lactobacillaceae, and unclassified Clostridiales. The growth performance parameters obtained after feeding broilers with fermented feed in the presence of these bacteria are shown in Table 2.
In the last years, besides corn, soybean, cotton-seed, and rapeseed, other vegetal sources are used as feed for broiler. Leaf meals (LM) are leaves and twigs dried, pulverized, and used as a feed for livestock. They are an important management tool during the dry months when fresh fodder is in short supply [68]. For instance, tropical leaf meals (TLMs) can be used in poultry production due to their health and nutritional benefits. However, their large-scale use is limited due to their high crude fiber content and moderate anti-nutritional factors. Fermentation, particularly microbial fermentation, has been shown to reduce these factors, increase nutritional benefits, and improve growth performance in broiler production. Ogbuewu et al. [61] find out that the growth performance of broilers fed with fermented tropical leaf meals (FTLM) may be linked to decreased ANC levels and the breakdown of complex biomass by fermentation microorganisms. This may also improve intestinal health and function, as the intestine is the primary site for immunity, nutrient digestion, and uptake [61].
Fermented feeds have been found to promote growth in broilers by increasing intestinal length indices, maintaining normal gut microbial ecosystems, and improving intestinal morphology, such as villus height. These feeds also improve digestion and absorption, leading to improved production performance [20]. This can be sustained by the study of Saleh et al. [67], where Bacillus spp. appear to be a viable alternative for antibacterial growth promoters that improve animal health and performance. Bacillus licheniformis can sporulate, rendering them stable under thermal processing of feed and resistant to enzymatic digestion along the gastrointestinal tract (GIT). Bacillus licheniformis addition in broiler drinking water or diets boosted growth performance by increasing the body weight and feed conversion ratio of broilers [67].

3.2. Gut Microbiota Modulation

The microbiota is the entire microbial population (including viruses, bacteria, fungi, protists, and archaea) that lives in complex multicellular organisms such as plants, animals, and humans [9]. The microbiota in broiler chickens’ gastrointestinal tract (GIT) plays a crucial role in their health, immune system, and productivity. It reduces colonization by enteric pathogens and prevents inflammation, leaky gut, and other gut-related disorders [69]. Broiler microbiota composition is influenced by factors like age, diet, genetics, and antibiotic use. Broad-spectrum antibiotics cause collateral damage, leading to dysbiosis and antibiotic resistance. Poultry production systems use antibiotics for growth promotion, but indiscriminate use reduces microbiota stability and Lactobacillus population in broilers. Long-term antibiotic usage has disrupted the gut microbiome of the animals in general, and impaired immune function [56]. Furthermore, increasing treatment resistance among pathogenic strains has emerged as one of the world’s most severe issues. The observations described above has given rise to a growing interest in the management of infections caused by antibiotic resistant pathogens by selectively targeting the disease-causing bacteria, without disturbing the commensal microbiota of the GIT [70].
Due to their immature immunological and digestive systems, chickens have poor nutrition utilization and low condition resistance. 44 bacterial strains have been licensed by the Food and Drug Administration (FDA) and Association of American Feed Control Officials (AAFCO) for use in fermented feed, which has improved animal husbandry [71]. By secreting chemical signals known as auto-inducers, which alter bacterial behaviour, bacteria are able to interact with one another across cells. Bacteria also utilize the quorum sensing mechanism of bacterial communication to communicate with their host. Probiotics may impact pathogenic bacteria’s ability to sense quorum, which could change how harmful they are [72]. For instance, fermentation products from L. acidophilus La-5 significantly reduced the extracellular secretion of a chemical signal (autoinducer-2) by human enterohaemorrhagic E. coli serotype O157:H7. This led to the in vitro suppression of the expression of the virulence gene (LEE, locus of enterocyte effacement). This interferes with quorum sensing and stops E. Coli serotype O157:H7 from colonizing the GIT [73].
In order to mitigate the concentration of ANC, cereals and vegetables commonly used in broiler feed are most often subjected to fermentation and then fed to the animals [73]. Fermented mixed feed had lower pH, phytic acid, trypsin inhibitor, and β-glucan concentrations, compared to unfermented feed. Fermentation increased crude protein content, but unfermented mixed feed contained higher molecular mass proteins (60–120 kDa) [68].
Fermentation of feed introduces beneficial bacteria like Lactobacillus and Bifidobacterium to the gut. These microbes compete with harmful bacteria for space and resources, promoting a healthy gut balance. The analysis reveals positive correlations between intestinal morphology and certain bacteria related to gut health, while negative correlations exist with bad microorganism. Fermentation improves feed safety by preventing the growth of pathogenic bacteria [74].
The diverse habitats that make up the gastrointestinal lumen’s various segments’ distinct functions are reflected by them. Additionally, the gut lumen has a variety of habitats that could add to the microbiota’s spatial variability [68]. The most listed chemical gradients (like, pH, bile concentrations, etc.), nutritive molecules availability, and immunological interactions are some of the possible causes of this heterogeneity [75]. The upper section of the gut is thought to have a bacterial density of 10–103 bacteria per gram of stomach and duodenal contents, in the ileum and jejunum, it rises to 104–107 bacteria/gram of content [76].
