INTRODUCTION

The contemporary chicken industry necessitates elevated levels of productivity and efficient feed conversion, which can be partially attained through the use of particular feed additives [1]. The practice of administering antibiotics in poultry feed has been prevalent worldwide since the mid-20th century [2]. Antibiotics are administered in food animal production at both therapeutic and subtherapeutic levels to improve growth performance and maximize feed efficiency [2]. Nevertheless, there is increasing understanding and recognition of the negative consequences of using antibiotics as growth promoters in animal production, such as antimicrobial resistance in humans and animals, drug residue in animal products, toxicity, and environmental pollution. Several countries have implemented bans on the utilization of antibiotics in farm animal production [2].

The ban on antibiotic utilization in farm animal production has led to the emergence of alternative approaches, including the use of various organic acids, prebiotics, probiotics, enzymes, essential oils, bacteriophages, eubiotics, and phytogenic feed additives [3, 4]. Among the alternatives for replacing antibiotic growth promoters, organic acids and salts of organic acids, whether used individually or as blends, have garnered international recognition as potential substitutes for antibiotic growth promoters. This heightened attention stems from the growing global demand for organic and antibiotic-free poultry production, as these acids have demonstrated the ability to improve the health and performance of the poultry industry [5].

The term “organic acids,” popularly referred to as “acidifiers,” refers to a broad spectrum of chemical compounds often found in nature as typical components of plants, animal tissues, and microbes and are used in essential physiological processes and functions of the body [6]. Chemically, organic acids share similar properties with respect to their solubility in water, acidity, and lack of primary or secondary amines, as shown by their ninhydrin negativity [6].

Organic acids are characterized by the presence of a carboxylic acid group, denoted as R-COOH, and are classified as weak acids that act as intermediates in the breakdown of amino acids, sugars, and fatty acids. They are utilized in animal feed for their nutritional value, antibacterial properties, and role in stimulating energy metabolism [5]. Several types of organic acids are frequently employed in animal nutrition as feed additives (refer to Table 1). These acids' modes of action depend solely upon their pH and pKa values [4]. The use of organic acids and their salts as nonantibiotic feed additives in animal production is generally recognized as safe and has been authorized by the European Union [8].

Organic acids have been incorporated into animal diets worldwide over time because of their antibacterial properties, which can reduce the pH of the gastrointestinal tract. Most organic acids with antimicrobial properties have pKa values ranging from 3 to 5 [7]. Organic acids enhance growth performance by increasing nutrient accessibility in feed, increasing nutrient solubility in the gastrointestinal tract, and facilitating feed digestion and nutrient absorption [9]. Research has shown that organic acids and salts increase gastric proteolysis and improve the ability to digest protein and amino acids [10]. This review provides an overview of recent research findings regarding the antimicrobial effect of organic acids and the impact of organic acids on growth performance, intestinal health, and carcass and organ characteristics in broiler chickens.

MECHANISM OF ACTION OF ORGANIC ACIDS

Similar to antibiotics, organic acids possess antibacterial properties that significantly benefit gut health and development, ultimately impacting animal productivity and health. They exhibit both bactericidal and bacteriostatic properties. According to the study in ref. [11], the unique dissociation properties of organic acids are connected to their mode of action. Organic acids can penetrate the walls of bacterial cells and disrupt the physiological functions of numerous pathogenic microorganisms [6]. At low pH, organic acids are particularly effective, especially in their dissociated state, making them potent antimicrobial agents [7]. In their nondissociated form, organic acids are lipophilic, allowing themselves to penetrate bacterial and fungal cell membranes. Once inside the cell, they dissociate, lowering the intracellular pH and disrupting normal physiology [7, 10] (Figure 1). This dissociation process produces protons and anions, further reducing the internal pH to below 4.5 and inhibiting the growth of pH-sensitive bacteria such as coliforms, Clostridia, and Listeria, whereas pH-tolerant bacteria such as Lactobacillus and Bifidobacterium spp. endure [4]. The acidic intracellular environment hinders enzymatic reactions, transport systems, and energy-generating processes, ultimately leading to bacteriostasis [12]. To return the intracellular pH to an optimal range for development and to maintain the functionality of macromolecules, bacterial cells are compelled to expel protons via the H⁺-ATPase enzyme [13, 14] (Figure 1). H⁺-ATPase requires a significant quantity of metabolic energy, specifically adenosine triphosphate (ATP), to expel protons. The potential consequence of this phenomenon is the gradual reduction in ATP within cellular structures, ultimately resulting in cell death due to energy depletion [14].

