1. Please check and comment entries here.
Table of Contents

    Topic review

    Organic Acids and Feeding

    View times: 9
    Submitted by: Dhanushka Rathnayake

    Definition

    Because the application of antibiotic growth promoters (AGP) causes accelerated adverse effects on the animal diet, the scientific community has taken progressive steps to enhance sustainable animal productivity without using AGP in animal nutrition. Organic acids (OAs) are non-antibiotic feed additives and a promising feeding strategy in the swine and broiler industry. Mechanistically, OAs improve productivity through multiple and diverse pathways in: (a) reduction of pathogenic bacteria in the gastro-intestinal tract (GIT) by reducing the gut pH; (b) boosting the digestibility of nutrients by facilitating digestive enzyme secretion and increasing feed retention time in the gut system; and (c) having a positive impact and preventing meat quality deterioration without leaving any chemical residues. Recent studies have reported the effectiveness of using encapsulated OAs and synergistic mechanisms of OAs combinations in swine and broiler productivity. On the other hand, the synergistic mechanisms of OAs and the optimal combination of OAs in the animal diet are not completely understood, and further intensive scientific explorations are needed. 

    1. Introduction

    The ultimate goal in the global livestock sector is to achieve enhanced quantitative and qualitative productive parameters. A few decades ago, enhanced production was gained by incorporating various antibiotic growth promoters (AGP), which resulted in improved feed efficacy, growth rate, and lower mortality and disease. On the other hand, the emergence of antimicrobial-resistant bacteria has led to a discussion regarding the global health problem. Consequently, the utilization of AGP was banned by the European Union. Thus, scientists and researchers have focused on sustainable potential antibiotic-free production systems in the poultry sector [1] and swine industry [2].
    Researches have highlighted the effective utilization of organic acids (OAs), phytobiotics, probiotics, prebiotics, bacteriophages, and other numerous alternatives instead of antibiotics to establish appropriate health and production parameters of animals. As a group of chemicals, organic acids can be defined as carboxylic acids including fatty acids, which have the chemical structure of R-COOH with specific chemical characteristics. They can be categorized into three groups: (a) simple mono-carboxylic acids (acetic, formic, propionic, and butyric acids); (b) carboxylic acids containing hydroxyl group (malic, lactic, tartaric, and citric acids); and (c) carboxylic acids with double bonds (sorbic and fumaric acids) [3]. OAs produce effective responses owing to their antimicrobial properties, which can enhance the pH reduction rate in the GIT [4]. Consequently, the intestinal digestibility and mineral utilization were improved [5][6]. Acidifiers were incorporated into animal diets a few years earlier owing to the presence of preservatives and nutritional characteristics [7][8]. Despite controlling the desirable growth rate of molds, fungi, and bacteria in animal feed, several studies have reported the potential ability of improving nutrition digestion and retention, intestinal health, and ultimate growth development of non-ruminant animals, including feed sanitizing characteristics [9][10][11]. Effective production parameters and health-promoting evidence have been discovered for numerous OAs, such as citric, fumaric, and formic acids and their salts [12]. Enhanced meat quality characteristics and growth performances were observed in broilers fed a diet supplemented with OAs, including 30% lactic, 25.5% benzoic, 7% formic, 8% citric, and 6.5% acetic acid [13]. Partanen and Morz [7] reported that incorporating OAs into the pig diet modulates the beneficial gut microbiota and improves the growth performance. A reduced gastric pH and retarded enterotoxigenic E. coli proliferation in the gut system occurred due to the inclusion of lactic acid into the pig diet. Thus, developed gut health led to optimal feed intake and weight gain of the animal [14]. Furthermore, supplementation of OAs with feedstuff will increase the stimulation rate of the nutrient digestion process [15]. The application of OAs in the livestock sector has produced numerous benefits in both economic and quality product perspectives in the livestock sector (Figure 1).
    Figure 1. Various application and benefits of organic acids in the livestock sector [16].
    Each organic acid has a distinguished range of pH, antimicrobial potential, pKa values, and membrane structure. Especially, a combination of OAs has various pKa values directly influencing the intestine pH due to the developed synergistic effect [17]. The most common OAs involved in animal nutrition are listed below (Table 1).
    Table 1. Common organic acids involved in animal nutrition and their properties [16][18].
    Acid Chemical Name Registration Number Molecular Weight/GE (MJ/Kg) Odor pKa
    Butyric Butanoic Acid - 88.12/24.8 rancid 4.82
    Citric 2-Hydroxy-1,2,3-Propanetricarboxylic Acid E 330 192.1/10.2 odorless 3.13
    Propionic 2-Propanoic Acid 1a297 74.08/20.6 pungent 4.88
    Sorbic 2,4-Hexandienoic Acid E 200 112.1/27.85 mildly acrid 4.76
    Formic Methanoic Acid E 236 46.03/5.7 pungent 3.75
    Acetic Ethanoic Acid E 260 60.05/14.6 pungent 4.76
    Lactic 2-Hydroxypropanoic Acid E 260 90.08/15.1 sour milk 3.83
    Malic Hydroxybutanedioic Acid E 296 134.1/10.0 apple 3.40
    Fumaric 2-Butenedioic Acid 2b08025 116.1/11.5 odorless 3.02
    Benzoic Benzenecarboxylic acid - - - 4.20

    2. Potential Modes of Action of OAs

    OAs have numerous benefits on the health and development of the gut system. Nevertheless, the mode of action is not completely understood. Their modes of action may be attributed partially to different factors, such as (A) mineral chelation and stimulation on intermediary metabolism; (B) inhibition of the development of pathogenic microbes; (C) facilitation of proper digestion due to lower gastric pH and enhanced pepsin secretion; and (D) reduction of gastric emptying rate and maintenance of endogenous enzymes secretion [4][19].

    2.1. Effect of OAs on Mineral Utilization and Nutrient Digestibility

    OA anions form complexes with Mg, P, Ca, and Zn, improving digestion and minimizing the excretion of beneficial minerals from the body. Phytate phosphorous utilization occurs through OAs administration by providing favorable pH conditions to convert phytase into hydrolyze phytate [20]. Bolling et al. [21] reported that citric acid facilitates the removal of attached minerals to phytate molecules, such as Ca, P, and Zn. Furthermore, it has been found that fumaric acid also can enhance the apparent absorption and retention of Ca, P, and Zn in the gastro-intestinal tract (GIT) [22].
    The inclusion of OAs into the diet can improve energy utilization of certain feedstuffs. In soybean meal, for instance, the lower metabolizable energy (ME) in soybean meal occurs due to retarded digestibility in the carbohydrate portion. However, the presence of endogenous α-(1,6)-galactosidase enzyme in the intestines will facilitate the proper digestion of carbohydrate portion in the soybean meal. Ao [23] reported that the inclusion of 2% citric acid increased the digestion process by enhancing the activity of the α-galactosidase enzyme. Moreover, by reducing the chime pH, OAs supplementation improved protein digestion owing to microbial phytase activity and induced pepsin secretion [24]. A further protein digestion process improves through the secretion of a greater level of chymotrypsinogen A, chymotrypsinogen B, procarboxy peptidase A, procarboxy peptidase B, and trypsinogen enzymes [25]. OAs inclusion also increased the proper absorption rate of nutrients in the GIT by increasing the digesta retention time [26]. The increased ME and crude protein (CP) were observed due to the reduced microbial competition with the host, ammonia emission, and endogenous nitrogen elimination [27].