The broiler intestinal health is very broad and relies on an understanding of nutrition, intestinal morphology, and gut microbiota [77]. All of these components interact with one another to ensure the appropriate functioning and dynamic balance of the GIT lumen (Figure 3). The intestinal histological structure has a crucial impact in the GIT’s ability to move nutrients from the lumen into the systemic circulation. As shown in Figure 3A, the gut mucosa functions as both a physical and immunological defensive barrier. The barrier is primarily composed of the mucus layer, biofilm, microorganism metabolites, and secretory immunoglobulin A (sIgA) molecules, which are linked to the specialized epithelial central single cell layer with the epithelium’s tight junction proteins (ETJP) and the inner lamina propria, which is made up of immune cells, loose connective tissue, blood vessels, and lymphatics [78,79]. Goblet cells secrete high molecular weight glycoproteins, known as intestinal mucous layer [80]. Enterocytes, goblet cells, and other specialized cells form a continuous and polarized monolayer. It separates the lumen of the intestine and lamina propria. In the absence of specialized transporters, cell membranes are impermeable to hydrophilic solutes, limiting their transit through ETJP. Diffusion and endocytosis are the primary mechanisms for lipophilic or large-molecule absorption [79]. Junctional complexes govern the transport of molecules between ETJP. Generally speaking, there are two ways that nutritional compounds can go from the intestinal lumen to the subepithelial space: transcellular and paracellular [81]. Large antigenic molecules, lipophilic substances, and nutrients will prefer the transcellular pathway. It assumed binding to certain transporters, endocytosis, or passive diffusion to move molecules across the ETJP. Ions, particularly cations, and tiny hydrophilic molecules (<600 Da) will leave the lumen by paracellular transport pathway. These substances will diffuse via the intercellular gaps between neighbouring IECs, with the TJs acting as the rate-limiting step for epithelial permeability [79,82]. Fermented feed contains small molecules with molecular weight less than 600 Daltons, like amino acids, monosaccharides, antioxidants like vitamin C or polyphenols, SCFA. These molecules are easily absorbed by villus enterocyte which is the absorptive surface of the intestines. Also, the study prove that increased dimensions of intestinal villi are connected with an increase in the absorbent surface of the intestines as well as the absorbing rate of the intestine [80]. Good microbiome is preserved by competition with the pathologic microorganism (Figure 3A).
So, intestinal morphology (like, villus height, crypt depth) changes in response to exogenous agents, such as the presence or lack of good nutrient feed or pathological circumstances. Based on the previous presented fact, fermented food is quickly absorbed from the lumen of the intestine, also stimulate the peristalsis of the intestine. Also, unfermented feed stays longer time in the intestine and the presence of ANC conduct to modification and pathology development like inflammation, villus atrophy, corrupted epithelium’s tight junction proteins (ETJP), and goblet cells perturbation and decreasing in mucous layer secretion represent an unwanted scenario having dramatic consequences on broiler health (Figure 3B). Mucous layer is protecting the enterocyte and, in its absence, the perturbance of microbiome appear and together with pathological microorganism metabolites can pass from the intestine lumen complicated even more the broiler health. The decreased number of healthy microbes allow the development of the rest of the unwanted bacteria and yeast. The important concentration of ANC (like, protein-tannin complex, metal—starch—phytate complex, inhibitor—enzyme complex) overlap existing problems (Figure 3B).
The gastrointestinal tract (GIT) microflora is primarily composed of bacteria, with minor populations of fungi and protozoa. Because different bacterial species have distinct growth requirements and substrate preferences, the chemical content of diet might affect the composition of microflora in GIT. Fermented feeds promote wellness by lowering feed viscosity [82]. Fermented barley, wheat, oats, and rye diets substantially raised caecal butyrate and propionate levels. Nutrient degradation and solubilization enhance accessible substrates for microbial fermentation in the intestine, including oligosaccharides and monosaccharides. Increasing of short-chain fatty acids (SCFA) from digestion due to fermented substrates promote the growing of the healthier microflora (for example, Lactic Acid Bacteria (LAB)) [83]. Other study showed that certain beneficial bacteria can synthesize essential vitamins and SCFAs, further contributing to broiler health and growth. The number of LAB adhering to the gut mucosa forming biofilm is more developed when the number of benefic bacteria increased and significantly dropped in the case of pathologic case. The lately situation conduct the formation of pathogenic microorganism biofilm [84]. Similarly, in the presence of prebiotic compounds, which pass undigested, the growth of beneficial bacteria is promoted [85].
Many research indicate that fermented feed may improve immune function [23]. A balanced gut microbiome can strengthen the immune system, making broilers less susceptible to diseases. The study conducted by [68] found that fermented feed, particularly 6% and 8%, significantly improved jejunum secretory immunoglobulin A concentration (sIgA is an important component of the immune shield) and jejunum morphology in laying hens, indicating its positive effects on gut mucosa barrier function and reducing adverse effects on gut health [24].
Figure 4 emphasizes the most important achievements of the present paper. Fermented feed decreased the concentration of ANC and enhanced the concentration of beneficial probiotics, enzymes and metabolites. Beside this, the fermentation process has acidic pH and molecules with lower molecular mass. Those factors stimulate gut microbiota by growing the number of good microorganism and regulation of the immune response. Healthy broiler chicken will improve growth performance (feed conversion ratio (FCR), body weights gaining (BW) and feed intake (FI)).

4. Conclusions

Proper control of fermentation parameters and the use of good quality practices are essential whatever fermentation techniques—liquid, solid-state, and ensiling—offering distinct benefits for enhancing vegetal-based feeds, including decreased concentration of antinutrient components. Tailoring the fermentation process to the specific substrate characteristics, selection of fermentation microorganism and conducting regular nutritional assessments ensure improved feed quality and safety.
Using fermented feeds in broiler nutrition has shown promising effects on growth performance and gut health. However, it’s essential to consider various factors, including feed composition, fermentation conditions, and the specific needs of the broiler production system. Fermented feeds often contain higher levels of beneficial microorganisms, most lactic acid bacteria. These bacteria can contribute to a healthier gut environment by stimulating and supporting a balanced immune response the host or exhibiting anti-inflammatory properties.
Studies suggest that fermented feeds can positively influence intestinal morphology, including increased villus height and crypt depth, which is indicative of better nutrient absorption. Fermented feeds may stimulate the production of mucin, a protective layer in the gut. This can contribute to a healthier gut lining and protection against pathogens.
Certain fermented feed components, such as prebiotics and short chain fatty acids, can influence the relative abundance of specific microbial populations, promoting a balanced microbiota. Fermented feeds may enhance the palatability of the diet, leading to increased feed intake and subsequently supporting growth performance.
Research in this field continues to explore optimal strategies for incorporating fermented feeds into broiler diets. The type and composition of the feed used in fermentation, as well as the specific fermentation microorganisms employed, can impact the outcomes.