ANTIMICROBIAL EFFECTS OF ORGANIC ACIDS

The intestinal microbiota is crucial for the digestion and immunological function of chickens, leading to improved growth performance [15]. The commonly encountered pathogenic bacteria that adversely affect the gastrointestinal health of chickens include Salmonella, Escherichia coli (E. coli), Campylobacter, and Clostridium perfringens. The proliferation of these bacteria can be effectively regulated by incorporating an organic acid into their dietary intake or drinking water.

Several studies have indicated that dietary organic acids promote feed consumption and growth performance by inhibiting the development and multiplication of pathogenic microbes while fortifying beneficial microorganisms in the gastrointestinal system [5, 16-18]. Emami et al. [19] found that the caecal microbiota of broiler chickens was altered when they were fed diets with organic acid blends (0.05%–0.1% formic and propionic acids). This resulted in an increase in the population of Lactobacilli and a decrease in the population of E. coli. Supplementation with a coated essential oil and organic acid mixture at 500 mg/kg in the diet of broiler chickens, both challenged and nonchallenged with E. coli, effectively reduced caecal E. coli counts without significantly impacting Lactobacillus populations [20]. Similarly, dietary supplementation with coated essential oils and organic acid mixture at 300, 500, and 800 mg/kg in broiler chickens infected with Salmonella Enteritidis reduced the Salmonella load in the cecum and internal organs (liver and spleen) [21]. A latest study demonstrated that broiler chickens supplemented with 0.5% and 1.0% formic acid, 0.5% and 1.0% acetic acid, and 2.0% and 3.0% citric acid exhibited a significant reduction in total bacterial count, including E. coli and Proteus spp., while simultaneously showing a significant increase in Lactobacillus count [22]. Ebeid et al. [23] reported that giving broiler chickens a 0.06% mixture of propionic and acetic acid in their drinking water decreased the presence of Salmonella and E. coli in the gut compared with that in broiler chickens in the control group. In their study, adding a blend of organic acids at a concentration of 0.03% increased the population of Bacillus subtilis in broiler chickens' breast meat, while the addition of a 0.06% blend of organic acid led to a reduction in both the total bacterial count and the count of E. coli [23]. Islam et al. [24] noted that the growth of Clostridium perfringens, E. coli, and Salmonella was reduced in broiler chickens that were fed organic acid blends alone or in combination with essential oils, whereas Lactobacillus growth was positively improved. In an experiment conducted by Bourassa et al. [25], dietary inclusion of formic and propionic acid in broiler chicken diet at a concentration of 1–5 kg per ton led to a reduction in Salmonella levels in the caeca. The potential ability of organic acids to inhibit the growth of harmful bacteria in the gastrointestinal system and breast meat can be attributed to a decrease in pH, which effectively impedes the reproduction and spread of pathogenic bacteria. Moreover, acidophilic bacteria such as Lactobacilli are capable of withstanding variations in pH levels between the internal and external environments [26]. Manvatkar et al. [9] discovered that incorporating 1 g/kg of mix-coated organic acids into the feed of broiler chickens led to a noteworthy decrease in the caecal bacterial population. In addition, a significant reduction in the total number of bacteria in the cecum was observed when broiler chickens were fed diets containing organic acid [27]. The observed decline in the overall number of viable microorganisms could be attributed to the antibacterial properties of the blend-coated organic acid. This acid is believed to penetrate bacterial cells in an undissociated state, leading to a decrease in the intracellular pH and a subsequent reduction in microbial viability.