    2.2. Effect of OAs on Antimicrobial Activity and Pathogenic Bacteria

    Both animals and plants have symbiotic relationships with various microbes to survive in the environment through an active defense system against pathogens and to regulate the metabolism associated with hormones. On the other hand, an excessive microflora content produces unnecessary competition between the host and nutrition. Hence, maintenance of the optimal microbe composition in the GIT should be investigated. Some OAs can alter the GIT by eradicating foodborne pathogens, such as Salmonella and E. coli species [28]. Owing to pH reduction and their influence on the buffering capacity of the diet, OAs can improve gut health by providing the optimal environment to beneficial microbes while preventing the proliferation of pathogens [7][29][30]. OAs can be divided into two groups based on the microbial ameliorate capacity in the GIT (Figure 2).
    Figure 2. Two different mechanisms of organic acids on altering the pH of the GIT and their impact on pathogens [15].
    Non-disassociated OAs enter the cytoplasm through the semipermeable membrane of the microorganism. Thereafter, OAs release their protons (H+), and the cytoplasm pH decreases gradually. The enzymes involving reactions, such as nutrient transportation and glycolysis signal transductions of the microbes, are curtailed. Consequently, an energy deficiency occurs to maintain the normal pH [31]. Owing to the acidic conditions in the stomach, the efficacy of OAs is greater than under neutral pH conditions, as in the intestines. On the other hand, most bacteria species require optimal environmental pH conditions and pH < 4.5 (extreme lower) conditions, which adversely affect their survival. By releasing H+ ions, OAs aid in the dysfunctions, retardation, or inhibition of the multiplication of pH-sensitive bacteria [32].
    Some bacteria in the GIT secrete various harmful compounds that reduce fat digestibility, stimulate rapid turnover of absorptive epithelial cells, stimulate mucus secretion, and induce an inflammatory responses due to the developed immune system. These factors help retard the growth performance, and approximately 6% net energy losses in pigs can be attributed to microflora [33]. OAs have the potential to eliminate specific species, such as Coliforms, while generating eubiosis. Thus, they can provide the optimal microbial atmosphere in the GIT that can benefit the host by accumulating lower toxic compounds, amines, and ammonia. While the gram-positive (G+) bacteria are susceptible to long-chained OAs, the gram-negative (G) bacteria cannot resist OAs with fewer than eight carbons [34]. However, stronger effects of OAs affect G+ bacteria due to cell structural differences. In contrast, the cytoplasmic membrane of bacteria is surrounded by a thick peptidoglycan layer. Generally, this peptidoglycan layer is thicker in G+ bacteria than G bacteria. Nevertheless, G bacteria have an extra lipopolysaccharide layer that is more resistant to hydrophobic antibiotics and chemical compounds.
    Because OAs have both bactericidal and bacteriostatic properties, Luckstadt and Mellor [35] sketched out the mode of action of OAs on G bacteria as follows: (1) Lipophilic undissociated OAs penetrate the G bacteria cytoplasm (Salmonella). (2) OAs release H+ ions, which reduces the cellular pH, and the enzyme-based microbial metabolism tends to decrease (3). To restore the normal cytoplasmic pH, the cell is forced to discard H+ ions through the cell membrane via the H+- ATPase pump. (4) Ultimately, G bacteria proliferation is gradually impeded when exposed to OAs for some time (Figure 3).
    Figure 3. Mode of action of organic acids on pH-sensitive bacteria (ClostridiaSalmonellaColiformsListeria spp.) [36].
    This anion model of OAs can vary upon two factors: (1) the lipophilic nature of the OAs, which can transmit through the microbes cell wall; and (2) various anion complexes involved with different inhibitory actions within the cell [37][38].