Author Contributions

Conceptualization, N.C.P. writing—original draft preparation, N.C.P., M.P.R., G.S. and C.P.; writing—review and editing, N.C.P. and C.P.; validation, N.C.P., M.P.R., G.S. and C.P.; resources, NCP.; visualization, N.C.P., M.P.R., G.S. and C.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

This work was supported by the Romanian UEFISCDI project PN-III-P2-2.1-PED2021-2001, no. 631PED/2022.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Maharjan, P.; Martinez, D.A.; Weil, J.; Suesuttajit, N.; Umberson, C.; Mullenix, G.; Hilton, K.M.; Beitia, A.; Coon, C.N. Review: Physiological Growth Trend of Current Meat Broilers and Dietary Protein and Energy Management Approaches for Sustainable Broiler Production. Animal 2021, 15, 100284. [Google Scholar] [CrossRef]
  2. Zampiga, M.; Calini, F.; Sirri, F. Importance of feed efficiency for sustainable intensification of chicken meat production: Implications and role for amino acids, feed enzymes and organic trace minerals. J. World’s Poult. Sci. 2021, 77, 639–659. [Google Scholar] [CrossRef]
  3. Siegel, P.B. Evolution of the Modern Broiler and Feed Efficiency. Annu. Rev. Anim. Biosci. 2014, 2, 375–385. [Google Scholar] [CrossRef] [PubMed]
  4. Desbruslais, A.; Wealleans, A.L. Oxidation in Poultry Feed: Impact on the Bird and the Efficacy of Dietary Antioxidant Mitigation Strategies. Poultry 2022, 1, 246–277. [Google Scholar] [CrossRef]
  5. Krysiak, K.; Konkol, D.; Korczyński, M. Overview of the Use of Probiotics in Poultry Production. Animals 2021, 11, 1620. [Google Scholar] [CrossRef] [PubMed]
  6. Xu, C.; Kong, L.; Gao, H.; Cheng, X.; Wang, X. A Review of Current Bacterial Resistance to Antibiotics in Food Animals. Front. Microbiol. 2022, 13, 822689. [Google Scholar] [CrossRef]
  7. Selaledi, L.A.; Hassan, Z.M.; Manyelo, T.G.; Mabelebele, M. The Current Status of the Alternative Use to Antibiotics in Poultry Production: An African Perspective. Antibiotics 2020, 9, 594. [Google Scholar] [CrossRef]
  8. Panaite, T.D.; Saracila, M.; Papuc, C.P.; Predescu, C.N.; Soica, C. Influence of Dietary Supplementation of Salix alba Bark on Performance, Oxidative Stress Parameters in Liver and Gut Microflora of Broilers. Animals 2020, 10, 958. [Google Scholar] [CrossRef]
  9. Clavijo, V.; Morales, T.; Vives-Flores, M.J.; Reyes Muñoz, A. The gut microbiota of chickens in a commercial farm treated with a Salmonella phage cocktail. Sci. Rep. 2022, 12, 991. [Google Scholar] [CrossRef]
  10. Mangan, M.; Siwek, M. Strategies to combat heat stress in poultry production-A review. J. Anim. Physiol. Anim. Nutr. 2024, 108, 576–595. [Google Scholar] [CrossRef]
  11. Ivanova, S.; Sukhikh, S.; Popov, A.; Shishko, O.; Nikonov, I.; Kapitonova, E.; Krol, O.; Larina, V.; Noskova, S.; Babich, O. Medicinal Plants: A Source of Phytobiotics for the Feed Additives. J. Agric. Food Res. 2024, 16, 101172. [Google Scholar] [CrossRef]
  12. Abdel-Moneim, A.E.; Shehata, A.M.; Alzahrani, S.O.; Shafi, M.E.; Mesalam, N.M.; Taha, A.E.; Swelum, A.A.; Arif, M.; Fayyaz, M.; El-Hack, M.E.A. The Role of Polyphenols in Poultry Nutrition. J. Anim. Physiol. Anim. Nutr. 2020, 104, 1851–1866. [Google Scholar] [CrossRef] [PubMed]
  13. Papuc, C.; Goran, G.V.; Predescu, C.N.; Nicorescu, V.; Stefan, G. Plant Polyphenols as Antioxidant and Antibacterial Agents for Shelf-Life Extension of Meat and Meat Products: Classification, Structures, Sources, and Action Mechanisms. Compr. Rev. Food Sci. Food Saf. 2017, 16, 1243–1268. [Google Scholar] [CrossRef]
  14. Mamun, M.A.A.; Rakib, A.; Mandal, M.; Kumar, S.; Singla, B.; Singh, U.P. Polyphenols: Role in Modulating Immune Function and Obesity. Biomolecules 2024, 14, 221. [Google Scholar] [CrossRef] [PubMed]
  15. Masiala, A.; Vingadassalon, A.; Aurore, G. Polyphenols in Edible Plant Leaves: An Overview of Their Occurrence and Health Properties. Food Funct. 2024, 15, 6847–6882. [Google Scholar] [CrossRef]
  16. Bié, J.; Sepodes, B.; Fernandes, P.C.B.; Ribeiro, M.H.L. Polyphenols in Health and Disease: Gut Microbiota, Bioaccessibility, and Bioavailability. Compounds 2023, 3, 40–72. [Google Scholar] [CrossRef]
  17. Bešlo, D.; Golubić, N.; Rastija, V.; Agić, D.; Karnaš, M.; Šubarić, D.; Lučić, B. Antioxidant Activity, Metabolism, and Bioavailability of Polyphenols in the Diet of Animals. Antioxidants 2023, 12, 1141. [Google Scholar] [CrossRef]
  18. Zhang, L.; Guan, Q.; Jiang, J.; Khan, M.S. Tannin Complexation with Metal Ions and Its Implication on Human Health, Environment and Industry: An Overview. Int. J. Biol. Macromol. 2023, 253, 127485. [Google Scholar] [CrossRef]
  19. Wu, H.; Oliveira, G.; Lila, M.A. Protein-binding Approaches for Improving Bioaccessibility and Bioavailability of Anthocyanins. Compr. Rev. Food Sci. Food Saf. 2022, 22, 333–354. [Google Scholar] [CrossRef]
  20. Sugiharto, S.; Ranjitkar, S. Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Anim. Nutr. 2019, 5, 1–10. [Google Scholar] [CrossRef]
