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Review

Time for a Paradigm Shift in Animal Nutrition Metabolic Pathway: Dietary Inclusion of Organic Acids on the Production Parameters, Nutrient Digestibility, and Meat Quality Traits of Swine and Broilers

by
Dhanushka Rathnayake
1,†,
Hong Seok Mun
1,2,†,
Muhammad Ammar Dilawar
1,2,
Kwang Soo Baek
2 and
Chul Ju Yang
1,2,*
1
Animal Nutrition and Feed Science Laboratory, Department of Animal Science and Technology, Sunchon National University, Suncheon 57922, Korea
2
Interdisciplinary Program in IT-Bio Convergence System (BK21 PLUS), Sunchon National University, Suncheon 57922, Korea
*
Author to whom correspondence should be addressed.
†
This author contributed equally to this work.
Life 2021, 11(6), 476; https://doi.org/10.3390/life11060476
Submission received: 20 April 2021 / Revised: 21 May 2021 / Accepted: 22 May 2021 / Published: 24 May 2021
(This article belongs to the Section Animal Science)
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Abstract

:
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. Moreover, the ultimate production parameters are not similar owing to the type of OAs, concentration level, growth phase, health status of animals, hygienic standards, and environmental factors. Thus, those factors need to be considered before implementing OAs in feeding practices. In conclusion, the current review evaluates the basics of OAs, mode of action, novel strategies to enhance utilization, influence on growth performances, nutrient digestibility, and meat quality traits of swine and broilers and their potential concerns regarding utilization.

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).
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).
This review evaluates the response of swine and broilers to OAs supplementation of previous studies in terms of the growth production parameters, including feed intake, weight gain, feed conversion ratio (FCR), nutrient digestibility, and meat quality traits. The possible modes of action, causes of various responses due to OAs, and potential concerns regarding OAs are also assessed.

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).
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).
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. Novel Strategies for Enhancing Efficacy of OAs Availability in the Gastrointestinal Tract (GIT)

The supplementation of feed and water with OAs did not show better efficacy in the latter part of the GIT. It occurs due to the high proportion of short-chain fatty acids (SCFA) that are metabolized and absorbed rapidly in the upper segments of the GIT [39]. Thus, the OAs concentration tends to decrease and exert negative feedback on modifying the host microflora content in the GIT. New studies have shown that microencapsulated lipid shells facilitate the transportation of SCFA further down the GIT while increasing the retention time [39,40]. Furthermore, microencapsulated feed improves palatability, removes unpleasant odors/ flavors, and delivers the necessary compounds to the specific target place inside the animal body while acting as a “biological agent” [2]. Further studies have demonstrated that the efficiency of OAs can be improved by incorporating phytogenic feed additives. Owing to the synergistic effects of both OAs and botanicals, food-safety bacteria, such as C. jejuni and S. typhimurium counts, tend to decrease. In particular, pore-forming agents derived from numerous aromatic compounds caused changes in the bacterial cell membrane by providing a pathway for OAs entrance [41,42]. Grilli et al. [43] indicated that a combination of microencapsulated OAs (citric and sorbic acid) and pure botanicals in weaning pigs’ diet improved the maturation of the intestinal mucosa by exerting a positive impact on the barrier integrity in the jejunum and ileum while performing better growth performance. Gheisar et al. [44] observed a higher Lactobacilli content in the feces of broilers fed a diet supplemented with 0.075% microencapsulated OAs. Gheisari et al. [45] also reported that 0.2% OAs inclusion enhanced the Lactobacilli content while reducing the Clostridium perfringens, E. coli, and Salmonella spp content. Moreover, a 0.5% microencapsulated blend of OAs reduced the oxidative status, microbial loads, and improved the shelf life of broiler meat [46]. The protected OAs could be delivered to specific sites in the body and had a positive effect by eliminating the Coliforms counts in both the distal jejunum and cecum. In contrast, freely available OAs had little influence [47].
Since the form of OAs (SCFA) is naturally produced by the GIT, some studies reported that introducing both prebiotics and probiotics could stimulate the synthesis of SCFAs in the GIT [48,49]. This could be implemented in two ways: (1) direct administration of lactic acid-producing bacteria in the diet; and (2) the addition of prebiotic substances that enhance the proliferation of lactic acid bacteria and increase SCFA production [50,51]. Streptococcus, Saccharomyces, Enterococcus, Lactobacilli, Bacillus, Bifidobacterium, and Pediococcus are the probiotic strains mainly used in nutritional studies. These microbes protect the GIT through barrier effects, competitive exclusion, bacterial interference process, prevention of colonization, and bacterial antagonism [52,53]. These probiotic supplementations develop the cell structure, have immunological effects, and are resistant to pathogens. Ultimately, they enhance the production rate of SCFAs, intermediary products, and H2O2. Lactobacilli spp. can generate lactic acid, which can facilitate the synthesis of butyric acids with the collaboration of Clostridial clusters that reinforce the animal cross-feeding process [48]. Oligosaccharides and polysaccharides (non-digestible carbohydrates (NDC)), proteins, and particular lipids are used as prebiotics to provide a proper substrate for beneficial host microbes. Previous studies have stated that the administration of prebiotics has a positive effect on the natural production of OAs in the GIT. The supplementation of the diet with NDC enhances the Lactobacilli and Bifidobacterium population. In contrast, these microbes promote the synthesis of SCFA, such as propionate, acetate, and butyrate acids [54]. Rehman et al. [55] reported that 1% inulin inclusion increased the jejunum acetate concentration and n-valerate in the cecal digesta in broilers compared to the control diet. Overall, the dietary supplementation of prebiotics and probiotics will lead to optimal OAs production in the animal body.