    3. Effect of OAs in Swine and Broiler

    3.1. Supplementation of OAs on the Growth Performance of Swine and Broilers

    Studies have found that the optimal dosage of OAs can enhance the productivity of pigs compared to AGPs. Increased growth performance, gain to feed (G: F), and feed intake (FI) was observed in piglets supplemented with an OAs mixture (benzoic, fumaric, lactic, propionic, and citric) [39]. Because benzoic acid in the diet can increase the butyric acid concentration in the GIT, the gut microflora ameliorating process occurs by acting as an energy source agent in gut epithelial cells [40]. The feed conversion ratio (FCR) was increased by 10%, and the average daily gain (ADG) was increased by 3% when pigs were administered fumaric and citric acids at four weeks of age [41]. Kuang et al. [42] reported that the inclusion of an OAs blend (calcium formate, calcium lactate, and citric acid) and medium-chain fatty acids (MCFAs—lauric, capric, and myristic) enhanced the FI, ADG, and FCR in weaning pigs compared to pigs fed with dietary zinc oxide inclusion. Feeding weaning pigs with 0.8% fumaric acids reduced the E. coli and Coliforms population in the cecum [43]. On the other hand, Risley et al. [44] reported that 1.5 % fumaric acid addition did not affect the microflora composition in the GIT. According to the study conducted by Htto et al. [45], the ADG, FCR, and body weight (BW) during 0–14 days (piglets) were not significantly different from those fed OAs. In the same study, however, the ADG and FCR were enhanced during 15–35 days and, overall, 35 days of periods due to salts of organic acid (potassium diformate and potassium formate) supplementation. Furthermore, a trend of developed growth performance in response to the inclusion of OAs combined with salts combination was more reliable in growing-finishing pigs than in weaning pigs [6]. Canibe et al. [46] and Partanen et al. [47] reported increased ADG and G: F ratios in pigs fed a diet containing formic acid, ammonium formate, and formic acids. A combination of phytogenic feed additives with organic acids (10% citric, 10% sorbic, 6.5% malic, and 13.5% fumaric acid) also improved the BW and ADG of weaning pigs. Moreover, Yang et al. [48] reported that a high abundance of Limosilactobacillus mucosae also occurred compared to the control treatment. Nevertheless, 1.8% formic acid inclusion did not have a positive response on the ADG and average daily feed intake (ADFI) of weaning pigs, but it enhanced the G: F [46]. The above dissimilarities among the different studies might be related to the inclusion dosage of OAs, diet complexity, growth phase, and animals’ health conditions (Table 2). Therefore, further studies will be needed to identify the best OAs concentration for different growth stages.
    In the broiler growth performance, the utilization of OAs has not gained as much attention as in the swine industry. The rapid metabolization process in crops to the gizzard (foregut) causes a deficiency of OAs availability and retards the growth performance [33]. However, Fascina et al. [13] reported that the administration of OAs combination (30% lactic, 25.5% benzoic, 7% formic, 8% citric, and 6.5% acetic acid) improved the BW, weight gain (WG), and FCR compared to the control group at 42-day-old broilers. Broilers fed OAs-supplemented diets showed a significant (p < 0.05) improvement in the FCR due to better utilization of nutrients [49]. Hassan et al. [50] reported that microencapsulated galliacid OAs mixture (fumaric acid, calcium formate, calcium propionate, potassium sorbate, and hydrogenated vegetable oil) enhanced the WG by 16% compared to the control groups. Kamal and Ragaa [51] also indicated that in 42 days old broilers, the BWG and FCR were enhanced in those fed 3% organic acids (butyric, fumaric, and lactic acid). Hence, the higher BWG was achieved through direct antimicrobial effect, reducing the digesta pH level in the GIT while acting as a barrier to pathogens and buffering reactivity in conjunction with the enhanced nutrient digestibility [52]. Interestingly, the synergistic effects of combined 0.3 g/kg essential oils (thymol, vanillin, and eugenol) with encapsulated OAs (fumaric, sorbic, malic, and citric) increased the FCR significantly while minimizing the E. coli population through a lower gut pH value [53].
    Table 2. Effect of organic acids mixture on growth performances and other parameters of swine and broilers.
    Dosage and Organic Acid/Acids Growth Phase Growth Performances Intestinal/Fecal Microbial Counts (CFU) Other Parameters References
    BWG/FBW ADFI G:F
    Swine
    0.1% and 0.2% fumaric, citric, malic, MCFA (capric and caprylic) Weaning S NS S E. coli; S
    Lactobacilli; S
    Clostridium; S
    Salmonella; S
    • Reduced diarrhea score, fecal ammonia, and acetic acid emission
    Yang et al., 2018 [54]
    0.1% and 0.2% fumaric, citric, malic, MCFA (capric and acrylic) Growing S NS S Lactobacilli; S
    E. coli; NS
    - Upadhya et al., 2016 [55]
    0.15% benzoic, fumaric, calcium formate Weaning S NS NS E. coli; NS
    Lactobacilli; NS
    • Increased villus height in duodenum and jejunum
    • Increased butyric acid level in the cecum and valeric acid level in the colon
    Xu et al., 2017 [56]
    1.1% acetic, propionic, phosphoric, citric acid Weaning NS NS NS Lactobacilli; NS
    E. coli; NS
    Coliforms; NS
    • Reduced pH level in colon
    • Retardation of Coliforms proliferation
    Namkung et al., 2004 [57]
    0.4% and 0.2% fumaric, lactate, citric, propionic, benzoic acid Weaning NS NS NS E. coli; NS - Walsh et al., 2007 [39]
    0.5% benzoic acid Weaning S S S Lactobacilli; S - Wei et al., 2021 [58]
    0.5, 1% benzoic acid Weaning S NS NS NE
    • Reduced the number of aerobic, total anaerobic, lactic acid-forming, and gram-negative bacteria in the stomach
    • Reduced gram-negative bacteria and acetic acid in the duodenum
    • Reduced gram-negative bacteria in ileum
    Kluge et al., 2005 [59]
    0.5% butanoic, fumaric, benzoic acid Piglets S NS S Lactobacilli; NS
    E. coli; NS
    • Decreased ileal E. coli bacteria level
    • Did not exert negative impacts on GIT pH level and immunity
    Li et al., 2008 [60]
    0.1% fumaric, citric, malic, MCFA (capric and caprylic) Finishing S NS S Lactobacilli; NS
    E. coli; NS
    • Reduced feces H2S gas emission
    Upadhya et al., 2014 [61]
    0.85% formic, benzoic, sorbic, Ca- butyrate Growing male pigs NS NS NS E. coli; S
    Lactobacilli; S
    • Lower level of ColiformsEnterococci, and lactic acid bacteria in jejunum and colon descendens
    Øverland et al., 2007 [62]
    0.5% benzoic acid Weaning S S S E. coli; NS
    Lactobacilli; NS
    • Reduced diarrhea in weaning pigs
    Papatsiros et al., 2011 [63]
    0.14% and 0.64% formic acid Weaning S S NS Lactobacilli; S
    • Higher microbiota diversity in 0.64% dosage
    Luise et al., 2017 [9]
    Broilers
    0.3% and 0.4% calcium formate, calcium propionate
    0.3, 0.4% ammonium formate, ammonium propionate
    Finishing S NS S NE
    • Reduced the ileal total bacterial count
    • Improved villi length
    Saleem et al., 2020 [64]
    1% formic, lactic, propionic, citric acid Finishing S NS NS NE
    • Enhanced V: C in GIT
    • Increased water consumption during 15–22 days
    Ali et al., 2020 [65]
    0.5% citric, sorbic, synthetic essential oil Finishing NS NS NS E. coli; NS
    Enterococci; S
    Clostridium; NS
    Enterobacteriaceae; NS
    • Increased villi height, crypt depth, number of villi, mucosa thickness, and villi area
    Stamilla et al., 2020 [66]
    0.15% formic, lactic, citric, malic, tartaric, phosphoric acids Finishing S S S Lactobacilli; S
    E. coli; S
    • Enhanced inhibitory action owing to organic acid
    Goh et al., 2020 [67]
    0.3% formic, acetic, propionic, ammonium formate Finishing S NS NS NE
    • Increased SCFAs level in the cecum
    • Increased jejunal goblet cell density and ileal villus height
    Dai et al., 2021 [68]
    0.1% lactic, citric, acetic, formic, propionic, phosphoric, and sodium butyrate Finishing S NS S Lactobacilli; S
    Coliforms; NS
    • Increased jejunum villus height
    • Enhanced humoral immune response
    Sabour et al., 2018 [69]
    0.3, 0.5% formic, propionic acid Finishing S NS S Lactobacilli; S
    E. coli; S
    • Lower duodenal pH
    • High immune response against Newcastle disease, infectious bronchitis
    Fathi et al., 2016 [70]
    0.06% fumaric, calcium format, calcium propionate, potassium sorbate, hydrogenated vegetable oil Finishing S S S Lactobacilli; S
    Salmonella; S
    • Increased dressing percentage and bursa weight
    Hassan et al., 2010 [50]
    0.2, 0.4, and 0.6% butyric acid Finishing S NS S E. coli; S
    • pH reduction of upper GIT
    • Increased villus length and crypt depth in the duodenum
    Panda et al., 2009 [71]
    0.5, 1, 1.5, and 2% citric, lactic, phosphoric acid Finishing S NS S E. coli; S
    Salmonella; S
    • 2% OAs blend enhanced the carcass yield
    • 1.5%, 2% OAs blend increased the liver weight
    Sultan et al., 2015
    [72]
    0.6% formic acid Finishing S NS S E. coli; S (in crop)
    • Higher digestibility of crude protein, high dressed yield, and lower fat content in carcass
    Panda et al., 2009
    [73]
    2% butyric, fumaric, lactic, and 3% butyric, fumaric, lactic acid Finishing S NS S NE
    • Increased villus height in the small intestines
    • Enhanced serum calcium and phosphorus concentrations
    Adil et al., 2010 [25]
    0.2% propionic, 0.3% butyric acid Finishing S NE S NE
    • Increased tibia weight, tibia length
    Lakshmi and Sunder., 2015 [74]
    BWG, body weight gain; FBW, final body weight; ADFI, average daily feed intake; G: F, gain to feed ratio; S, significant; NS, non-significant; NE, not evaluated.