  21. Peng, W.; Talpur, M.Z.; Zeng, Y.; Xie, P.; Li, J.; Wang, S.; Wang, L.; Zhu, X.; Gao, P.; Jiang, Q.; et al. Influence of fermented feed additive on gut morphology, immune status, and microbiota in broilers. BMC Vet. Res. 2022, 18, 218. [Google Scholar] [CrossRef] [PubMed]
  22. Xu, F.; Wu, H.; Xie, J.; Zeng, T.; Hao, L.; Xu, W.; Lu, L. The Effects of Fermented Feed on the Growth Performance, Antioxidant Activity, Immune Function, Intestinal Digestive Enzyme Activity, Morphology, and Microflora of Yellow-Feather Chickens. Animals 2023, 13, 3545. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, M.; Yang, Z.; Wu, G.; Xu, F.; Zhang, J.; Luo, X.; Ma, Y.; Pang, H.; Duan, Y.; Chen, J.; et al. Effects of Probiotic-Fermented Feed on the Growth Profile, Immune Functions, and Intestinal Microbiota of Bamei Piglets. Animals 2024, 14, 647. [Google Scholar] [CrossRef] [PubMed]
  24. Zhu, X.; Tao, L.; Liu, H.; Yang, G. Effects of fermented feed on growth performance, immune organ indices, serum biochemical parameters, cecal odorous compound production, and the microbiota community in broilers. Poult. Sci. 2023, 102, 102629. [Google Scholar] [CrossRef]
  25. Leeuwendaal, N.K.; Stanton, C.; O’Toole, P.W.; Beresford, T.P. Fermented Foods, Health and the Gut Microbiome. Nutrients 2022, 14, 1527. [Google Scholar] [CrossRef]
  26. Sun, H.; Chen, D.; Cai, H.; Chang, W.; Wang, Z.; Liu, G.; Deng, X.; Chen, Z. Effects of Fermenting the Plant Fraction of a Complete Feed on the Growth Performance, Nutrient Utilization, Antioxidant Functions, Meat Quality, and Intestinal Microbiota of Broilers. Animals 2022, 12, 2870. [Google Scholar] [CrossRef] [PubMed]
  27. Han, S.; Xu, G.; Zhang, K.; Ahmad, S.; Wang, L.; Chen, F.; Liu, J.; Gu, X.; Li, J.; Zhang, J. Fermented Astragalus Powder, a New Potential Feed Additive for Broilers to Improve the Growth Performance and Health. Animals 2024, 14, 1628. [Google Scholar] [CrossRef]
  28. Dai, Z.; Cui, L.; Li, J.; Wang, B.; Guo, L.; Wu, Z.; Zhu, W.; Wu, G. Fermentation Techniques in Feed Production; Elsevier eBooks: Amsterdam, The Netherlands, 2020; pp. 407–429. [Google Scholar]
  29. Sokrab, A.M.; Mohamed Ahmed, I.A.; Babiker, E.E. Effect of fermentation on antinutrients, and total and extractable minerals of high and low phytate corn genotypes. J. Food Sci. Technol. 2014, 51, 2608–2615. [Google Scholar] [CrossRef]
  30. Samtiya, M.; Aluko, R.E.; Dhewa, T. Plant food anti-nutritional factors and their reduction strategies: An overview. Food Prod. Process. Nutr. 2020, 2, 6. [Google Scholar] [CrossRef]
  31. Salim, R.; Nehvi, I.B.; Mir, R.A.; Tyagi, A.; Ali, S.; Bhat, O.M. A review on anti-nutritional factors: Unraveling the natural gateways to human health. Front. Nutr. 2023, 10, 1215873. [Google Scholar] [CrossRef]
  32. Anderson, R.L.; Wolf, W.J. Compositional changes in trypsin inhibitors, phytic acid, saponins and isoflavones related to soybean processing. J. Nutr. 1995, 125, 581S–588S. [Google Scholar] [CrossRef]
  33. Adeyemo, S.M.; Onilude, A.A. Enzymatic Reduction of Anti-Nutritional Factors in Fermenting Soybeans by Lactobacillus plantarum Isolates from Fermenting Cereals. Niger. Food J. 2013, 31, 84–90. [Google Scholar] [CrossRef]
  34. Gogoi, P.; Sharma, P.; Mahajan, A.; Goudar, G.; Chandragiri, A.K.; Sreedhar, M.; Longvah, T. Exploring the nutritional potential, anti-nutritional components and carbohydrate fractions of Indian pigmented maize. Food Chem. Adv. 2023, 2, 100176. [Google Scholar] [CrossRef]
  35. Șonea, C.; Toader, M.; Năstase, I.P. The quality of maize grains in organic farming system. Rom Biotechnol. Lett. 2020, 25, 1781–1789. [Google Scholar] [CrossRef]
  36. Roger, T.; Léopold, T.N.; Funtong, M.C.M. Nutritional Properties and Antinutritional Factors of Corn Paste (Kutukutu) Fermented by Different Strains of Lactic Acid Bacteria. Int. J. Food Sci. 2015, 2015, 1–13. [Google Scholar] [CrossRef] [PubMed]
  37. Emkani, M.; Oliete, B.; Saurel, R. Effect of Lactic Acid Fermentation on Legume Protein Properties, a Review. Fermentation 2022, 8, 244. [Google Scholar] [CrossRef]
  38. Etuk, E.B.; Ifeduba, A.V.; Okata, U.E.; Chiaka, I.; Charles, O.I.; Okeudo, N.J.; Esonu, B.O.; Udedibie, A.B.I.; Moreki, J.C. Nutrient Composition and Feeding Value of Sorghum for Livestock and Poultry: A Review. Anim. Sci. Adv. 2012, 2, 510–524. [Google Scholar]
  39. Aladeen, A.M.A.; Omer Elbashier, M. The Effect of Replacement of Sorghum with Millet on Broilers Performance. Int. J. Sci. Res. 2013, 6, 2319–7064. [Google Scholar]
  40. McCuistion, K.C.; Selle, P.H.; Liu, S.Y.; Goodband, R.D. Sorghum as a feed grain for animal production. In Sorghum and Millets. Chemistry, Technology, and Nutritional Attributes, 2nd ed.; Taylor, J., Duodu, K., Eds.; Elsevier Inc. in cooperation with AACC International: Amsterdam, The Netherlands, 2019; pp. 355–391. [Google Scholar]