Furthermore, there was a notable increase in the population of Lactobacillus in the microbial community of broiler chicken excreta fed a diet supplemented with a combination of medium-chain fatty acids and organic acids [28]. Organic acids in the broiler chicken diet have been found to improve the beneficial microbial profile, specifically by increasing Lactobacillus spp., as observed in several other studies [29]. An increase in the Lactobacillus population yields a beneficial effect on intestinal function through a reduction in enteric pathogen viability, which is attributable to the acidic conditions produced by Lactobacillus fermentation [28]. When the population of pathogenic microorganisms decreases, there is a corresponding decrease in the metabolic demands of these microbes. Consequently, this reduction in metabolic requirements leads to an increase in the availability of dietary energy and nutrients for the host animal.

EFFECTS OF ORGANIC ACIDS ON GROWTH PERFORMANCE

The utilization of organic acids has become important as a growth enhancer to improve the performance of poultry (Table 2). There has been growing evidence that broiler chickens that are fed diets with different sources and concentrations of organic acids perform better in terms of growth [40]. The growth-enhancing effects of organic acids are attributed to their capacity to regulate the gastrointestinal tract microbiota, improve the microstructure of the gut, activate the immunological system, and trigger the release of various digestive enzymes [17, 41].

Fik et al. [30] demonstrated that adding citric acid to the drinking water of broiler chickens at different concentrations (0.5%, 1.0%, and 1.50%) resulted in an increase in body weight compared with that of the control group. The findings indicated that the inclusion of 1.50% citric acid in the drinking water of broiler chickens had the most significant impact on growth performance. The positive impact of citric acid on the gut microbiota is likely the main cause of improved body weight growth. The results of Islam et al. [24] revealed that an organic acid blend supplemented at 200 mg/kg alone or in combination with 150 mg/kg essential oil in a broiler chicken diet improved body weight gain (BWG) and feed intake without affecting the feed conversion ratio (FCR) compared with the control group and the group supplemented with 50 mg/kg enramycin in the starter, finisher, and overall phases. Similarly, improved average body weight and average body gain were obtained in broiler chickens supplemented with mixed organic acids and essential oils in drinking water [32]. In a recent study, supplementing the diet of broiler chickens with 800 mg/kg of the new buffer salt-protected sodium butyrate significantly improved average daily gain and average daily feed intake, while also enhancing the FCR compared to broiler chickens supplemented with antibiotics [31]. In addition, the inclusion of protected organic acid blends in the diets of broiler chickens at doses of 0.3, 0.6, and 1 g per kg of feed resulted in increased BWG and an improved FCR compared with those of the control group [9]. The results revealed that broiler chickens fed with 1 g of protected organic acid blends presented the highest BWG (2806.70 g) and better FCR (1.50). Better nutrient utilization leading to higher BWG could cause an improvement in the FCR. The findings of Ma et al. [33] showed that the supplementation of mixed organic acid in a broiler chicken diet at rates of 3000 and 6000 mg/kg significantly improved the average daily weight gain, final weight, and FCR. The results showed that supplementing mixed organic acids in broiler diets did not affect average daily feed intake.

According to Nourmohammadi et al. [42], acidifiers such as organic acid positively impact performance by increasing nutrient utilization and enhancing digestibility. The findings of Rehman et al. [35] indicated that broiler chickens fed with acetic acid at concentrations of 10, 20, and 30 g/kg of feed from 8 to 42 days of age had improved FCR and BWG than the broiler chickens in the control group. Compared with the other groups, the broiler chickens fed with 30 g acetic acid kg⁻¹ of feed presented the highest BWG, low feed consumption, and an improved FCR. The observed improvement in FCR may be due to reduced feed intake, leading to greater weight gain as a result of improved nutrient utilization. Katoch et al. [36] reported that commercial broiler birds fed with citric acid (0.5%) in a formulated diet with low and moderately low mineral density (calcium and phosphorus), respectively, had better BWG and lower mortality percentages than the control group. Additionally, Salgado-Tránsito et al. [43] reported that, compared with control chicks, broiler chicks fed with 6.25, 12.5, 25, or 50 g of citric acid per kg of feed from days 1 to 28 had improved FCR and live body weight. The results revealed that broiler chicks fed with 50 g of citric acid per kg of feed had the greatest live weight gain (1013 g) and better FCR (1.55). The observed improvement in the growth performance of broiler chickens resulting from the inclusion of organic acids can be attributed to several factors. These factors include an increase in the energy and protein composition of the feed, a decrease in harmful microorganisms, an enhancement of the immune system, a decrease in the spread of infectious agents, and a decrease in the presence of ammonia and other harmful metabolites. Organic acids are widely recognized for their ability to enhance overall performance through a reduction in the total microbial load and microbial competition for nutrients within the gastrointestinal tract. As a result, the risk of subclinical infections is diminished, resulting in an improved ability to break down food and reduce the energy requirement of the gut-associated tissue [44]. Furthermore, organic acids play crucial roles in various physiological processes inside the gastrointestinal tract. One such function is their ability to convert inactive pepsinogen into its active form, known as pepsin. Additionally, organic acids play crucial roles as significant sources of energy in the gastrointestinal tract and contribute to the regulation of the stomach-emptying rate. Moreover, these acids have been found to increase the production of endogenous enzymes. Finally, organic acids can chelate minerals, hence influencing their availability and absorption [13].