4. Effect of OAs in Swine and Broiler

4.1. 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) [56]. 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 [57]. 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 [58]. Kuang et al. [59] 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 [60]. On the other hand, Risley et al. [61] 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. [62], 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. [63] and Partanen et al. [64] 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. [65] 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 [63]. 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 [66]. Hassan et al. [67] 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 [68] 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 [69]. 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 [70].
Table
Table 2. Effect of organic acids mixture on growth performances and other parameters of swine and broilers.
Table 2. Effect of organic acids mixture on growth performances and other parameters of swine and broilers.
Dosage and Organic Acid/Acids Growth PhaseGrowth PerformancesIntestinal/Fecal Microbial Counts (CFU)Other ParametersReferences
BWG/FBWADFIG:F
Swine
0.1% and 0.2% fumaric, citric, malic, MCFA (capric and caprylic) Weaning SNSSE. coli; S
Lactobacilli; S
Clostridium; S
Salmonella; S
  • Reduced diarrhea score, fecal ammonia, and acetic acid emission
Yang et al., 2018 [71]
0.1% and 0.2% fumaric, citric, malic, MCFA (capric and acrylic) Growing SNSSLactobacilli; S
E. coli; NS		-Upadhya et al., 2016 [72]
0.15% benzoic, fumaric, calcium formateWeaning SNSNSE. 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 [73]
1.1% acetic, propionic, phosphoric, citric acidWeaning NSNSNSLactobacilli; NS
E. coli; NS
Coliforms; NS
  • Reduced pH level in colon
  • Retardation of Coliforms proliferation
Namkung et al., 2004 [74]
0.4% and 0.2% fumaric, lactate, citric, propionic, benzoic acidWeaning NSNSNSE. coli; NS-Walsh et al., 2007 [56]
0.5% benzoic acidWeaning SSSLactobacilli; S-Wei et al., 2021 [75]
0.5, 1% benzoic acidWeaning SNSNSNE
  • 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 [76]
0.5% butanoic, fumaric, benzoic acidPigletsSNSSLactobacilli; 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 [77]
0.1% fumaric, citric, malic, MCFA (capric and caprylic)Finishing SNSSLactobacilli; NS
E. coli; NS
  • Reduced feces H2S gas emission
Upadhya et al., 2014 [78]
0.85% formic, benzoic, sorbic, Ca- butyrate Growing male pigsNSNSNSE. coli; S
Lactobacilli; S
  • Lower level of Coliforms, Enterococci, and lactic acid bacteria in jejunum and colon descendens
Øverland et al., 2007 [79]
0.5% benzoic acidWeaning SSSE. coli; NS
Lactobacilli; NS
  • Reduced diarrhea in weaning pigs
Papatsiros et al., 2011 [80]
0.14% and 0.64% formic acidWeaning SSNSLactobacilli; 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 		FinishingSNSSNE
  • Reduced the ileal total bacterial count
  • Improved villi length
Saleem et al., 2020 [81]
1% formic, lactic, propionic, citric acidFinishingSNSNSNE
  • Enhanced V: C in GIT
  • Increased water consumption during 15–22 days
Ali et al., 2020 [82]
0.5% citric, sorbic, synthetic essential oil FinishingNSNSNSE. 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 [83]
0.15% formic, lactic, citric, malic, tartaric, phosphoric acidsFinishingSSSLactobacilli; S
E. coli; S
  • Enhanced inhibitory action owing to organic acid
Goh et al., 2020 [84]
0.3% formic, acetic, propionic, ammonium formate FinishingSNSNSNE
  • Increased SCFAs level in the cecum
  • Increased jejunal goblet cell density and ileal villus height
Dai et al., 2021 [85]
0.1% lactic, citric, acetic, formic, propionic, phosphoric, and sodium butyrateFinishing SNSSLactobacilli; S
Coliforms; NS
  • Increased jejunum villus height
  • Enhanced humoral immune response
Sabour et al., 2018 [86]
0.3, 0.5% formic, propionic acidFinishingSNSSLactobacilli; S
E. coli; S
  • Lower duodenal pH
  • High immune response against Newcastle disease, infectious bronchitis
Fathi et al., 2016 [87]
0.06% fumaric, calcium format, calcium propionate, potassium sorbate, hydrogenated vegetable oilFinishingSSSLactobacilli; S
Salmonella; S
  • Increased dressing percentage and bursa weight
Hassan et al., 2010 [67]
0.2, 0.4, and 0.6% butyric acidFinishingSNSSE. coli; S
  • pH reduction of upper GIT
  • Increased villus length and crypt depth in the duodenum
Panda et al., 2009 [88]
0.5, 1, 1.5, and 2% citric, lactic, phosphoric acidFinishingSNSSE. coli; S
Salmonella; S
  • 2% OAs blend enhanced the carcass yield
  • 1.5%, 2% OAs blend increased the liver weight
Sultan et al., 2015
[89]
0.6% formic acidFinishingSNSSE. coli; S (in crop)
  • Higher digestibility of crude protein, high dressed yield, and lower fat content in carcass
Panda et al., 2009
[90]
2% butyric, fumaric, lactic, and 3% butyric, fumaric, lactic acidFinishingSNSSNE
  • Increased villus height in the small intestines
  • Enhanced serum calcium and phosphorus concentrations
Adil et al., 2010 [25]
0.2% propionic, 0.3% butyric acidFinishingSNESNE
  • Increased tibia weight, tibia length
Lakshmi and Sunder., 2015 [91]
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.