  41. Gunawan, S.; Dwitasari, I.; Rahmawati, N.; Darmawan, R.; Wirawasista Aparamarta, H.; Widjaja, T. Effect of Process Production on Antinutritional, Nutrition, and Physicochemical Properties of Modified Sorghum Flour. Arab. J. Chem. 2022, 15, 104134. [Google Scholar] [CrossRef]
  42. Karunaratne, N.D.; Newkirk, R.W.; Ames, N.P.; Van Kessel, A.G.; Bedford, M.R.; Classen, H.L. Effects of exogenous β-glucanase on ileal digesta soluble β-glucan molecular weight, digestive tract characteristics, and performance of coccidiosis vaccinated broiler chickens fed hulless barley-based diets with and without medication. PLoS ONE 2021, 16, e0236231. [Google Scholar] [CrossRef]
  43. McNab, J.M.; Smithard, R.R. Barley β-Glucan: An Antinutritional Factor in Poultry Feeding. Nutr. Res. Rev. 1992, 5, 45–60. [Google Scholar] [CrossRef] [PubMed]
  44. Ram, S.N.; Narwal, S.; Gupta, O.P.; Pandey, V.; Singh, G. 4—Anti-nutritional factors and bioavailability: Approaches, challenges, and opportunities. In Wheat and Barley Grain Biofortification; Woodhead Publishing Series in Food Science, Technology and Nutrition; Gupta, O.P., Pandey, V., Narwal, S., Sharma, P., Ram, S., Singh, G.P., Eds.; Woodhead Publishing: Sawston, UK, 2020; pp. 101–128. [Google Scholar] [CrossRef]
  45. Tanasković, S.J.; Šekuljica, N.; Jovanović, J.; Gazikalović, I.; Grbavčić, S.; Đorđević, N.; Sekulić, M.V.; Hao, J.; Luković, N.; Knežević-Jugović, Z. Upgrading of Valuable Food Component Contents and Anti-Nutritional Factors Depletion by Solid-State Fermentation: A Way to Valorize Wheat Bran for Nutrition. J. Cereal Sci. 2021, 99, 103159. [Google Scholar] [CrossRef]
  46. Alemayehu, G.F.; Forsido, S.F.; Tola, Y.B.; Teshager, M.A.; Assegie, A.A.; Amare, E. Proximate, mineral and anti-nutrient compositions of oat grains (Avena sativa) cultivated in Ethiopia: Implications for nutrition and mineral bioavailability. Heliyon 2021, 7, e07722. [Google Scholar] [CrossRef] [PubMed]
  47. Mehta, B.; Jood, S. Anti-Nutritional Factors and Mineral Content of Different Oat (Avena sativa L.) Varieties. Food Sci. Res. J. 2018, 9, 117–120. [Google Scholar] [CrossRef]
  48. Jasinska-Kuligowska, I.; Kuligowski, M.; Kolodziejczyk, P.; Michniewicz, J. Effect of fermentationextrusion and baking processes on content of fructans in rye products. Zywnosc-Nauka Technol. Jakosc 2013, 20, 129–141. [Google Scholar]
  49. Ismagilov, R.; Ayupov, D.; Nurlygayanov, R.; Ahiyarova, L.; Abdulloev, V. Ways to reduce anti-nutritional substances in winter rye grain. Physiol. Mol. Biol. Plants 2020, 26, 1067–1073. [Google Scholar] [CrossRef]
  50. Osman, A.; Hartung, C.B.; Lingens, J.B.; Rohn, K.; Schreiner, T.; Ahmed, M.F.E.; Hankel, J.; Abd El-Wahab, A.; Visscher, C. Fermentation Characteristics of Rye and Sorghum Depending on Water:Feed Ratio. Fermentation 2022, 8, 155. [Google Scholar] [CrossRef]
  51. Kumar, R. Anti-nutritional factors, the potential risks of toxicity and methods to alleviate them in Legume Trees and Other Fodder Trees as Protein Sources for Livestock. In Proceedings of the FAO Expert Consultation, Kuala Lumpur, Malaysia, 14–18 October 1991; FAO Animal and Health paper. Speedy, A., Pugliese, P., Eds.; FAO: Rome, Italy, 1991; p. 102. [Google Scholar]
  52. Shqueir, A.A.; Brown, D.L.; Taylor, S.J.; Rivkin, I.; Klasing, K.C. Effects of solvent extraction, heat treatments and added cholesterol on Sesbania sesban toxicity in growing chicks. Anim. Feed Sci. Technol. 1989, 27, 127–135. [Google Scholar] [CrossRef]
  53. Raharjo, Y.C.; Cheeke, P.R.; Patton, N.M. Effect of cecotrophy on the nutrient digestibility of alfalfa and black locust leaves. J. Appl. Rabbit Res. 1990, 613, 56–61. [Google Scholar]
  54. Sharma, R.; Garg, P.; Kumar, P.; Bhatia, S.K.; Kulshrestha, S. Microbial Fermentation and Its Role in Quality Improvement of Fermented Foods. Fermentation 2020, 6, 106. [Google Scholar] [CrossRef]
  55. Ramireddy, L.; Radhakrishnan, M. Cold Plasma Applications on Pulse Processing; Elsevier eBooks: Amsterdam, The Netherlands, 2021; pp. 295–307. [Google Scholar]
  56. Dittoe, D.K.; Olson, E.G.; Ricke, S.C. Impact of the Gastrointestinal Microbiome and Fermentation Metabolites on Broiler Performance. Poult. Sci. 2022, 101, 101786. [Google Scholar] [CrossRef] [PubMed]
  57. Saadi, S.; Saari, N.; Ghazali, H.M.; Abdulkarim, M.S. Mitigation of Antinutritional Factors and Protease Inhibitors of Defatted Winged Bean-Seed Proteins Using Thermal and Hydrothermal Treatments: Denaturation/Unfolding Coupled Hydrolysis Mechanism. Curr. Res. Food Sci. 2022, 5, 207–221. [Google Scholar] [CrossRef] [PubMed]
  58. Li, J.; Tao, L.; Zhang, R.; Yang, G. Effects of Fermented Feed on Growth Performance, Nutrient Metabolism and Cecal Micro-flora of Broilers. Anim. Biosci. 2022, 35, 596–604. [Google Scholar] [CrossRef]