    3.2. Supplementation of OAs on Nutrient Digestibility of Swine and Broilers

    Generally, OAs have been utilized as an acidifier in the livestock feeding sector. Furthermore, OAs inclusion is considered to be an effective antibiotic alternative for enhancing nutrient digestibility. Microencapsulated OAs, including 10% malic, 13% citric, and 17% fumaric acids, enhanced the digestion of nitrogen (N), dry matter (DM), and energy in finishing pigs and lactating sows [61][75][76] and significantly increased DM, crude protein (CP), fat, and energy digestibility in growing pigs [77]. The supplementation of 1.5% citric acid increased the coefficient of the total tract digestibility (CTTAD) of crude protein (CP), calcium (Ca), and phosphorous (P) of sows during the late gestation and lactation period [78]. Moreover, Yang et al. [54] stated that protected OAs incorporation has positive effects on the apparent total tract digestibility (ATTD) of (DM) in weaning pigs. The inclusion of benzoic acid resulted in improved apparent digestibility of Ca and P in growing pigs [79][80]; CP digestibility in weaning pigs [81]; and the DM, CP, ether extract (EE), and crude fiber (CF) of sows [82]. Previous studies demonstrated positive influence of OAs supplementation on the nutrient digestibility in both swine and broilers (Table 3).
    Nevertheless, Upadhya et al. [55] found no significant differences in DM, N, and energy digestibility owing to dietary supplementation of OAs in three different concentration levels.
    Since OAs were used as an alternative feed additive, they helped improve the growth performance and productivity parameters in broilers. The addition of 0.5% and 1% formic acid into the finisher diet enhanced apparent ileal digestibility (AID) of DM and CP compared to the control treatment [83][84]. Ao et al. [85] reported that 2% citric acid incorporation improved the retention of DM, CP, and neutral detergent fiber content in the GIT. In one study, the gross energy, CP, and EE digestibility of broilers at nine days of age was found to be 78.01, 76.07, and 72.85% in the 200ppm ascorbic acid-supplemented group, which was significantly higher as compared with 76.20, 72.62, and 67.65% in the non-supplemented group, respectively [86]. The supplementation of 0.2% OAs with a phytase combination more significantly enhanced the CP (88.58%) and EE (85.61) digestibility in chicks than the CP (77.51) and EE (79.49) values in the control treatment [87].
    Smulikowska et al. [88] reported that fat-coated OAs inclusion improved the N retention, organic matter (OM), and metabolizable energy corrected for nitrogen (AMEn) values. The reason for the higher N retention might have been the improved epithelial cell proliferation in the GIT, while non-protected OAs tended to be metabolized rapidly [89]. Owing to the synergistic effect, combined OAs and essential oil (EO) administration into the broiler diet enhanced the AID of DM and energy at 21 days of rearing [90]. Nevertheless, the expected synergism effect was not observed from the combination of citric acid with microbial phytase. The non-significant impact on the AID of CP and amino acids (AA) might be associated with the formation of complexes among citric acids with Ca and the subsequent decrease in binding ability with phytate allowing easy hydrolyzation by the enzymes.
    Table 3. Effect of organic acids combination on nutrient digestibility of swine and broilers.
    Dosage and Organic Acid/Acids Growth Phase Digestibility Reference
    DM N E CP
    Swine
    0.2% fumaric, citric, malic, capric, and caprylic acid Growing S S S S Hossain et al., 2011 [77]
    0.05% citric, sorbic acid Growing S NS S NC Cho et al., 2014 [91]
    2% benzoic acid Lactating sows S (OM) NE NE S Kluge et al., 2010 [82]
    0.1% and 0.2% fumaric, citric, MCFA Finishing S S S NE Upadhaya et al., 2014 [75]
    0.5% phenyllactic acid Weaning S S NE NE Wang et al., 2009 [92]
    0.3% formic, acetic, propionic, MCFA Weaning S (DM)
    NS (OM)
    NS NS NS Long et al., 2018 [93]
    0.5% formic, propionic, lactic, citric, sorbic acid Post-weaning NS NS NS NS Gerritsen et al., 2010 [94]
    300 mEq acid/kg formic, n-butyric acid Growing S S S S Mroz et al., 2000 [95]
    0.15% citric acid Lactating sows NE NE NE S Liu et al., 2014a [78]
    0.2% fumaric, citric, malic, capric, caprylic acid Lactating sows S S S NE Devi et al., 2016 [96]
    Broilers
    0.2% formic, propionic acid Finishing NS NE NE S Emami et al., 2013 [87]
    0.5% formic acid Finishing NS NE NE NS Hernández et al., 2006 [84]
    0.25, 0.5, and 0.75% formic acid Finishing NS NE NE S Ndelekwute et al., 2015 [97]
    5000ppm and 10,000ppm formic acid Finishing S NE NE S Garcia et al., 2007 [84]
    0.25% acetic, butyric, citric, formic acid Finishing S NE NS S Ndelekwute et al., 2019 [98]
    1, 2, and 3% citric acid Finishing NE NE S S Ghazalah et al., 2011 [52]
    0.5, 1, and 1.5% fumaric acid Finishing NE NE S S Ghazalah et al., 2011 [52]
    0.25, 0.5% formic acid Finishing NE NE NS S Ghazalah et al., 2011 [52]
    0.25, 0.5, and 0.75% acetic acid Finishing NE NE S NS Ghazalah et al., 2011 [52]
    N, nitrogen; E, energy; CP, crude protein; S, significant; NS, non-significant; NE, not-evaluated; OM, organic matter; DM, dry matter.

    3.3. Effect of OAs Supplementation on Meat Quality on Pigs and Broilers

    Few studies have investigated the meat quality parameters based on the incorporation of OAs in animal diets. Moreover, an examination of the meat quality traits of pigs and broilers is important because the consumption of quality meat has gained an important place in the food industry. Upadhya et al. [75] reported that supplementation of an OAs blend (consisting of fumaric, citric, malic, and MCFA) did not have adverse effects or improvements in the meat color, pH, cooking loss, drip loss, and water holding capacity (WHC). Similarly, Cho et al. [91] reported that the administration of a microencapsulated OAs combination, including citric and sorbic acids, did not significantly affect the meat color, pH, sensory attributes (color, firmness, marbling), cooking loss, and WHC. In contrast, the inclusion of 0.05 and 0.1% fumaric, citric, malic, and MCFAs resulted in lower drip loss in pork (22.05%) except for any differences in meat color, sensory evaluation, cooking loss, pH, and WHC [99]. Jansons et al. [100] reported a higher protein content (21.94%) in longissimus lumborum muscle tissues and lower cholesterol content (51.1 mg/kg−1) in pork after the addition of formic, acetic, citric, phosphoric acid along with phytogenic feed additives to the diet. This might be attributed to the synergistic effect and the presence of antioxidant compounds in the feed. However, further investigations will be needed to determine the possible mode of actions associated with the meat quality characteristics by introducing OAs to the animal diet.
    Brzóska et al. [101] reported that the supplementation of OAs to a broiler diet resulted in no significant influence on breast muscle content and leg muscle weight. The chemical constitutes of the leg meat, including DM, protein, and fat content, also did not vary due to OAs application. Nevertheless, Jha et al. [102] reported that the inclusion of OAs (formic + propionic acid, formic + citric acid, formic + sorbic, and formic+ lactic acid) enhanced the meat thigh weight (29.03%), back weight (53.4%), wings weight (31.27%), and breast weight (34.57%) compared to the control group. On the other hand, they did not evaluate any other meat quality parameters regarding OAs inclusion. Supplementation at the recommended dosage of an acetic, butyric, formic, phosphoric, lactic acid blend did not have significantly favorable results on carcass pH, shear force, WHC, cooking loss, and meat color values, but the TBARS value was increased significantly in birds fed with an OAs mixed diet (2.01 nmol MDA/mg) as compared with control group (1.10 nomol MDA/mg). This suggests that a higher fat content facilitated a higher lipid oxidation process in meat [103]. Meat pH has a significant influence on WHC, meat color, juiciness, tenderness, and shelf-life. The changes of meat pH result from post-mortem metabolism and the conversion of glycogen into lactic acid [104]. In contrast, at a lower pH range (pH < 5.8), broiler meat exhibited a pale, soft, and exudative (PSE) condition, which is considered a degraded meat quality parameter compared to meat exposed to higher pH levels (pH > 5.8) [105]. Sugiharto et al. [106] found that a higher meat pH (6.7%) in broilers occurred in a diet administered with 0.1% formic and 0.3% butyric acid compared to the control group. El-Senousey et al. [107] presented a possible reason for the OAs and higher meat pH occurrence: the decline in post-mortem muscle glycolysis inhibited the decrease in muscle pH after slaughter. Furthermore, lower drip loss and a lightness value were reported in the diet combined with both formic and butyric acid but decreased due to the single administration of butyric acid. This might be due to the distinctive characteristics of each OA and the metabolic activities of each associated with specific pKa. Menconi et al. [108] reported less drip loss (65.85%) in broiler meat with feeding blends of lactic, tannic, caprylic, propionic, acetic acids, and butyric acid. Nevertheless, inconsistent results were obtained by Attia et al. [109], who reported a decrease in WHC (26.45%) in broiler meat owing to the supplementation of citric and fumaric acids. These results were attributed to differences in the OAs type, dosage, and experimental environment.
    Nutritional quality of meat can also be influenced by the feeding strategies. Akbar et al. [110] observed a significantly higher PUFA content and lower SFA proportion of the birds fed a diet supplemented with organic acid salts (1% calcium propionate), which is beneficial, from the human nutrition point of view, as lower saturated fatty acid (SFA) and higher (PUFA) may positively influence human health. Furthermore, a lower cholesterol content was also reported in the diet containing dietary OAs.