On the other hand, organic acids do not always positively affect broiler performance or productivity. Several studies [36, 43, 44] have demonstrated that the use of organic acids as dietary supplements has no significant effect on the growth performance of broiler chickens. These results may depend on the chemical form of the organic acid, pKa values, differences in the levels of organic acids, site of action of the acids, poultry species, agroclimatic differences, diet ingredients, health status, and age of the animal [5]. These inconsistent findings may be attributed to broiler chickens being exposed to suboptimal conditions, such as feed with low digestibility and less hygienic environmental conditions. However, higher inclusion levels of organic acids, such as citric acid, at 6% and 60 g/kg in the diet of broiler chickens resulted in retarded growth and lower feed consumption [45, 46]. This could result from the reduced palatability of the feed due to the higher inclusion level of the acid.

EFFECTS OF ORGANIC ACIDS ON INTESTINAL HEALTH

Indices related to the histomorphology of the intestine, such as the villus height, muscularis thickness, crypt depth, villus surface area, epithelial thickness, and villus height-to-crypt depth ratio, are important markers for assessing the function of the small intestine. Moreover, goblet cells serve as a reliable indicator of intestinal function because of their role in the production of mucin, a substance that coats the epithelial surface and acts as a protective barrier against the attachment of detrimental microorganisms [47]. Various researchers have documented the beneficial effects of organic acid supplementation on the intestinal histomorphometry of broiler chickens [25, 47]. The inclusion of mixed organic acid at 3000 mg/kg and 6000 mg/kg in the diet of broiler chickens had a positive effect on crypt depth, villus height, and the ratio of villus height to crypt depth in different sections of the small intestine of 21-day-old and 42-day-old broiler chickens [33]. However, a contrary finding was reported in broiler chickens supplemented with a mixed liquid acidifier and essential oil in drinking water [32].

According to Khosravinia et al. [38], adding 30 g/kg and 60 g/kg citric acid to the feed of broiler chickens had a positive effect on the length of the villi, depth of the crypts, and the ratio of villus length to crypt depth in the duodenum, jejunum, and ileum of 42-day-old broiler chickens. Manvatkar et al. [9] also reported that 42-day-old broiler chickens fed a diet with blend-coated organic acids at rates of 0.6 and 1 g/kg had significantly greater intestinal villus heights in the duodenum, jejunum, and ileum than those in the control group. Similarly, a study by Rehman et al. [35] reported that dietary supplementation with acetic acid at 10, 20, and 30 g/kg of feed in broiler chicken diet significantly (p < 0.05) improved the duodenal villus height, crypt depth, and villus surface area of 49-day-old broiler chickens. Broiler chickens supplemented with 30 g of acetic acid in their diet presented the highest duodenal villus height (1379.70 μm), deeper crypt depth (229.33 μm), and larger villus surface area (0.3167 mm²). In addition, supplementation with acetic acid also increased the villus height of the jejunum and ileum, the villus surface area of the jejunum, and the crypt depth of the ileum. Broiler birds supplemented with 30 g of acetic acid per kg of feed had the greatest villus height in the jejunum (147.43 μm) and ileum (828.00 μm). However, acetic acid supplementation in the broiler chicken diet did not significantly affect the crypt depth or the villus surface area in either the jejunum or ileum. The results of Sikandar et al. [37] revealed that, compared with control chickens, broiler chickens fed with sodium butyrate (at 0.5 and 1 g/kg of feed) for 21 and 35 days had increased villus surface areas, higher villus heights, and increased villus height-to-crypt depth ratios in various sections of the small intestine. This could be attributed to the fact that butyrate serves as a highly abundant energy source for enterocytes in the intestinal gastrointestinal tract, perhaps leading to an increase in cell mitosis within the crypt.