  59. Feng, J.; Liu, X.; Xu, Z.R.; Wang, Y.Z.; Liu, J.X. Effects of Fermented Soybean Meal on Digestive Enzyme Activities and Intestinal Morphology in Broilers. Poult. Sci. 2007, 86, 1149–1154. [Google Scholar] [CrossRef]
  60. Haryati Supriyati, T.; Susanti, T.; Susana, I.W.R. Nutritional value of rice bran fermented by Bacillus amyloliquefaciens and humic substances and its utilization as a feed ingredient for broiler chickens. Asian Aust. J. Anim. Sci. 2015, 28, 231–238. [Google Scholar] [CrossRef] [PubMed]
  61. Ogbuewu, I.P.; Mabelebele, M.; Mbajiorgu, C.A. Determination of performance response of broilers to fermented tropical leaf meal supplementation using meta-analytical method. Trop. Anim. Health Prod. 2024, 56, 98. [Google Scholar] [CrossRef]
  62. Chen, B.; Li, D.; Leng, D.; Kui, H.; Bai, X.; Wang, T. Gut microbiota and meat quality. Front. Microbiol. 2022, 13, 951726. [Google Scholar] [CrossRef] [PubMed]
  63. Yang, X.Y.; Li, Y.X.; Li, Y. Effect of Ginkgo biloba extract on growth performance, slaughter performance and immune index in broilers. J. Fujian Agric. For. Univ. 2008, 3, 295–298. [Google Scholar]
  64. Agboola, T.O.; Balogun, O.L.; Rahji, M.A.Y. Stock Size and Relative Efficiency in Broiler Production in SouthWestern Nigeria: A Normalized Profit Function Approach. IOSR J. Agric. Vet. Sci. 2014, 7, 43–50. [Google Scholar] [CrossRef]
  65. Castellone, V.; Bancalari, E.; Rubert, J.; Gatti, M.; Neviani, E.; Bottari, B. Eating Fermented: Health Benefits of LAB-Fermented Foods. Foods 2021, 10, 2639. [Google Scholar] [CrossRef]
  66. Irawan, A.; Ratriyanto, A.; Respati, A.N.; Ningsih, N.; Fitriastuti, R.; Suprayogi, W.P.S.; Hadi, R.F.; Setyono, W.; Akhirini, N.; Jayanegara, A. Effect of feeding fermented soybean meal on broiler chickens’ performance: A meta-analysis. Anim. Biosci. 2022, 35, 1881–1891. [Google Scholar] [CrossRef] [PubMed]
  67. Saleh, A.A.; Shukry, M.; Farrag, F.; Soliman, M.M.; Abdel-Moneim, A.E. Effect of Feeding Wet Feed or Wet Feed Fermented by Bacillus licheniformis on Growth Performance, Histopathology and Growth and Lipid Metabolism Marker Genes in Broiler Chickens. Animals 2021, 11, 83. [Google Scholar] [CrossRef]
  68. Liu, Y.; Feng, J.; Wang, Y.; Lv, J.; Li, J.; Guo, L.; Min, Y. Fermented Corn-Soybean Meal Mixed Feed Modulates Intestinal Morphology, Barrier Functions and Cecal Microbiota in Laying Hens. Animals 2021, 11, 3059. [Google Scholar] [CrossRef] [PubMed]
  69. Bajagai, Y.S.; Klieve, A.V.; Dart, P.J.; Bryden, W.L. Probiotics in animal nutrition—Production, impact and regulation. In FAO Animal Production and Health Paper; Makkar, H.P.S., Ed.; FAO: Rome, Italy, 2016; Volume 179. [Google Scholar]
  70. Fathima, S.; Shanmugasundaram, R.; Adams, D.; Selvaraj, R.K. Gastrointestinal Microbiota and Their Manipulation for Improved Growth and Performance in Chickens. Foods 2022, 11, 1401. [Google Scholar] [CrossRef]
  71. Pendleton, B. The regulatory environment. In Direct-Fed Microbial, Enzyme and Forage Additive Compendium; The Miller Publishing Company: Minnetonka, MN, USA, 1998; Volume 4, pp. 47–52. [Google Scholar]
  72. Medellin-Peña, M.J.; Wang, H.; Johnson, R.; Anand, S.; Griffiths, M.W. Probiotics affect virulence-related gene expression in Escherichia coli O157: H7. Appl. Environ. Microbiol. 2007, 73, 4259–4267. [Google Scholar] [CrossRef]
  73. Meng, Q.; Yan, L.; Ao, X.; Zhou, T.; Wang, J.S.; Garrido-Galand, A.; Asensio-Grau, J.; Calvo-Lerma, A.; Heredia, A. The potential of fermentation on nutritional and technological improvement of cereal and legume flours: A review. Int. Food Res. 2021, 145, 110398. [Google Scholar] [CrossRef]
  74. Xiang, H.; Sun-Waterhouse, D.; Waterhouse, G.I.N.; Cui, C.; Ruan, Z. Fermentation-enabled wellness foods: A fresh perspective. Food Sci. Hum. Wellness 2019, 8, 203–243. [Google Scholar] [CrossRef]
  75. Tropini, C.; Earle, K.A.; Huang, K.C.; Sonnenburg, J.L. The Gut microbiome: Connecting spatial organization to function. Cell Host Microbe 2017, 21, 433–442. [Google Scholar] [CrossRef]
  76. Farré, R.; Fiorani, M.; Abdu Rahiman, S.; Matteoli, G. Intestinal Permeability, Inflammation and the Role of Nutrients. Nutrients 2020, 12, 1185. [Google Scholar] [CrossRef]
  77. Izadi, H.; Arshami, J.; Golian, A.; Raji, M.R. Effects of Chicory Root Powder on Growth Performance and Histomorphometry of Jejunum in Broiler Chicks. Dir. Open Access J. 2013, 4, 169–174. [Google Scholar]
  78. Raza, A.; Bashir, S.; Tabassum, R. An update on carbohydrases: Growth performance and intestinal health of poultry. Heliyon 2019, 5, e01437. [Google Scholar] [CrossRef] [PubMed]
  79. Vancamelbeke, M.; Vermeire, S. The Intestinal Barrier: A Fundamental Role in Health and Disease. Expert Rev. Gastroenterol. Hepatol. 2017, 11, 821–834. [Google Scholar] [CrossRef] [PubMed]
  80. Dao, D.P.D.; Le, P.H. Histology, Goblet Cells. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2024. Available online: https://www.ncbi.nlm.nih.gov/books/NBK553208/ (accessed on 23 September 2024).