4.2. 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 [78,92,93] and significantly increased DM, crude protein (CP), fat, and energy digestibility in growing pigs [94]. 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 [95]. Moreover, Yang et al. [71] 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 [96,97]; CP digestibility in weaning pigs [98]; and the DM, CP, ether extract (EE), and crude fiber (CF) of sows [99]. Previous studies demonstrated positive influence of OAs supplementation on the nutrient digestibility in both swine and broilers (Table 3).
Nevertheless, Upadhya et al. [72] 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 [100,101]. Ao et al. [102] 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 [103]. 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 [104].
Smulikowska et al. [105] 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 [106]. 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 [107]. 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
Table 3. Effect of organic acids combination on nutrient digestibility of swine and broilers.
Table 3. Effect of organic acids combination on nutrient digestibility of swine and broilers.
Dosage and Organic Acid/AcidsGrowth PhaseDigestibilityReference
DM NECP
Swine
0.2% fumaric, citric, malic, capric, and caprylic acidGrowingSSSSHossain et al., 2011 [94]
0.05% citric, sorbic acidGrowingSNSSNCCho et al., 2014 [108]
2% benzoic acidLactating sowsS (OM)NENESKluge et al., 2010 [99]
0.1% and 0.2% fumaric, citric, MCFAFinishingSSSNEUpadhaya et al., 2014 [92]
0.5% phenyllactic acidWeaningSSNENEWang et al., 2009 [109]
0.3% formic, acetic, propionic, MCFAWeaningS (DM)
NS (OM)		NSNSNSLong et al., 2018 [110]
0.5% formic, propionic, lactic, citric, sorbic acidPost-weaningNSNSNSNSGerritsen et al., 2010 [111]
300 mEq acid/kg formic, n-butyric acidGrowingSSSSMroz et al., 2000 [112]
0.15% citric acidLactating sowsNENENESLiu et al., 2014a [95]
0.2% fumaric, citric, malic, capric, caprylic acidLactating sowsSSSNEDevi et al., 2016 [113]
Broilers
0.2% formic, propionic acidFinishingNSNENESEmami et al., 2013 [104]
0.5% formic acidFinishingNSNENENSHernández et al., 2006 [101]
0.25, 0.5, and 0.75% formic acidFinishingNSNENESNdelekwute et al., 2015 [114]
5000ppm and 10,000ppm formic acidFinishingSNENESGarcia et al., 2007 [101]
0.25% acetic, butyric, citric, formic acidFinishingSNENSSNdelekwute et al., 2019 [115]
1, 2, and 3% citric acidFinishingNENESSGhazalah et al., 2011 [69]
0.5, 1, and 1.5% fumaric acidFinishingNENESSGhazalah et al., 2011 [69]
0.25, 0.5% formic acidFinishingNENENSSGhazalah et al., 2011 [69]
0.25, 0.5, and 0.75% acetic acidFinishingNENESNSGhazalah et al., 2011 [69]
N, nitrogen; E, energy; CP, crude protein; S, significant; NS, non-significant; NE, not-evaluated; OM, organic matter; DM, dry matter.

4.3. 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. [92] 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. [108] 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 [116]. Jansons et al. [117] 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. [118] 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. [119] 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 [120]. 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 [121]. 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) [122]. Sugiharto et al. [123] 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. [124] 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. [125] 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. [126], 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. [127] 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.

5. Potential Concerns Regarding OAs Utilization

Pathogenic microbial activities encompass a broad range of survival mechanisms that facilitate the multiplication and survival by evading their host defense system. Although OAs supplementation has a favorable impact on pigs and broiler production through the biological defense system, bacterial resistance should be considered. Recent studies revealed the specific, developed mechanisms of Escherichia coli [128] and Salmonella enterica [129,130]. Mutations of some genes, such as wecA (rfe), waaG (rfaG), fcl (Fucose, FX-like), and wecB (rffE), influence creating adaptation ability in Salmonella spp and E. coli groups against the OAs. This adaption process consists of two mechanisms: (1) transient adaptation and (2) pre-challenge adaptation, which occurs specifically in lower pH ranges [131,132,133]. On the other hand, the prevalence is affected by the temperature and type of the acidifier. OAs, being SCFA, have lower pH levels in the GIT, consequently reducing the livability of pathogenic bacteria at the cellular level. Nevertheless, bacterial pH-independent tolerance is also possible. Higher resistance to S. typhimurium was observed when the animals were exposed to higher SCFA concentrations, which produced a lower pH environment in the GIT [134]. Another considerable effect of supplementation of OAs is the reduction of lactic acid synthesis and lactic acid bacteria population in the GIT. Thompsan and Hinton [135] reported the interaction of formic and propionic acid inclusion on lower lactic acid production in the crop. Thus, the concentrations and interactions among each OA combination may require further molecular-based studies to identify the associated potential risks.

6. Conclusions

The supplementation of organic acids has significant effects on the growth performance and digestion of nutrients by modulating the gut environment of both swine and broilers. According to the literature, OAs supplementation effectively induces a pH reduction in the GIT, plays a significant role against pathological bacteria colonization, and eventually improves nutrients utilization and growth performances. Incorporation of microencapsulation technology has potential ability to enhance the uniform transportation of SCFA further down the GIT while allowing effective utilization. Moreover, prebiotics and probiotics inclusion also influence enhanced SCFA availability through beneficial gut microflora activities. Further, acting as an energy source during GIT intermediary metabolism, OAs inclusion positively influences growth performances. The growth performances and carcass quality development occur due to proper nutrient utilization, feed conversion efficiency, and improved weight gain. On the other hand, to benefit from the effectiveness of OAs, the inclusion dosage, rearing environment, nutrient composition, growth phase, and health status of animals need to be considered in future studies. The chemical mechanisms of OAs in animal diet and synergism effects are not completely understood. Therefore, it is impossible to recommend a specific combination of OAs and concentrations that will positively affect the swine and broiler production parameters and meat quality traits. Once more knowledge becomes available, promising feeding strategies can be implemented by incorporating various organic acid formulas into the animal diet. In a nutshell, OAs supplementation to the animal diet exerts a positive impact on growth performances, inhibition of pathogenic bacteria, enhancement of nutrient digestibility, meat quality characteristics, and mineral utilization by minimizing microbial competition.

Author Contributions

Conceptualization, C.J.Y. and D.R.; validation, M.A.D. and K.S.B.; formal analysis, H.S.M.; investigation, C.J.Y.; resources, H.S.M.; writing—original draft preparation, D.R. and M.A.D.; writing—review and editing, D.R.; supervision, C.J.Y. and H.S.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not Applicable.

Acknowledgments

Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, and Forestry (IPET) and Korea Smart Farm R&D Foundation through Smart Farm Innovation Technology Development Program, funded by Ministry of Agriculture, Food, and Rural Affairs (MAFRA) and Ministry of Science and ICT (MSIT) and Rural Development Administration (RDA) (421023-04, 421047-03).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Various application and benefits of organic acids in the livestock sector [16].
Figure 1. Various application and benefits of organic acids in the livestock sector [16].
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Figure 2. Two different mechanisms of organic acids on altering the pH of the GIT and their impact on pathogens [15].
Figure 2. Two different mechanisms of organic acids on altering the pH of the GIT and their impact on pathogens [15].
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Figure 3. Mode of action of organic acids on pH-sensitive bacteria (Clostridia, Salmonella, Coliforms, Listeria spp.) [36].
Figure 3. Mode of action of organic acids on pH-sensitive bacteria (Clostridia, Salmonella, Coliforms, Listeria spp.) [36].
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Table
Table 1. Common organic acids involved in animal nutrition and their properties [16,18].
Table 1. Common organic acids involved in animal nutrition and their properties [16,18].
AcidChemical NameRegistration NumberMolecular Weight/GE (MJ/Kg)OdorpKa
ButyricButanoic Acid-88.12/24.8rancid4.82
Citric2-Hydroxy-1,2,3-Propanetricarboxylic AcidE 330192.1/10.2odorless3.13
Propionic2-Propanoic Acid1a29774.08/20.6pungent4.88
Sorbic2,4-Hexandienoic AcidE 200112.1/27.85mildly acrid4.76
FormicMethanoic AcidE 23646.03/5.7pungent3.75
AceticEthanoic AcidE 26060.05/14.6pungent4.76
Lactic2-Hydroxypropanoic AcidE 26090.08/15.1sour milk3.83
MalicHydroxybutanedioic AcidE 296134.1/10.0apple3.40
Fumaric2-Butenedioic Acid2b08025116.1/11.5odorless3.02
BenzoicBenzenecarboxylic acid---4.20
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Rathnayake, D.; Mun, H.S.; Dilawar, M.A.; Baek, K.S.; Yang, C.J. Time for a Paradigm Shift in Animal Nutrition Metabolic Pathway: Dietary Inclusion of Organic Acids on the Production Parameters, Nutrient Digestibility, and Meat Quality Traits of Swine and Broilers. Life 2021, 11, 476. https://doi.org/10.3390/life11060476

AMA Style

Rathnayake D, Mun HS, Dilawar MA, Baek KS, Yang CJ. Time for a Paradigm Shift in Animal Nutrition Metabolic Pathway: Dietary Inclusion of Organic Acids on the Production Parameters, Nutrient Digestibility, and Meat Quality Traits of Swine and Broilers. Life. 2021; 11(6):476. https://doi.org/10.3390/life11060476

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Rathnayake, Dhanushka, Hong Seok Mun, Muhammad Ammar Dilawar, Kwang Soo Baek, and Chul Ju Yang. 2021. "Time for a Paradigm Shift in Animal Nutrition Metabolic Pathway: Dietary Inclusion of Organic Acids on the Production Parameters, Nutrient Digestibility, and Meat Quality Traits of Swine and Broilers" Life 11, no. 6: 476. https://doi.org/10.3390/life11060476

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