Similarly, Ogwuegbu et al. [48] discovered that adding sodium butyrate at a dosage of 4 g/kg to the feed of broiler chickens resulted in a significant increase in the length of the villi, depth of the crypts, thickness of the epithelium, and muscle thickness in the duodenum, jejunum, and ileum of both starter and finisher birds. Sodium butyrate promotes the proliferation of enterocytes in the intestinal mucosa and the elongation of villi, leading to an increase in villus height and deeper crypts [8]. Zhao et al. [34] reported that broiler birds who were fed chemically protected sodium butyrate (1000 mg/kg) had greater villus height-to-crypt depth ratios in the duodenum, jejunum, and ileum of 21-day-old broiler chickens than those in the control group and broiler group supplemented with antibiotics in their diet. In addition, the crypt depth in the duodenum, jejunum, and ileum of 21-day-old broiler chickens was not significantly different between birds that were fed a control diet, those that were fed a chemically protected sodium butyrate diet, and those that were fed a diet supplemented with antibiotics. Sun et al. [49] concluded that supplementing organic acid in the diets of broiler chickens at various inclusion levels (500, 1000, and 1200 mg/kg) increased the duodenal villus height, crypt depth, and villus height of the jejunum compared with those of the control. Broiler birds fed with 1000 and 1200 mg/kg organic acid products had the highest villi height (4045 and 4085 μm, respectively) in the duodenum. Compared with the control diet, supplementation with 1000 or 1200 mg/kg organic acid products in the broiler chicken diet decreased the villus height in the ileum. However, the crypt depth of the jejunum and ileum, as well as the villus height-to-crypt depth ratio, were not significantly affected.

The improvements in villus height, villus surface area, and crypt depth in the small intestine of broiler chickens could be a result of the acidic nature of organic acids in lowering the pH of the gastrointestinal tract, thereby creating a less favorable environment for harmful bacteria and pathogens [35]. This promotes the growth of beneficial bacteria, which can improve nutrient absorption and reduce inflammation in the gut. As a result, the villi in the intestine can grow longer and more efficiently absorb nutrients from feed. Furthermore, Liao et al. [50] found a strong correlation between organic acids and intestinal microbial populations in promoting the development of a healthy gut structure in broiler chickens. Additionally, organic acids have been shown to stimulate the production of digestive enzymes, further enhancing nutrient absorption and overall gut health.

EFFECTS OF ORGANIC ACIDS ON CARCASS AND ORGAN CHARACTERISTICS

According to Malematja et al. [51], carcass assessment is the most crucial aspect of broiler production because it reflects the amount of meat produced. Fik et al. [30] reported that supplementation with 0.5, 1.0, or 1.5% citric acid in the drinking water of broiler chickens did not affect the carcass yield or drumstick percentage of the birds. However, a significant increase in the proportion of breast meat was observed in broiler chickens supplemented with citric acid. The organ weights (the heart, crop, neck, proventriculus, pancreas, cecum, kidney, and large intestine) of the control group and broiler birds supplemented with citric acid did not differ. However, the inclusion of 0.5% citric acid in the drinking water of broiler chickens resulted in substantial decreases in the liver, gizzard, and small intestine compared with those of the groups supplemented with 1.0% or 1.5% citric acid. Manvatkar et al. [9] reported that eviscerated yield, carcass yield, drumstick, breast meat, and relative organ weights were improved in broiler chickens fed with blend-coated organic acids, but the yield of cutup parts (thigh, wing, and back cut weight) was comparable. The findings of Rehman et al. [35] showed that the dressing percentage of broiler chickens was not significantly affected by dietary supplementation with acetic acid at 10, 20, or 30 g/kg of feed, but significantly improved the length and weight of the small intestine. The beneficial effects of acetic acid on the small intestine may be due to the bacteriostatic and bactericidal properties of organic acids, which enhance the health of the gastrointestinal tract. Citric acid supplementation at 2.4, 3.2, and 4.0 mg/kg of feed in broiler chicken diets did not affect dressing or carcass percentage or gizzard, liver, or heart weight in 42-day-old broiler chickens [39]. Similarly, dietary supplementation with acetic acid at various inclusion levels (1%, 2%, 4%, 8%, and 10%) in broiler chicken diet did not significantly (p > 0.05) affect the internal organs (liver, pancreas, spleen, and small intestine) of broiler chickens [52]. The eviscerated carcass percentage, giblet weight, and carcass cuts (excluding the back cut) of broiler chickens were not affected by supplementation with formic acid, butyric acid, or their combination in the diet of broiler chickens [53].

CHALLENGES AND POSSIBLE SOLUTIONS IN UTILIZING ORGANIC ACIDS IN BROILER CHICKEN NUTRITION

Despite the ability of organic acids to enhance gut health, increase nutrient uptake, and act as a substitute for antibiotics, the practical application of organic acids in broiler diets poses several challenges, and these challenges may impact their efficacy and cost efficiency. First, the efficacy of organic acids can vary greatly based on factors such as the specific acid, its concentration, the age and health of the birds, and diet composition. To address this issue, additional research is necessary to pinpoint the best blends and levels of organic acids for various production setups. Precision feeding strategies, where the diet is tailored to the specific requirements of the birds, can contribute to attaining more reliable results.

Second, one difficulty in utilizing organic acid as a feed additive and substitute for antibiotics in broiler chicken nutrition is that it has the potential to render the feed less palatable, especially at relatively high concentrations, which could result in feed refusal. Encapsulation technologies can be used to cover the flavor of organic acids, ensuring that their inclusion does not compromise feed intake. In addition, broiler birds can gradually acclimate to the taste of organic acids through strategies that slowly increase the concentration of organic acids over time. This gradual acclimation may enhance feed acceptance and optimize the beneficial effects of organic acids on gut health and nutrient absorption.

Furthermore, the cost of organic acids can be relatively high, particularly when high-purity forms or encapsulated products are used. This can create economic challenges for widespread adoption in broiler production systems. Using organic acids along with probiotics or essential oils can increase cost-effectiveness by potentially lowering dosages without compromising effectiveness.

Additionally, the continuous use of organic acids may lead to the development of microbial resistance, similar to the issues faced with antibiotic use. This could reduce the long-term effectiveness of organic acids in controlling pathogenic bacteria. Hence, the rotational use of different types of organic acids combined with other antimicrobial strategies can help mitigate the risk of resistance development. However, the presence of other antimicrobial compounds may reduce their efficacy. Hence, it is important to understand the chemical interactions between different compounds.

CONCLUSION AND FUTURE PROSPECTS

Organic acids have demonstrated efficacy as a viable substitute for antibiotic growth promoters in broiler chicken nutrition. Previous findings indicate that organic acids have a positive impact on the intestinal microbial balance, promote growth performance, improve carcass characteristics, and enhance the intestinal health of broiler chickens. Organic acids can alter or decrease the pH of the gastrointestinal tract; hence, decreasing the impact of pathogenic bacteria and increasing the proliferation of beneficial microbes. Consequently, this leads to an increase in the intestinal histomorphological traits in the different segments of the small intestine, thereby leading to increased nutrient absorption. However, the efficacy of organic acids is influenced by numerous factors, and additional studies are necessary to establish standardized protocols, dosages, and application methods to achieve a more thorough understanding and maximize the effectiveness of organic acids in broiler chicken nutrition. In addition, future research is needed to determine the influence that dietary organic acids have on the palatability of feed in broiler chickens.

AUTHOR CONTRIBUTIONS

Prosper Chukwudi: Conceptualization; writing—original draft; writing—review & editing. Paulinus Ikenna Umeugokwe: writing—original draft; writing—review & editing. Nnanna Ephraim Ikeh: Conceptualization; writing—original draft; writing—review & editing. Bright Chigozie Amaefule: Writing—original draft; writing—review & editing.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.