  81. Horowitz, A.; Chanez-Paredes, S.D.; Haest, X.; Turner, J.R. Paracellular Permeability and Tight Junction Regulation in Gut Health and Disease. Nat. Rev. Gastroenterol. Hepatol. 2023, 20, 417–432. [Google Scholar] [CrossRef] [PubMed]
  82. Ménard, S.; Cerf-Bensussan, N.; Heyman, M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol. 2010, 3, 247–259. [Google Scholar] [CrossRef] [PubMed]
  83. Annunziata, G.; Arnone, A.; Ciampaglia, R.; Tenore, G.C.; Novellino, E. Fermentation of Foods and Beverages as a Tool for Increasing Availability of Bioactive Compounds. Focus on Short-Chain Fatty Acids. Foods 2020, 9, 999. [Google Scholar] [CrossRef] [PubMed]
  84. Siddique, A.; Azim, S.; Ali, A.; Adnan, F.; Arif, M.; Imran, M.; Ganda, E.; Rahman, A. Lactobacillus reuteri and Enterococcus faecium from Poultry Gut Reduce Mucin Adhesion and Biofilm Formation of Cephalosporin and Fluoroquinolone-Resistant Salmonella enterica. Animals 2021, 11, 3435. [Google Scholar] [CrossRef]
  85. Iqbal, Y.; Cottrell, J.J.; Suleria, H.A.R.; Dunshea, F.R. Gut Microbiota-Polyphenol Interactions in Chicken: A Review. Animals 2020, 10, 1391. [Google Scholar] [CrossRef]
Agriculture 14 01752 g001
Figure 1. The ingredients involved in the fermentation process (wet milled vegetal material in the presence of microorganisms acting in specific pH and temperature conditions) are in correlation with four of the most important arguments for using fermentation to improve feed safety and quality for broiler nutrition.
Figure 1. The ingredients involved in the fermentation process (wet milled vegetal material in the presence of microorganisms acting in specific pH and temperature conditions) are in correlation with four of the most important arguments for using fermentation to improve feed safety and quality for broiler nutrition.
Agriculture 14 01752 g001
Agriculture 14 01752 g002
Figure 2. The influence of fermenting plant material rich in anti-nutritional compounds on feed quality and implications for broiler health and, consequently, human health. (A) Most often found antinutritional complex in feed protein-tannin complex, metal—starch—phytate complex, inhibitor—enzyme complex; (B) Fermentation process enhancing feed quality and safety through microbial degradation of the complex compounds into smaller and easily absorbable compounds; (C) Highlighted products found in fermented feed like beneficial microorganism and antimicrobial peptides, metal ions, antioxidants, vitamins, short chain fatty acids, amino acids; (D) consequences of administration of fermented feed to broiler and humans as final receiver.
Figure 2. The influence of fermenting plant material rich in anti-nutritional compounds on feed quality and implications for broiler health and, consequently, human health. (A) Most often found antinutritional complex in feed protein-tannin complex, metal—starch—phytate complex, inhibitor—enzyme complex; (B) Fermentation process enhancing feed quality and safety through microbial degradation of the complex compounds into smaller and easily absorbable compounds; (C) Highlighted products found in fermented feed like beneficial microorganism and antimicrobial peptides, metal ions, antioxidants, vitamins, short chain fatty acids, amino acids; (D) consequences of administration of fermented feed to broiler and humans as final receiver.
Agriculture 14 01752 g002
Agriculture 14 01752 g003
Figure 3. Intestinal cytoprotective effect of fermented feed (A) and unfermented feed (B). Probiotic and prebiotic condition and stabilizes the gut structure; reduce pathogenic bacteria, increase small molecules content (amino acids, monosaccharides, antioxidants like vitamin C, polyphenols, SCFA) and free ions (Mg2+, Ca2+, Fe2+, Zn2+); increases the number of beneficial bacterial metabolites like bacteriocins; stabilize mucus layer; (A); unfermented feed promote longer period for digestion of protein—tannin complex, and metal—phytate complex, increased of inhibitor—enzyme complex, enterocyte villus atrophy, inflammation via pathogenic bacteria metabolites, development of pathogen microorganism on account of the fall in good bacteria number, goblet cells perturbation with the result of diminishing of mucus layer secretion (B).
Figure 3. Intestinal cytoprotective effect of fermented feed (A) and unfermented feed (B). Probiotic and prebiotic condition and stabilizes the gut structure; reduce pathogenic bacteria, increase small molecules content (amino acids, monosaccharides, antioxidants like vitamin C, polyphenols, SCFA) and free ions (Mg2+, Ca2+, Fe2+, Zn2+); increases the number of beneficial bacterial metabolites like bacteriocins; stabilize mucus layer; (A); unfermented feed promote longer period for digestion of protein—tannin complex, and metal—phytate complex, increased of inhibitor—enzyme complex, enterocyte villus atrophy, inflammation via pathogenic bacteria metabolites, development of pathogen microorganism on account of the fall in good bacteria number, goblet cells perturbation with the result of diminishing of mucus layer secretion (B).
Agriculture 14 01752 g003
Agriculture 14 01752 g004
Figure 4. Intercorrelation between gut microbiota and growth performance under the influence of fermented feed in broiler chicken.
Figure 4. Intercorrelation between gut microbiota and growth performance under the influence of fermented feed in broiler chicken.
Agriculture 14 01752 g004
Table 1. Antinutrient components found in plants, side effects and biotechnological solutions to mitigate them.
Table 1. Antinutrient components found in plants, side effects and biotechnological solutions to mitigate them.