    The entry is from 10.3390/life11060476

    References

    1. Nguyen, D.H.; Kim, I.H. Protected Organic Acids Improved Growth Performance, Nutrient Digestibility, and Decreased Gas Emission in Broilers. Animals 2020, 10, 416.
    2. Tugnoli, B.; Giovagnoni, G.; Piva, A.; Grilli, E. From Acidifiers to Intestinal Health Enhancers: How Organic Acids Can Improve Growth Efficiency of Pigs. Animals 2020, 10, 134.
    3. Shahidi, S.; Yahyavi, M.; Zare, D.N. Influence of Dietary Organic Acids Supplementation on Reproductive Performance of Freshwater Angelfish (Pterophyllum Scalare). Global Vet. 2014, 13, 373–377.
    4. Kim, Y.Y.; Kil, D.Y.; Oh, H.K.; Han, I.K. Acidifier as an Alternative Material to Antibiotics in Animal Feed. Asian Australas. J. Anim. Sci. 2005, 18, 1048–1060.
    5. Kil, D.Y.; Piao, L.G.; Long, H.F.; Lim, J.S.; Yun, M.S.; Kong, C.S.; Ju, W.S.; Lee, H.B.; Kim, Y.Y. Effects of Organic or Inorganic Acid Supplementation on Growth Performance, Nutrient Digestibility and White Blood Cell Counts in Weanling Pigs. Asian Australas. J. Anim. Sci. 2005, 19, 252–261.
    6. Mroz, Z.; Reese, D.E.; Øverland, M.; Van Diepen, J.T.M.; Kogut, J. The effects of potassium diformate and its molecular constituents on the apparent ileal and fecal digestibility and retention of nutrients in growing-finishing pigs. J. Anim. Sci. 2002, 80, 681–690.
    7. Partanen, K.H.; Mroz, Z. Organic acids for performance enhancement in pig diets. Nutr. Res. Rev. 1999, 12, 117–145.
    8. Spratt, C.D. Effect of Mould Inhibitor Treated High Moisture Corn on Performance of Poultry. Master’s Thesis, University of Guelph, Guelph, ON, Canada, 1985.
    9. Luise, D.; Motta, V.; Salvarani, C.; Chiappelli, M.; Fusco, L.; Bertocchi, M.; Mazzoni, M.; Maiorano, G.; Costa, L.N.; Van Milgen, J.; et al. Long-term administration of formic acid to weaners: Influence on intestinal microbiota, immunity parameters and growth performance. Anim. Feed. Sci. Technol. 2017, 232, 160–168.
    10. Ndelekwute, E.K.; Assam, E.D.; Ekere, P.C.; Ufot, U.E. Effect of organic acid treated diets on growth, apparent nutrient digestibility and faecal moisture of broiler chickens. Niger. J. Anim. Prod. 2016, 43, 218–223.
    11. Huang, C.; Song, P.; Fan, P.; Hou, C.; Thacker, P.; Ma, X. Dietary Sodium Butyrate Decreases Postweaning Diarrhea by Modulating Intestinal Permeability and Changing the Bacterial Communities in Weaned Piglets. J. Nutr. 2015, 145, 2774–2780.
    12. Yang, X.; Xin, H.; Yang, C.; Yang, X. Impact of essential oils and organic acids on the growth performance, digestive functions and immunity of broiler chickens. Anim. Nutr. 2018, 4, 388–393.
    13. Fascina, V.B.; Sartori, J.R.; Gonzales, E.; De Carvalho, F.B.; De Souza, I.M.G.P.; Polycarpo, G.D.V.; Stradiotti, A.C.; Pelícia, V.C. Phytogenic additives and organic acids in broiler chicken diets. Rev. Bras. Zootec. 2012, 41, 2189–2197.
    14. Tsiloyiannis, V.K.; Kyriakis, S.C.; Vlemmas, J.; Sarris, K. The effect of organic acids on the control of porcine post-weaning diarrhea. Res. Vet. Sci. 2001, 70, 287–293.
    15. Dittoe, D.K.; Ricke, S.C.; Kiess, A.S. Organic Acids and Potential for Modifying the Avian Gastrointestinal Tract and Reducing Pathogens and Disease. Front. Vet. Sci. 2018, 5, 216.
    16. Pearlin, B.V.; Muthuvel, S.; Govidasamy, P.; Villavan, M.; Alagawany, M.; Farag, M.R.; Dhama, K.; Gopi, M. Role of acidifiers in livestock nutrition and health: A review. J. Anim. Physiol. Anim. Nutr. 2020, 104, 558–569.
    17. Ravindran, V.; Kornegay, E.T. Acidification of weaner pig diets: A review. J. Sci. Food Agric. 1993, 62, 313–322.
    18. Nguyen, D.H.; Seok, W.J.; Kim, I.H. Organic Acids Mixture as a Dietary Additive for Pigs—A Review. Animals 2020, 10, 952.
    19. De Lange, C.; Pluske, J.; Gong, J.; Nyachoti, C. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest. Sci. 2010, 134, 124–134.
    20. Jongbloed, A.; Mroz, Z.; van der Weij-Jongbloed, R.; Kemme, P. The effects of microbial phytase, organic acids and their interaction in diets for growing pigs. Livest. Prod. Sci. 2000, 67, 113–122.
    21. Boling, S.D.; Webel, D.M.; Mavromichalis, I.; Parsons, C.M.; Baker, D.H. The effects of citric acid on phytate-phosphorus utilization in young chicks and pigs. J. Anim. Sci. 2000, 78, 682–689.
    22. Kirchegessner, M.; Roth, F.X. Fumaric acid as a fed additive in pig nutrition. Pig News Inf. 1982, 3, 259.
    23. Ao, T. Exogenous Enzymes and Organic Acids in the Nutrition of Broiler Chicks: Effects on Growth Performance and In Vitro and In Vivo Digestion. Ph.D. Thesis, University of Kentucky, Lexington, KY, USA, 2005.
    24. Afsharmanesh, M.; Pourreza, J. Effects of calcium, citric acid, ascorbic acid, vitamin D3 on the efficacy of mi-crobial phytase in broiler starters fed wheat-based diets I. Performance, bone mineralization and ileal digestibility. Int. J. Poult. Sci. 2005, 4, 418–424.
    25. Adil, S.; Banday, T.; Bhat, G.A.; Mir, M.S.; Rehman, M. Effect of Dietary Supplementation of Organic Acids on Performance, Intestinal Histomorphology, and Serum Biochemistry of Broiler Chicken. Vet. Med. Int. 2010, 2010, 479485.
    26. Van Der Sluis, W. Water quality is important but often overestimated. World Poult. 2002, 18, 26–32.
    27. Omogbenigun, F.O.; Nyachoti, C.M.; Slominski, B.A. The effect of supplementing microbial phytase and organic acids to a corn-soybean based diet fed to early-weaned pigs. J. Anim. Sci. 2003, 81, 1806–1813.
    28. Skřivanová, E.; Marounek, M.; Benda, V.; Březina, P. Susceptibility of Escherichia coli, Salmonella sp and Clostridium perfringens to organic acids and monolaurin. Vet. Med. Praha 2006, 51, 81–88.
    29. Biagi, G.; Piva, A.; Hill, T.; Schneider, D.K.; Crenshaw, T.D. Low buffering capacity diets with added organic acids as substitute for antibiotics in diets for weaned pigs. In Proceedings of the 9th International Symposium on Digestive Physiology in Pigs, Banff, AB, Canada, 14–18 May 2003; Ball, R., Ed.; University of Alberta: Banff, AB, Canada, 2003; pp. 217–219.
    30. Pinheiro, V.; Mourao, J.L.; Alves, A.; Rodrigues, M.; Saavedra, M.J. Effect of Zinc bacitracin on the performance, digestibility and caecal development of growing rabbits. In Proceedings of the 8th World Rabbit Congress, Puebla, Mexico, 7–10 September 2004; pp. 942–947.
    31. Mroz, Z.; Koopmans, S.J.; Bannink, A.; Partanen, K.; Krasucki, W.; Overland, M.; Radcliffe, S. Carboxylic acids as bio regulators and gut growth promoters in non-ruminants. In Biology of Nutrition in Growing Animals; Mosenthin, R., Zentek, J., Zebrowska, T., Eds.; Elsevier: Edinburgh, UK, 2006; Volume 3, pp. 81–133.
    32. Stratford, M.; Eklund, T. Organic acids and esters. In Food Preservatives; Springer: Boston, MA, USA, 2003; pp. 48–84.
    33. Suiryanrayna, M.V.A.N.; Ramana, J.V. A review of the effects of dietary organic acids fed to swine. J. Anim. Sci. Biotechnol. 2015, 6, 45.
    34. Dibner, J.; Buttin, P. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J. Appl. Poult. Sci. 2002, 11, 453–463.
    35. Luckstadt, C.; Mellor, S. The use of organic acids in animal nutrition, with special focus on dietary potassium diformate under European and Austral-Asian conditions. Recent Adv. Anim. Nutr. Aust. 2011, 18, 123–130.
    36. Gauthier, R. Intestinal health, the key to productivity: The case of organic acids. In Proceedings of the XXVII Convention ANECA-WPDC, Puerto Vallarta, Mexico, 3–6 April 2002.
    37. Hirshfield, I.N.; Terzulli, S.; O’Byrne, C. Weak Organic Acids: A Panoply of Effects on Bacteria. Sci. Prog. 2003, 86, 245–270.
    38. Ng, W.-K.; Koh, C.-B. The utilization and mode of action of organic acids in the feeds of cultured aquatic animals. Rev. Aquac. 2016, 9, 342–368.
    39. Walsh, M.C.; Sholly, D.M.; Hinson, R.B.; Saddoris, K.L.; Sutton, A.L.; Radcliffe, J.S.; Odgaard, R.; Murphy, J.; Richert, B.T. Effects of water and diet acidification with and without antibiotics on weanling pig growth and microbial shedding. J. Anim. Sci. 2007, 85, 1799–1808.
    40. Kathrin, B. Benzoic Acid as Feed Additive in Pig Nutrition: Effects of Diet Composition on Performance, Digestion and Ecological Aspects. Ph.D. Thesis, ETH, Zurich, Switzerland, 2009.
    41. Falkowski, J.F.; Aherne, F.X. Fumaric and Citric Acid as Feed Additives in Starter Pig Nutrition. J. Anim. Sci. 1984, 58, 935–938.
    42. Kuang, Y.; Wang, Y.; Zhang, Y.; Song, Y.; Zhang, X.; Lin, Y.; Che, L.; Xu, S.; Wu, D.; Xue, B.; et al. Effects of dietary combinations of organic acids and medium chain fatty acids as a replacement of zinc oxide on growth, digestibility and immunity of weaned pigs. Anim. Feed Sci. Technol. 2015, 208, 145–157.
    43. Grecco, H.A.; Amorim, A.B.; Saleh, M.A.; Tse, M.L.; Telles, F.G.; Miassi, G.M.; Pimenta, G.M.; Berto, D.A. Evaluation of growth performance and gastro-intestinal parameters on the response of weaned piglets to dietary organic acids. An. Acad. Bras. Ciênc. 2018, 90, 401–414.
    44. Risley, C.R.; Kornegay, E.T.; Lindemann, M.D.; Wood, C.M.; Eigel, W.N. Effect of feeding organic acids on selected intestinal content measurements at varying times post weaning in pigs. J. Anim. Sci. 1992, 70, 196–206.
    45. Htoo, J.; Molares, J. Effects of dietary supplementation with two potassium formate sources on performance of 8- to 22-kg pigs. J. Anim. Sci. 2012, 90, 346–349.
    46. Canibe, N.; Højberg, O.; Højsgaard, S.; Jensen, B.B. Feed physical form and formic acid addition to the feed affect the gastrointestinal ecology and growth performance of growing pigs. J. Anim. Sci. 2005, 83, 1287–1302.
    47. Partanen, K.; Siljander-Rasi, H.; Alaviuhkola, T.; Suomi, K.; Fossi, M. Performance of growing-finishing pigs fed mediumor high-fibre diets supplemented with avilamycin, formic acid or formic acid-sorbate blend. Livest. Prod. Sci. 2002, 73, 139–152.
    48. Yang, C.; Zhang, L.; Cao, G.; Feng, J.; Yue, M.; Xu, Y.; Dai, B.; Han, Q.; Guo, X. Effects of dietary supplementation with essential oils and organic acids on the growth performance, immune system, fecal volatile fatty acids, and microflora community in weaned piglets. J. Anim. Sci. 2019, 97, 133–143.
    49. Adil, S.; Banday, T.; Bhat, G.A.; Salahuddin, M.; Raquib, M.; Shanaz, S. Response of Broiler Chicken to Dietary Supplementation of Organic Acids. J. Cent. Eur. Agric. 2011, 12, 498–508.
    50. Hassan, H.M.A.; Mohamed, M.A.; Youssef, A.W.; Hassan, E.R. Effect of using organic acids to substitute antibiotic growth promoters on performance and intestinal microflora of broilers. Asian Australas. J. Anim. Sci. 2010, 23, 1348–1353.
    51. Kamal, A.M.; Ragaa, N.M. Effect of dietary supplementation of organic acids on performance and serum biochemistry of broiler chicken. Nat. Sci. 2014, 12, 38–45.
    52. Ghazala, A.A.; Atta, A.M.; Elkloub, K.; Mustafa, M.E.L.; Shata, R.F.H. Effect of dietary supplementation of organic acids on performance, nutrients digestibility and health of broiler chicks. Int. J. Poult. Sci. 2011, 10, 176–184.
    53. Yang, X.; Liu, Y.; Yan, F.; Yang, C.; Yang, X. Effects of encapsulated organic acids and essential oils on intestinal barrier, microbial count, and bacterial metabolites in broiler chickens. Poult. Sci. 2019, 98, 2858–2865.
    54. Yang, Y.; Lee, K.Y.; Kim, I. Effects of dietary protected organic acids on growth performance, nutrient digestibility, fecal microflora, diarrhea score, and fecal gas emission in weanling pigs. Can. J. Anim. Sci. 2019, 99, 514–520.
    55. Upadhaya, S.D.; Lee, K.Y.; Kim, I.H. Effect of protected organic acid blends on growth performance, nutrient digestibility and faecal micro flora in growing pigs. J. Appl. Anim. Res. 2016, 44, 238–242.
    56. Xu, Y.; Liu, L.; Long, S.; Pan, L.; Piao, X. Effect of organic acids and essential oils on performance, intestinal health and digestive enzyme activities of weaned pigs. Anim. Feed. Sci. Technol. 2018, 235, 110–119.
    57. Namkung, H.; Gong, M.L.J.; Yu, H.; Cottrill, M.; De Lange, C.F.M. Impact of feeding blends of organic acids and herbal extracts on growth performance, gut microbiota and digestive function in newly weaned pigs. Can. J. Anim. Sci. 2004, 84, 697–704.
    58. Wei, X.; Bottoms, K.; Stein, H.; Blavi, L.; Bradley, C.; Bergstrom, J.; Knapp, J.; Story, R.; Maxwell, C.; Tsai, T.; et al. Dietary Organic Acids Modulate Gut Microbiota and Improve Growth Performance of Nursery Pigs. Microorganisms 2021, 9, 110.
    59. Kluge, H.; Broz, J.; Eder, K. Effect of benzoic acid on growth performance, nutrient digestibility, nitrogen balance, gastrointestinal microflora and parameters of microbial metabolism in piglets. J. Anim. Physiol. Anim. Nutr. 2006, 90, 316–324.
    60. Li, Z.; Yi, G.; Yin, J.; Sun, P.; Li, D.; Knight, C. Effects of Organic Acids on Growth Performance, Gastrointestinal pH, Intestinal Microbial Populations and Immune Responses of Weaned Pigs. Asian Australas. J. Anim. Sci. 2008, 21, 252–261.
    61. Upadhaya, S.; Lee, K.; Kim, I. Influence of protected organic acid blends and diets with different nutrient densities on growth performance, nutrient digestibility and faecal noxious gas emission in growing pigs. Vet. Med. 2014, 59, 491–497.
    62. Øverland, M.; Kjos, N.; Borg, M.; Skjerve, E.; Sørum, H. Organic acids in diets for entire male pigs: Effect on skatole level, microbiota in digesta, and growth performance. Livest. Sci. 2008, 115, 169–178.
    63. Papatsiros, V.G.; Tassis, P.D.; Tzika, E.D.; Papaioannou, D.S.; Petridou, E.; Alexopoulos, C.; Kyriakis, S.C. Effect of benzoic acid and combination of benzoic acid with a probiotic containing Bacillus Cereus var. toyoi in weaned pig nutrition. Pol. J. Vet. Sci. 2011, 14, 117–125.
    64. Saleem, K.; Saima; Rahman, A.; Pasha, T.N.; Mahmud, A.; Hayat, Z. Effects of dietary organic acids on performance, cecal microbiota, and gut morphology in broilers. Trop. Anim. Health Prod. 2020, 52, 3589–3596.
    65. Ali, A.M.; El Agrab, H.M.; Hamoud, M.M.; Gamal, A.M.; Mousa, M.R.; Nasr, S.A.E.; El Shater, M.A.H.; Laban, S.E.; Zahran, O.K.; Ali, M.M. Effect of Acidified Drinking Water by Organic Acids on Broiler Performance and Gut Health. Adv. Anim. Vet. Sci. 2020, 8.
    66. Stamilla, A.; Messina, A.; Sallemi, S.; Condorelli, L.; Antoci, F.; Puleio, R.; Loria, G.R.; Cascone, G.; Lanza, M. Effects of Microencapsulated Blends of Organics Acids (OA) and Essential Oils (EO) as a Feed Additive for Broiler Chicken. A Focus on Growth Performance, Gut Morphology and Microbiology. Animals 2020, 10, 442.
    67. Goh, C.H.; Loh, T.C.; Foo, H.L.; Nobilly, F. Fecal Microbial Population and Growth in Broiler Fed Organic Acids and Palm Fat-Composed Diet. Trop. Anim. Sci. J. 2020, 43, 151–157.
    68. Dai, D.; Qiu, K.; Zhang, H.-J.; Wu, S.-G.; Han, Y.-M.; Wu, Y.-Y.; Qi, G.-H.; Wang, J. Organic Acids as Alternatives for Antibiotic Growth Promoters Alter the Intestinal Structure and Microbiota and Improve the Growth Performance in Broilers. Front. Microbiol. 2021, 11, 618144.
    69. Sabour, S.; Tabeidian, S.A.; Sadeghi, G. Dietary organic acid and fiber sources affect performance, intestinal morphology, immune responses and gut microflora in broilers. Anim. Nutr. 2019, 5, 156–162.
    70. Fathi, R.; Samadi, M.S.; Qotbi, A.A.; Seidavi, A.; Marín, A.L.M. Effects of feed supplementation with increasing levels of organic acids on growth performance, carcass traits, gut microbiota and pH, plasma metabolites, and immune response of broilers. Anim. Sci. Pap. Rep. 2016, 34, 195–206.
    71. Panda, A.K.; Rao, S.V.R.; Raju, M.V.L.N.; Sunder, G.S. Effect of Butyric Acid on Performance, Gastrointestinal Tract Health and Carcass Characteristics in Broiler Chickens. Asian Australas. J. Anim. Sci. 2009, 22, 1026–1031.
    72. Sultan, A.; Ullah, T.; Khan, S.; Khan, R.U. Effect of organic acid supplementation on the performance and ileal microflora of broiler during finishing period. Pak. J. Zool. 2015, 47, 32–38.
    73. Panda, A.K.; Raju, M.V.L.N.; Rao, S.R.; Sunder, G.S.; Reddy, M.R. Effect of graded levels of formic acid on gut microflora count, serum biochemical parameters, performance and carcass yield of broiler chickens. Indian J. Anim. Sci. 2009, 79, 1165–1168.
    74. Lakshmi, K.V.; Sunder, G.S. Supplementation of Propionic Acid (PA), Butyric Acid (BA) or Antibiotic (AB) in diets and their influence on broiler performance, carcass parameters and immune response. IJSR 2015, 4, 1002–1006.
    75. Upadhaya, S.D.; Lee, K.Y.; Kim, I.H. Protected Organic Acid Blends as an Alternative to Antibiotics in Finishing Pigs. Asian Australas. J. Anim. Sci. 2014, 27, 1600–1607.
    76. Rosiński, S.; Grigorescu, G.; Lewinska, D.; Ritzén, L.G.; Viernstein, H.; Teunou, E.; Poncelet, D.; Zhang, Z.; Fan, X.; Serp, D.; et al. Characterization of microcapsules: Recommended methods based on round-robin testing. J. Microencapsul. 2002, 19, 641–659.
    77. Hossain, M.; Jayaraman, B.; Kim, S.; Lee, K.; Kim, I.; Nyachoti, C. Effects of a matrix-coated organic acids and medium-chain fatty acids blend on performance, and in vitro fecal noxious gas emissions in growing pigs fed in-feed antibiotic-free diets. Can. J. Anim. Sci. 2018, 98, 433–442.
    78. Liu, S.; Hou, W.; Cheng, S.; Shi, B.; Shan, A. Effects of dietary citric acid on performance, digestibility of calcium and phosphorus, milk composition and immunoglobulin in sows during late gestation and lactation. Anim. Feed. Sci. Technol. 2014, 191, 67–75.
    79. Sauer, W.; Cervantes, M.; Yanez, J.; Araiza, B.; Murdoch, G.; Morales, A.; Zijlstra, R.T. Effect of dietary inclusion of benzoic acid on mineral balance in growing pigs. Livest. Sci. 2009, 122, 162–168.
    80. Bühler, K.; Liesegang, A.; Bucher, B.; Wenk, C.; Broz, J. Influence of benzoic acid and phytase in low-phosphorus diets on bone characteristics in growing-finishing pigs. J. Anim. Sci. 2010, 88, 3363–3371.
    81. Guggenbuhl, P.; Séon, A.; Quintana, A.P.; Nunes, C.S. Effects of dietary supplementation with benzoic acid (VevoVitall®) on the zootechnical performance, the gastrointestinal microflora and the ileal digestibility of the young pig. Livest. Sci. 2007, 108, 218–221.
    82. Kluge, H.; Broz, J.; Eder, K. Effects of dietary benzoic acid on urinary pH and nutrient digestibility in lactating sows. Livest. Sci. 2010, 134, 119–121.
    83. Hernandez, F.; García, V.; Madrid, J.; Orengo, J.; Catalá, P.; Megías, M.D. Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. Br. Poult. Sci. 2006, 47, 50–56.
    84. García, V.; Catalá-Gregori, P.; Hernandez, F.; Megías, M.D.; Madrid, J. Effect of Formic Acid and Plant Extracts on Growth, Nutrient Digestibility, Intestine Mucosa Morphology, and Meat Yield of Broilers. J. Appl. Poult. Res. 2007, 16, 555–562.
    85. Ao, T.; Cantor, A.H.; Pescatore, A.J.; Ford, M.J.; Pierce, J.L.; Dawson, K.A. Effect of enzyme supplementation and acidification of diets on nutrient digestibility and growth performance of broiler chicks. Poult. Sci. 2009, 88, 111–117.
    86. Lohakare, J.D.; Ryu, M.H.; Hahn, T.-W.; Lee, J.K.; Chae, B.J. Effects of Supplemental Ascorbic Acid on the Performance and Immunity of Commercial Broilers. J. Appl. Poult. Res. 2005, 14, 10–19.
    87. Emami, N.K.; Naeini, S.Z.; Ruiz-Feria, C. Growth performance, digestibility, immune response and intestinal morphology of male broilers fed phosphorus deficient diets supplemented with microbial phytase and organic acids. Livest. Sci. 2013, 157, 506–513.
    88. Smulikowska, S.; Czerwiński, J.; Mieczkowska, A.; Jankowiak, J. The effect of fat-coated organic acid salts and a feed enzyme on growth performance, nutrient utilization, microflora activity, and morphology of the small intestine in broiler chickens. J. Anim. Feed. Sci. 2009, 18, 478–489.
    89. Stefanello, C.; Rosa, D.P.; Dalmoro, Y.K.; Segatto, A.L.; Vieira, M.S.; Moraes, M.L.; Santin, E. Protected Blend of Organic Acids and Essential Oils Improves Growth Performance, Nutrient Digestibility, and Intestinal Health of Broiler Chickens Undergoing an Intestinal Challenge. Front. Vet. Sci. 2020, 6, 491.
    90. Centeno, C.; Arija, I.; Viveros, A.; Brenes, A. Effects of citric acid and microbial phytase on amino acid digestibility in broiler chickens. Br. Poult. Sci. 2007, 48, 469–479.
    91. Cho, J.H.; Song, M.H.; Kim, I.H. Effect of microencapsulated blends of organic acids and essential oils supplementation on growth performance and nutrient digestibility in finishing pigs. Rev. Colomb. Cienc. Pecu. 2014, 27, 264–272.
    92. Wang, J.P.; Yoo, J.S.; Lee, J.H.; Jang, H.D.; Kim, H.J.; Shin, S.O.; Seong, S.I. Effects of phenyllactic acid on growth performance, nutrient digestibility, microbial shedding, and blood profile in pigs. J. Anim. Sci. 2009, 87, 3235–3243.
    93. Long, S.; Xu, Y.; Pan, L.; Wang, Q.; Wang, C.; Wu, J.; Wu, Y.; Han, Y.; Yun, C.; Piao, X. Mixed organic acids as antibiotic substitutes improve performance, serum immunity, intestinal morphology and microbiota for weaned piglets. Anim. Feed. Sci. Technol. 2018, 235, 23–32.
    94. Gerritsen, R.; van Dijk, A.; Rethy, K.; Bikker, P. The effect of blends of organic acids on apparent faecal digestibility in piglets. Livest. Sci. 2010, 134, 246–248.
    95. Mroz, Z.; Jongbloed, A.W.; Partanen, K.H.; Vreman, K.; Kemme, P.A.; Kogut, J. The effects of calcium benzoate in diets with or without organic acids on dietary buffering capacity, apparent digestibility, retention of nutrients, and manure characteristics in swine. J. Anim. Sci. 2000, 78, 2622–2632.
    96. Devi, S.M.; Lee, K.Y.; Kim, I.H. Analysis of the effect of dietary protected organic acid blend on lactating sows and their piglets. Rev. Bras. Zootec. 2016, 45, 39–47.
    97. Ndelekwute, E.; Afolabi, K.; Uzegbu, H.; Essien, E. Effect of dietary formic acid as replacement of streptomycin on growth and nutrient digestibility in broiler. Bangladesh J. Anim. Sci. 2015, 44, 69–74.
    98. Ndelekwute, E.K.; Unah, U.L.; Udoh, U.H. Effect of dietary organic acids on nutrient digestibility, faecal moisture, digesta pH and viscosity of broiler chickens. MOJ Anat. Physiol. 2019, 6, 40–43.
    99. Lei, X.J.; Lee, S.I.; Lee, K.Y.; Nguyen, D.H.; Kim, I.H. Effects of a blend of organic acids and medium-chain fatty acids with and without Enterococcus faecium on growth performance, nutrient digestibility, blood parameters, and meat quality in finishing pigs. Can. J. Anim. Sci. 2018, 98, 852–859.
    100. Jansons, I.; Jemeljanovs, A.; Konosonoka, I.H.; Sterna, V.; Lujane, B. The influence of organic acid additive, phytoadditive and complex of organic acid additive phytoadditive on pig productivity, meat quality. Agron. Res. 2011, 9, 389–394.
    101. Brzóska, F.; Sliwiński, B.; Michalik-Rutkowska, O. Effect of Dietary Acidifier on Growth, Mortality, Post-Slaughter Parameters and Meat Composition of Broiler Chickens/Wpływ zakwaszacza diety na masę ciała, śmiertelność, wydajność rzeźną i skład mięsa kurcząt rzeźnych. Ann. Anim. Sci. 2013, 13, 85–96.
    102. Jha, A.K.; Azad, H.; Ali, S.N.; Alam, P.; Sheikh, N.; Ali, H.; Ansari, K. Evaluation of Growth and Carcass Characteristics of Broiler Chickens (Cobb 500) Feed on Different Level of Organic Acids Inclusion in Diet at Parwanipur. Nepal. Vet. J. 2019, 36, 137–147.
    103. Galli, G.M.; Aniecevski, E.; Petrolli, T.G.; da Rosa, G.; Boiago, M.M.; Simões, C.A.; Wagner, R.; Copetti, P.M.; Morsch, V.M.; Araujo, D.N.; et al. Growth performance and meat quality of broilers fed with microencapsulated organic acids. Anim. Feed. Sci. Technol. 2021, 271, 114706.
    104. Mir, N.A.; Rafiq, A.; Kumar, F.; Singh, V.; Shukla, V. Determinants of Broiler Chicken Meat Quality and Factors Affecting Them: A Review. J. Food Sci. Technol. 2017, 54, 2997–3009.
    105. Karunanayaka, D.S.; Jayasena, D.D.; Jo, C. Prevalence of pale, soft, and exudative (PSE) condition in chicken meat used for commercial meat processing and its effect on roasted chicken breast. J. Anim. Sci. Technol. 2016, 58, 27.
    106. Sugiharto, S.; Yudiarti, T.; Isroli, I.; Widiastuti, E.; Wahyuni, H.I.; Sartono, T.A.; Nurwantoro, N.; Al-Baarri, A.N. Effect of dietary supplementation of formic acid, butyric acid or their combination on carcass and meat characteristics of broiler chickens. J. Indones. Trop. Anim. Agric. 2019, 44, 286–294.
    107. El-Senousey, H.K.; Fouad, A.M.; Yao, J.H.; Zhang, Z.G.; Shen, Q.W. Dietary Alpha Lipoic Acid Improves Body Composition, Meat Quality and Decreases Collagen Content in Muscle of Broiler Chickens. Asian Australas. J. Anim. Sci. 2013, 26, 394–400.
    108. Menconi, A.; Kuttappan, V.A.; Hernandez-Velasco, X.; Urbano, T.; Matté, F.; Layton, S.; Kallapura, G.; Latorre, J.; Morales, B.E.; Prado, O.; et al. Evaluation of a commercially available organic acid product on body weight loss, carcass yield, and meat quality during preslaughter feed withdrawal in broiler chickens: A poultry welfare and economic perspective. Poult. Sci. 2014, 93, 448–455.
    109. Attia, F.M. Effect of organic acids supplementation on nutrients digestibility, gut microbiota and immune response of broiler chicks. Egypt Poult. Sci. J. 2018, 38, 223–239.
    110. Akbar, M.A.; Tewatia, B.S.; Kumar, S. Effect of dietary supplementation of salts of organic acids on gut morphology and meat quality of broilers. Indian J. Anim. Res. 2018, 52, 1727–1731.
    More