Vegetal MatricesAntinutrient Components (ANC) Side Effects of Antinutrient ComponentsBiotechnological Solutions for Antinutrients MitigationReferences
Soybean Trypsin inhibitors, phytic acid, saponins and lectinsReduce the digestibility and absorption of the nutrients in the animal organismFermentation in the presence of Lactobacillus plantarum reduced the anti-nutritional factors in the milled soybeans[31,32,33]
Corn Phytate, tannins and polyphenolsBind dietary minerals in the gastrointestinal tract, decreasing their bio-accessibility and bioavailabilityFermentation with L. plantarum A6, L. brevis G11, L. brevis G25, L. fermentum N33, L. fermentum N25, L. buchneri M11, and L. cellobiosus M41, reduced the antinutritional factors.[29,34,35,36]
Sorghum Tannin (phenolic compounds), and dhurrinAffect the growth, feed intake, digestion of protein, egg production, and deformities of the legs of broiler chickensThe two-step procedure of sinking in a NaOH solution and fermentation (using L. bulgaricuss, L. casei, and L. brevis) lowers the ANC and enhances the nutritional composition. [37,38,39,40,41]
Barley β-glucanDecrease digestibility, form gels in aqueous media and excretion of sticky droppingsFermentation of barley with Rhizopus oligosporus, and supplementation with β-glucanase reduced ANC[42,43]
Wheat Phytate, protease inhibitors, tannins, lectins, alkaloids, and oxalateReduces the bioavailability of essential micronutrients such as iron and zincFermentation (Bacillus sp. TMF–2) as well as genetic engineering led to the reduction of ANC [44,45]
Oats Phytate, tannin, and oxalateDisrupt the stomach’s normal functioning and prevent nutrients from being absorbed.Saccharomyces cerevisiae fermentation, germination, de-branning, autoclaving, soaking reduced ANC[46,47]
Rye Water-soluble pentosans Clogged digestive tract with a viscous pentosan solution that prevents food nutrients being absorbed; esophageal and gastric blockagesFermentation with 1k2079 L. plantarum, 1k2103 Pediococcus pentosaceus, and 1k2082 L. lactis enzymes seem to reduce ANC[48,49,50]
Alfalfa Saponins Growth rate retardationFermentation with LAB reduced ANC[51,52,53]
Table 2. Examples of microorganisms used for preparation of fermented feed corelated with some growth performance parameters.
Table 2. Examples of microorganisms used for preparation of fermented feed corelated with some growth performance parameters.
Fermented Feed MicroorganismsVegetal MatricesEffects of Fermented Feed Groups Compared to the Control GroupReferences
Growth Performance ParametersOther Parameters
Lactobacillus casei (C37M41) Corn, soybean, and wheat, 6:2:2 (w:w:w)- ↗ BW during the first 21 days days for broiler treat with fermented feed in concentration of 3 kg ∙ t−1
↗ FCR during 0–42 days for broiler treat with fermented feed in concentration of 0.3 kg ∙ tone−1		- ↙ pathogenic microorganisms (phylum Delsulfobacterota and class Desulfovibriona and Negativicutes)
- ↗ beneficial microorganisms like Lactobacillaceae family		[21]
Bacillus amyloliquefaciensRice bran- ↗ fermented feed consumption in the first three weeks,
- ↗ FCR at the first three weeks of the feeding trial and BW		Zero mortality recorded during the experiment[60]
Lactobacillus and Bacillus subtilisCorn, soybean, cottonseed, and rapeseed (different ratio)- ↗ growth performance after addition of 10% fermented feed, in the first 21 days
- ↗ growth performance after addition of 5% fermented feed in 0–42 days of broiler life		- ↗ breast fat
- ↙ cholesterol content in broiler meat
- ↗ immune factors like IgM, IgG, and interferon-γ		[26]
Streptococcus alactolyticus, Lactobacillus acidophilus, Lactobacillus reuteriAstragalus powder- ↗ Final BW and ADG and ↙ F/G ratio for fermentation feed group compared to control and unfermented feed group- ↗ serum IgA and IgG, serum albumin, serum total antioxidant capacity
- ↙ serum and liver tissue malondialdehyde on day 28 and day 42. 		[27]
Bacillus licheniformisCorn–soybean (different ratio)↗ growth and digestibility for fermented feed group compared with other tested broiler groups- ↗ duodenal and ileal villi heights
- crypt depths weren’t not altered		[67]
Aspergillus oryzae 3.042Soybean- ↗ Fermented feed broiler presented growth and feed conversion promotion compared to another tested group- ↗ activities of trypsin, lipase, and protease in the intestinal content [59]
Bacillus spp., Lactobacillus spp., Saccharomyces cerevisiaeCorn, soybean and wheat bran, 6:2:2 (w:w:w)- ↗ nutrient absorption;
- ↙the abdominal fat rate and the muscle fat		- ↙ feed pH value and anti-nutritional factor concentrations
- ↗ good bacteria like Parasutterella, Butyricicoccus and Erysipelotrichaceae		[68]
Average daily gain—ADG; feed to gain ratio—F/G; ↗ means increased; ↙means decreased
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Predescu, N.C.; Stefan, G.; Rosu, M.P.; Papuc, C. Fermented Feed in Broiler Diets Reduces the Antinutritional Factors, Improves Productive Performances and Modulates Gut Microbiome—A Review. Agriculture 2024, 14, 1752. https://doi.org/10.3390/agriculture14101752

AMA Style

Predescu NC, Stefan G, Rosu MP, Papuc C. Fermented Feed in Broiler Diets Reduces the Antinutritional Factors, Improves Productive Performances and Modulates Gut Microbiome—A Review. Agriculture. 2024; 14(10):1752. https://doi.org/10.3390/agriculture14101752

Chicago/Turabian Style

Predescu, Nicoleta Corina, Georgeta Stefan, Mihaela Petronela Rosu, and Camelia Papuc. 2024. "Fermented Feed in Broiler Diets Reduces the Antinutritional Factors, Improves Productive Performances and Modulates Gut Microbiome—A Review" Agriculture 14, no. 10: 1752. https://doi.org/10.3390/agriculture14101752

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop