Research Article

An Update on the Promising Role of Organic Acids in Broiler and Layer Production

Ghulam Abbas1*, Muhammad Arshad1, Muhammad Saeed2*; Safdar Imran3, Ashgar Ali Kamboh4, Duraid KA Al-Taey5, Muhammad Asad Aslam1, Muhammad Saeed Imran6, Muhammad Ashraf3, Muhammad Asif7, Abdul Jabbar Tanveer8, Razia Abdul Majid Qureshi9, Maria Arshad1, Hussain Ahmed Khan Niazi1, Muhammad Tariq10, Sikandar Abbas1

1Riphah College of Veterinary Sciences, Riphah International University Lahore, Pakistan; 2Cholistan University of Veterinary and Animal Sciences, Bahawalpur, Pakistan;3Institute of Animal and Dairy Sciences, University of Agriculture Faisalabad, Pakistan; 4Department of Veterinary Microbiology, Sindh Agriculture University Tandojam, Pakistan; 5Department of Horticulture, College of Agriculture, AL-Qasim Green University, Iraq; 6Department of Pathology, University of Veterinary and Animal Sciences, Lahore, Pakistan; 7Institute of Continuing Education & Extension University of Veterinary and Animal Sciences, Lahore, Pakistan; 8Faculty of Veterinary and Animal Sciences, Gomal University Dera Ismaeel Khan, Pakistan; 9Department of Physics, University of Lahore, Pakistan; 10Department of Livestock Management, University of Agriculture Faisalabad, Sub-Campus Toba Tek Singh, Pakistan.

Received | February 04, 2022; Accepted | March 25, 2022; Published | June 15, 2022

*Correspondence | Ghulam Abbas, Muhammad Saeed, Riphah College of Veterinary Sciences, Riphah International University Lahore, Pakistan; Cholistan University of Veterinary and Animal Sciences, Bahawalpur, Pakistan; Email: [email protected]; [email protected]

Citation | Abbas G, Arshad M, Saeed M, Imran S, Kamboh AA, Al-Taey DK, Aslam MA, Imran MS, Ashraf M, Asif M, Tanveer AJ, Qureshi RAM, Arshad M, Niazi HAK, Tariq M, Abbas S (2022). An update on the promising role of organic acids in broiler and layer production. J. Anim. Health Prod. 10(3): 273-286.

DOI | http://dx.doi.org/10.17582/journal.jahp/2022/10.3.273.286

ISSN | 2308-2801

 

 

Copyright: 2022 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Chicken are our ‘‘bread and butter’’ and Poultry industry is a most active sector which has become employment source for the growing human population (estimated to be 6.8 thousands million) throughout the world (Abbas et al., 2020; Abbas et al., 2021). Commercial poultry production throughout the world is facing the challenges of diseases like mycoplasmosis, coccidiosis, salmonellosis etc., which produce economical losses due to poor weight gain or even huge mortality. In the past, antibiotic were excessively used in poultry o overcome these problems, in order to improve growth performance and to protect the poultry from the antagonistic effects of non-pathogenic and pathogenic enteric microorganisms. But in modern poultry production use of antibiotics is intensively controversial due to the expansion of anti-bacterial resistance and potential consequence on the human health, environment and food safety issues. Since, January 2006, European Union has strictly expelled the usage of antibiotic in poultry production. Therefore, prebiotics, probiotics, phytochemicals and organic acid are being taken into account as an alternative and substitutes of antibiotics (Abbas et al., 2022; Abbas et al., 2018; Lagua and Ampode, 2021; Refaie et al., 2022; Saeed et al., 2020).

Use of organic acids (OA) as an alternative of antibiotics is of great interest in poultry production (Panda et al., 2009). The OA are carbon-based compounds possessing weak acidic characteristics. Carboxyl group of the carboxylic acids make it the most commonly found OA on this planet. The strongest among organic acids are sulfonic acids that possess sulfide group. Alcohols can also be considered as OA due to their hydroxyl group, but they are very weak (Jones et al., 1998). The acidity of an OA is measured by the comparative steadiness of its conjugate base. The thiol, enol, and the phenol group can also impart weak acidic properties to their parent compounds. Some examples which are commonly found in the organic acid are citric acid, tartaric acid, oxalic acid, formic acid, acetic acid, malic acid and propionic acid (Deng et al., 2016). Organic acids are ubiquitous in nature and also found in microbes, plants and animals. The main feature is their carboxylic group which is covalently linked to either of amides, esters or peptides (Doores et al., 2005). They were first discovered in 1817 by dry distillation of malic acid resulting in tras form of fumaric acid and cris form of maleic acid. In 1937, Kreb described the involvement of these acids in the tricarboxylic acid (TCA) cycle (Goldberg et al., 2006). Soon, their production on large scale began predominantly with microbial origin. Currently, a number of organic acids are being produced on industrial scale comprising mainly of bacterial and fungal origin (Mattey et al., 1992). Most of them are mono-carboxylic acids but now the focus is also shifting on di- and tri-carboxylic acids. Citric acid and lactic acid are the most widely studied and produced organic acids (Yao et al., 2004).The gastric pH was observed to have a drop in value however caecal pH does not exhibit a similar fall in value by OA supplementation. The OA concentration depletes as it reaches the caeca hence the effect is not as pronounced as in the crop. However, the drop in the gastric pH has a beneficial effect in the overall digestion process as the reduced gastric pH enhances the activity of pepsin (Adil et al., 2010). The peptides that were a product of the proteolysis stimulate the eventual release of some hormones like gastrin and cholecystokinin which aid the degradation as well as the absorption of protein. The OA also promoted the production of pancreatic juices (chymotrypsinogen A, B and procarboxy peptidase enzyme) resulting in better degradation of protein (Adil et al., 2010; Afsharmaneshet al., 2005). Major aspect of the use of dietary OA supplements for broilers is its effects on the small intestine architecture such as villus height, villus width and crypts depth (Loddi et al., 2004; Pelicano et al., 2005). The OA seem to have a significant effect on the height of villus as well as the crypt depth. The use of OA also lessens the muscularis thickness. These positive effects are attributed to the depleted inflammation levels at mucosal surfaces because of the modulatory effects of OA on the gut bacterial communities. In absence of inflammatory reactions, the intestinal tissues undergo positive changes like increase in villus height and crypt depth. Muscularis thinning is also beneficial in the absorption of nutrients. All those factors lead to a higher degree of nutrient digestibility and absorption (Savage et al., 1996; Bradley et al., 1994). Enhancing effects on the gastrointestinal tract (GIT) length are also observed with OA supplementation as it increases the length and weight of the GIT tract owing to gut cell proliferation (Denli et al., 2003). Potential mediators of GIT cell proliferation such as jejunal glucose transporter-2 (GLUT-2) expression, ilealpro-glucagon expression and plasma glucagon-like peptide 2 (GLP-2) concentrations were increased with the use of OA and SCFAs (short-chain fatty acids) were also considered to have a similar effect (Tappenden et al., 1998). Enhancement of these potential mediators of GIT cell proliferation and decrease in inflammatory reactions have a symbiotic effect on the improvement of intestinal tissues which aids the digestion, absorption and assimilation of nutrients (Salvi et al., 2021). Ascorbic acid was reported to have a significant hepatoprotective effect against drug induced deleterious effects (Omara et al., 2021).

Growth metrics such as feed conversion ratio and body weight gain indicate a spike with use of OA in the broiler feed. Improvement in the absorption and digestion of the nutrients results in increased weight gain which eventually leads to a better feed conversion ratio (Vogt et al., 1981). However, an additional factor that helps improve the feed conversion ratio is the decreased feed intake. Feed intake falls slightly due to satiation effects produced by OA such as fumaric acid (Cave et al., 1978). As the utilization and assimilation of the already available nutrients improves, the need for additional nutrients falls and resultantly the feed intake also falls. The body weight gain however goes up as does the feed conversion ratio consequentially (Henry et al., 1987). Decreased microbial load in the gut leads to lessened competition for nutrients and eventually more nutrients get absorbed and utilized for the body to use in growth. There is no significant change in carcass properties have been observed by using dietary OA supplement in feed (Lückstädt et al., 2009). The use of OA as preservatives in grain and forage, and as nutrients in animal and poultry feed has been known for years. Their historic use in food preservation has been accepted by communities all over the world (Lückstädt et al., 2011). Their efficacy as performance enhancement, antimicrobial activity, feed preservatives, and nutrient digestibility has made them ideal candidates for use as an essential component of livestock and poultry feed. They reduce the microbial uptake, stabilize the gut micro-flora, and enhance the digestion and absorption from the intestines (Freitag et al., 2007).This review has summarized the importance OA in poultry industry with specific focus on broiler and layer birds. Various facts and figures about the correlation of bird performance with use of OA have been discussed to further highlight their potential to researchers to dig more focus on this research area.

Characteristics of organic acids

Generally, OA are considered as weak acids that are not completely dissolve in water, whereas strong mineral acids commonly do. Some OA like lactic acid and formic acid are soluble in water due to their lower molecular mass while benzoic acids in neutral form having higher molecular mass are insoluble. On the other hand, most of OA are easily miscible in the organic solvents such asp-TFoluene sulfonic acid which comparatively possess strong acidic properties and used in the organic chemistry often because it can efficiently dissociate in organic solvents (Baghernejad et al., 2011). In Table 1, the physiochemical properties of important organic acids is discussed.

Effects of Organic acid supplemented diet

The use of formic acid as feed preservative in poultry feed and as a supplement to enhance the production performance of poultry is well documented  (Lückstädt et al., 2014; Abbas et al., 2013; Lückstädt et al., 2011; Garciá et al., 2007; Freitag et al., 2007; Hernández et al., 2006). Afterwards, the use of calcium formate in broiler diet has also reported to reduce level of Salmonella spp. in the poultry carcass and fecal samples (Açıkgöz et al., 2011; Hassan

et al., 2010; Byrd et al., 2001). Buffered propionic acids were utilized to neutralize harmful gut micro-flora in the GIT of broiler chicken, as a resultant significant decrease in Escherichia coli as well as Salmonella spp. was observed in carcass (Ricke et al., 2020). Unadulterated formic acid’s utilization in the diet of breeders diminishes the taint of hatchery and tray liners with Salmonella enteritidis (Humphery et al., 1988).

Fermentation with different natural acids to diets, for example, formic acid, propionic acid, fumaric acid, sorbic, and lactic acid have been accounted for diminishing the colonization of microbes (Hamed et al., 2013; Hassan et al., 2010) and synthesis of noxious metabolites, enhancing the absorbability of various proteins and elements like magnesium, calcium, zinc and phosphorus and also acting as substrate in the intermediary digestion (Dibner et al., 2002; Sohail et al., 2016). A few studies exhibited that supplementation of OA to the broiler diet improved the growth performance, diminished illnesses, and managerial issues. Hinton and Linton (1988) observed the effects of utilizing formic acid and propionic acid in combination on salmonellosis in broilers. They reported that 0.6% (6kg/t) of this natural acid mix showed good results in intestinal proliferation of Salmonella spp. when fed with both natural as well as artificially manufactured feed. Performance and hygiene improvements have been observed in the broiler with time by the use of OA (Hamed et al., 2013; Açıkgöz et al., 2011; Byrd et al., 2001). However, a noteworthy limitation is that OA are quickly processed in the foregut (Lückstädt et al., 2011), which lessen their effect on growth development. Mixing of OA with salts, for example, sodium diformate (C2H2Na2O4),ammonium formate, potassium diformate (C2H3KO4) or calcium propionate that reach the digestive tract seemed to have a huge effect (Paul et al., 2007; Mikkelsen et al., 2009; Lückstädt et al., 2011). The impact of the use of C2H3KO4 i.e., potassium diformate at dose rate of 0.3-1.2 percent until 35 days after hatching has been observed. Potassium diformate decreased the number of pathogenic microorganisms such as Salmonella, Enterobacter and Campylobacter in broiler and increased the number of useful microorganisms like Lactobacillus and Bifidobacterium (Mikkelsen et al., 2009; Lückstädt et al., 2011). The anti-microbial characters of OA were observed at low pH, in such conditions their dissociated carboxyl groups infiltrate the bacterial cells ultimately causing cell death. The OA which have a broader range of pKa (acid dissociation constants; the lower the value of pKa, the stronger the OA) have a wide spectrum of mechanism in the gut. Hence owing to their antimicrobial characteristics, OA are considered substitutes to synthetic promoters of growth (Dibner and Buttin 2002; Cherrington et al., 1991). OA regardless of the kind and quantity of acid used were observed to have a beneficial effect on the performance of broilers (Adil et al., 2010).

 

Table 1: Physiochemical Properties of Important Organic Acids

Acid	Molecular Formula	Molecular Mass	Physical Form	Solubility in Water
Acetic acid	CH3COOH	60.1	Liquid	100%
Butyric acid	CH3CH2CH2COOH	88.1	Liquid	100%
Citric acid	COOHCH2C(OH)(COOH)CH2COOH	192.1	Solid	High
Formic acid	HCOOH	46.0	Liquid	100%
Lactic acid	CH3CH(OH)COOH	90.1	Liquid	High
Malic acid	COOHCH2CH(OH)COOH	134.1	Liquid	100%
Propionic acid	CH3CH2COOH	74.08	Liquid	100%
Sorbic acid	CH3CH:CHCH:CHCOOH	112.1	Liquid	Low
Tartaric acid	COOHCH(OH)CH(OH)COOH	150.1	Liquid	High

 

Table 2: Summarized effects of various studies that shown the importance of different organic acids.

Name of organic Acid	Dose	Specie	Effects (Increase: ↑, Decrease: ↓)	References
Butyric acid, Fumaric acid, Lactic acid	2% and 3%	Broiler	↓Coliform count, ↓Viable count in caeca, ↓ Crop pH, ↓Caecal pH, ↑FCR, ↑Body weight, ↓Feed intake	Banday et al., 2011
Butyric acid, Fumaric acid, Lactic acid	2% and 3%	Broiler	↑Serum Calcium (mg/dL), ↑Phosphorus (mg/dL), ↑Total protein (gm/dL)	Rehman et al., 2010, Banday et al., 2011
Butyric acid, Fumaric acid, Lactic acid	2% and 3%	Broiler	↑Villus height (μm), except for lactic acid (2%) that decreased villus height	Adil et al., 2010
Butyric acid, Lactic acid,	2% 2% and 3%	Broiler	↑Crypt depth (μm) in duodenum
Butyric acid, Fumaric acid,	3% 2% and 3%	Broiler	↓Crypt depth (μm) in duodenum
Butyric acid, Fumaric acid, Lactic acid	2% and 3%	Broiler	↓Muscularis thickness (μm) in duodenum, jejunum and ileum, ↑Villus height (μm) in jejunum and ileum
Butyric acid	2% and 3%	Broiler	↑Crypt depth (μm) in jejunum
Fumaric acid, Lactic acid	2% and 3%	Broiler	↓Crypt depth (μm) in jejunum
Butyric acid, Fumaric acid, Lactic acid	2% 3% 2%	Broiler	↑Crypt depth (μm) in ileum
Butyric acid, Fumaric acid, Lactic acid	3% 2% 3%	Broiler	↓Crypt depth (μm) in ileum
Butyric acid, Fumaric acid, Lactic acid	2% and 3%	Broiler	↑GIT length	Denli et al., 2003
Butyric acid, Fumaric acid	2% and 3% 3%	Broiler	↑Glucose (mg/dL)	Adil et al., 2010
Lactic acid Fumaric acid	2% and 3% 2%	Broiler	↓Glucose (mg/dL)
Butyric acid, Fumaric acid, Lactic acid	2% and 3% (except for Fumaric acid 2%)	Broiler	↓Cholesterol (mg/dL)
Butyric acid, Lactic acid	2%	Broiler	↓SGPT (μ/L)	SA et al., 2008; Adil et al., 2010
Butyric acid, Fumaric acid, Lactic acid	3% 2% and 3% 3%	Broiler	↑SGPT (μ/L)
Butyric acid, Fumaric acid, Lactic acid	2% 3% 2%	Broiler	↑SGOT(μ/L)
Butyric acid, Fumaric acid, Lactic acid	3% 2% 3%	Broiler	↓SGOT(μ/L)
Butyric acid, Fumaric acid, Lactic acid	2% and 3%		↑Ready to cook yield (%), ↑Dressing percentage, ↑Intestine length (cm), ↑Intestine weight (g), ↑Liver weight (g) (except in Lactic acid 3%), ↑Heart weight (g) (except in 2% Butyric and Fumaric acid), ↑Gizzard weight (g) (except in Butyric acid on 2% and 3%), ↑Total giblets weight (g), ↑Head weight (g), ↑Feather weight (g) ↑Blood weight (g), ↑Drumstick weight (g), ↑Breast weight (g), ↑Shank weight (g) (except in 3% Lactic acid), ↑Neck weight (g), ↑Back weight (g), ↑Wings weight (g), ↑Thigh weight (g),	Thirumeigmanam et al.,2006; Adil et al., 2011a
Butyric acid and lactic Acid	0.2% and 0.05%	Broiler	↑Antibody titer against ND	Salazar et al., 2018
Butyric acid	0.1% to 0.4%	Broiler	↓Caecal E. coli, Salmonella spp. and Clostridium spp. count, ↑Lactobacilli spp. count, ↑Villus height in duodenum and jejunum (day 21), duodenum, jejunum and ileum on day 42, ↑ Crypt depth in duodenum, jejunum and ileum	Nataraja et al., 2020
Butyric acid	4 g /kg	Broiler	↑villus length and width, ↑ serum protein, albumin, creatinine, aspartate aminotransaminase (AST), phosphorus and calcium ↓Serum uric acid and cholesterol,	Raza et al., 2019
Butyric acid	500 g/t feed (encapsulated)	Layer	↑Eggshell thickness, eggshell weight, ↑calcium concentrations in bones, ↓ammonia concentrations in the caecum	Alicja et al., 2016
Fumaric acid	1.5%	Broiler	↑body weight gains and FCR, ↓pH of crop, proventriculus and gizzard	Banday et al., 2015
Fumaric acid	10-15g/Kg	Quail	↑growth performance, ↑Digestibility of crude protein and metabolizable energy	Fayiz et al.,2021
Fumaric acid	5g/kg	Broiler	↑Serum total protein, albumin, globulin, total cholesterol, high-density lipoprotein cholesterol	Ding et al.2020
Fumaric acid	10g/Kg	Broiler	↑FBW, ADFI, ADG, antibody titres against SRBC, IgG, relative weights of spleen and bursa, activity of GPx in thymus and bursa, ↓ FCR and TC of thymus and bursa	He at al., 2020
Fumaric acid Thymol	0.9g/kg 0.6 g/kg	Broiler	↑FCR and increased ileal villi height-to-crypt depth ratio (VH:CD), cecal abundance of Bacteroidetes, Bacillaceae, and Rikenellaceae ↓Pseudomonadaceae	Abdelli et al., 2021
Lactic Acid	0.3 g/kg	Broiler	↓Escherichia coli and Salmonella in the cecum	Gao et al., 2021

FCR: feed conversion ratio; SGPT: Serum glutamic pyruvic transaminase; SGOT: aspartate aminotransferase; ND: Newcastle disease; FBW: Final body weight; ADFI: average daily feed intake; ADG: average daily gain; SRBC: Sheep red blood cells; IgG: Immunoglobulin G; GPx: Glutathione peroxidase

 

Serum analysis after the use of OA in broiler feed spotlight an increase in calcium, phosphorus and total protein levels owing to increased digestibility and absorption of these components in crop and intestine (Teirlynck et al., 2009). However, glucose levels as well as cholesterol levels did not go up significantly with organic acids supplementation. SGPT and SGOT values also did not indicate any considerable changes (Adil et al., 2010). Major aspect of the use of dietary OA supplements for broilers is its effects on the small intestine properties such as villus height, crypts depth and thickening of muscularis. OA increase the villus height, crypt depth and lessen the muscularis thickness (Loddi et al., 2004; Pelicano et al., 2005). All those factors lead to a higher degree of nutrient digestibility and absorption. Enhancing effects on the GIT length are also observed with OA supplementation as it increases the length and weight of the GIT tract owing to GIT cell proliferation (Denli et al., 2003).Table 2 summarizes different studies that have shown the importance of different organic acids.

Significance of organic acid in Layer production

Egg production

Layer egg production can be increased significantly by using OA as dietary supplement. Yesilbag et al. (2006) revealed a positive effect of OA supplementation on normal egg production (18 weeks of experimentation).Likewise, some other workers (Soltan et al., 2008; Rahman et al., 2012) suggested 1.5% OA supplementation to improve the egg production in commercial layers. The average percentage of hens’ egg production increased significantly at an age of 70 weeks by about 5.77% to 9.84% when diet was supplemented by 0.078% of OA (formic acid, propionic acid, butyric acid, and lactic acid) compared to a basal diet. The feed conversion ratio (FCR) of the layers were greatly improved 1.85%, 8.48% and 7.74% in groups that supplemented with organic acid at 0.026%, 0.052% and 0.078% respectively.

Directed a baseline study in which an acidifier was added in poultry diet called phenylalanine (Wang et al., 2009). They determined that production of egg through the consumption of phenyl-rich acid diet was improved by 1.55%, 2.64%, and 2.69% by 0.5%, 1.0%, or by 1.5% OA respectively, in comparison with control group birds. Increase in the production of eggs was parallel with the increase in the amount of phenyl lactic acid. It is suggested that the increase in production is probably due to the anti-microbial activity of OA. Consumption of OA in poultry diet promotes the nutrient digestibility and thus can lead to increased feed efficiency and egg production.

Youssef et al. (2013) proclaimed that as compared to control diet OA supplemented layer diet exhibited an increase in feed intake (105 vs. 109 g/d/bird), egg production (88.50%vs. 97.30%), and feed conversion rate (1.98 vs.1.81). Likewise, (Grashorn et al., 2013) described that supplementation of OA (contained ammonium propionate 30%, formic acid 40%, lactic acid 26%, sorbic acid 0.5%, sodium benzoate 0.5%, and carrier3%) to layer diets significantly increased egg weight, production and FCR.

Park et al. (2009) studied the effect on layer bird’s performance by the addition of 0.2% of OA in diet. The addition of OA produces good results in the production of eggs and FCR as well as reduces the production of soft shell and broken eggs. It was concluded that the addition of OA may improve the hens’ production, quality of eggs, and reduce mortality. The OA is proposed to be associated with the increased utilization/ absorption of phosphorus and calcium and other minerals for shell formation (Dhawale et al., 2005; Boiling et al., 2000).

Presently, for growth improvement of birds in broiler and layer industry OA is preferred to be added in drinking water (Abbas et al., 2013; Chaveerach et al., 2004). Kadim et al. (2008) proclaimed that supplementation of acetic acid has been observed to improve average production of eggs during the hot season when given in drinking water. Abbas et al. (2013) proclaimed that improved feed conversion ratio and more egg production has been observed in layer those consumed drinking water withthe addition of formic acid during summer. The results revealed that hens consuming water with formic acid percentages, 0%, 0.05%, 0.10% or 0.15% exhibited improved egg production approximately 72%, 80%, 86% and 88% respectively.

Gut flora and environmental temperature variations are contributing factors to the performance of poultry by the use of OA (Mahdavi et al., 2005). Different vitamins and minerals concentrations in body tissue and serum of birds decreased due to high temperature (Abbas et al., 2021) leading towards reduction in egg production (Khattak et al., 2012). Supplementation of OA to the drinking water assists in the elimination of number of microorganisms in the water as well as from the proventriculus to direct gut microflora which promotes the digestion and absorption of feed in gut and enhances growth and development (Chaveerach et al., 2004). Supplementation of natural acids in water has been observed more viable than dietary addition since OA utilization is reduced depending upon the decrease in feed consumption during heat stress.

Egg quality

The incorporation of OA into the layer diet can significantly increase the egg weight and egg quality traits. Reported significant improvements in yolk index (P <0.05) and albumen index (P < 0.05) in layer chickens treated with addition of lactic acid 1% concentration (Yalcin et al., 2000). The Haugh unit scale is used to define egg quality (storage quality) in relation to the height of the thick albumen in egg weight. Described that hens’ diet containing 1% lactic acid, 0.05% of acetic acid and0.2% phenyl lactic acid caused improvements in the Haugh unit score (Yalcin et al., 2000). Found that eggshell weight, eggshell strength, albumen percentage, eggshell thickness and yolk pH were significantly improved when the drinking water of layers was supplemented with acetic acid (Kadim et al., 2008). Elaborated the improvement of egg thickness of layers fed diets supplemented by organic acids (Soltan et al., 2008). The eggshell strength of layers was reported to be improved by supplementation of 0.2% phenyl lactic acid (Wang et al., 2009). Similarly found that the eggshell thickness as well as eggs grade of layers consuming formic acid supplemented water were significantly higher (Abbas et al., 2013). The use of OA had positive effect on calcium absorption in layers that is why increasing the effectiveness of calcium (Abbas et al., 2013). Proclaimed that the weight and thickness of the egg shell of the layers raised at high temperatures could be significantly improved following the addition of OA. The development of egg quality can be the result of increased absorption of minerals and proteins contributing to improved quality that can lead to increased shell weight and thickness (Soltan et al., 2008).

Significance of organic acids in broilers’ performance

In the world of poultry production, utilization of natural acids is acquiring a lot of consideration. The high degree of production and feed conversion ratio in the modern broiler industry could be accomplished by the utilization of OA. OA have properties relating to growth and development and can be utilized instead of anti-microbial agents (Fascina et al., 2012). Observed that butyrate with a concentration of 0.4% in the poultry diet gives the same advantages to bodyweight acquire as that of use of antibiotics (Panda et al., 2009). Furthermore, (Adil et al., 2010, 2011b) found that chicks whose diet was supplemented with OA showed a huge improvement in the performance when contrasted with chicks feed on the control diet. The most improved weight gain in broiler was observed when fed on the diet having 3% fumaric acid. The improved FCR could be due to better utilization of supplements bringing betterment in the body weight gain of chicks fed on OA in the diet. Adil et al. (2011a) also revealed that broilers fed on a diet supplemented with lactic acid, butyric acid and fumaricacid (2-3%) showed improved performance. The improvement in FCR was deemed to be because of decreased feed intake bringing better body weight gain as a result of better utilization of various feed nutrients.

The utilization of OA may be more valuable than the utilization of antimicrobials for the optimal growth of broilers in poultry production. Hassan et al., (2010) used two artificially manufactured combinations of OA (Biacid® and Galliacid®) and an antimicrobial (Eneramycin®) to compare their effect on broiler performance. The results showed a 16% improvement in weight gain in Galliacid® group than the control group; on the other hand chicks fed on the Biacid® and Eneramycin® showed 3% and 5.5% more weight gain respectively. Fascina et al. (2012) revealed that the utilization of OA combination (involving 30.0 percent lactic acid, 25.5 percent benzoic acid, 8 percent citrus extract,7 percent formic acid, and 6.5 percent acetic acid) in broilers improved performance when contrasted with the control diet at 42 days trial period along with better carcass attributes. The positive effect of dietary OA on performance may be because of a decrease in pH of stomach which has antimicrobial impact alongside improved diet absorbability (Ghazala et al., 2011).

Significance of organic acids on GIT of chicken

Healthy GIT is essential in achieving targeted growth and feed efficiency in poultry sector. OA supplemented diet significantly increased the height of villi, width of villus and the area of ileum, jejunum and duodenum of 14-days-old broiler chicks (Garcia et al., 2007). The study described that birds that feed on 0.5-1.0% formic acid-containing diet have the longest villi height of about 1273µm and 1250 µm in comparison with control of 1088 µm. Likewise, jejunum crypts were found deeper (266µm vs 186 µm, respectively; P< 0.05) in birds feeding on1% formic acid mixed diet than in birds feeding on antibiotic diet. Therefore, the study illuminated that formic acid supplemented diet can increase both crypt depth and villus height. It has been reported that SCFAs enhance the growth and multiplication of normal crypt cells, improving and maintaining the healthy tissues. Frankel et al. (1994) demonstrated some trophic related effects of SCFAs to increase height of villus, surface area and crypts depth in jejunum in rat colons when fed with butyric acid supplemented diet. Similarly, Leeson et al. (2005) proclaimed that butyrate regardless of the concentration (0.6%, 0.4% or 0.2%) in broilers feed could improve the crypt depth as well as the villus height in duodenum. Therefore, the addition of butyrate can be very helpful for intestinal growth of young birds. It is claimed that organic acid salts significantly raised villus height in the ileum, jejunum and duodenum part of intestine. Pelicano et al. (2005) proclaimed the elevated height of villus in ileum due to organic acid-based diets compared to diet without mannan oligosaccharide + OA salts. Intestinal histology results revealed that OA salts like Ca propionate and ammonium formate when supplemented with feed increase the villus height of various parts of intestine in comparison with control group by decreasing the intestinal proliferation of infectious and non-infectious bacteria possibly. Thus, improvement in the height of villus in intestine enhanced the role of gut epithelium to act as natural barrier against different types of pathogenic bacteria and toxins because pathogenic substances cause disruption in the natural micro flora and gut epithelial permeability, making it easier for invaders to alter the metabolic activities (digestion and absorption) resulting in chronic inflammation of mucosa.

OA commonly used as an acidifier in chicken feed are considered attractive ways to improve digestion. Samanta et al. (2010) described that OA compounds increased gastric proteolysis and lowered pH of chyme thus, resulted an improvement in the amino acids and proteins’ digestion. Van Der et al. (2002) reported that the significant OA effect on intestinal digestion was linked to the slow digestion of nutrients in the intestine, improved absorption of essential nutrients and droppings that are less wet. Smulikowskaet al. (2009) described the nitrogen (N) retention capacity of some specific preparations of fat coated OA in broiler gut compared to non-supplemented diet. Increased N retention may be interlinked with a significant improvement in epithelial cells in the gastrointestinal tract. Unprotected OA in chicken feed are easily digested (Sugiharto et al., 2014), while fat-coated preparations prevented the breakdown of OA inside the stomach and aided to counteract their functionality and bioactivity by moving to distal intestines and better balancing of intestinal micro flora and histo-morphology in birds. The addition of an OA mixture (sodium bentonite and propionic acid) to the broiler feed has resulted in increased digestion and nutrient uptake (such as Ca and P) due to the proliferation of the desired micro flora (Lactobacillus spp.) of the digestive tract, this results in on increased retention of mineral elements and bones mineralization (Sugiharto et al., 2019). The graphical demonstration of promising benefits of different OA on poultry gut that have ultimate outcome of improve production and meat quality were shown in Figure 1.

Significance of organic acids in meat production

Lactic and acetic acid solutions (1-3%) are the most frequently used supplements in poultry production. However, many others, like formic, propionic, citric, fumaric, and L-ascorbic acid have been researched either individually or as a mixture for use in the chemical washing of the carcass. The exact mechanism of action is not completely comprehended on the microbial cell by organic acids, but it is hypothesized that the un-dissociated molecules of organic acid are responsible for the antimicrobial activity.

Conversely, Gill, (2009) inferred that, when taking the outcomes from three meat processing plants in the US, the clear impacts of the lactic acid spray could be ascribed to the washing impact of the treatment instead of any antimicrobial impact of the lactic acid. Greig et al. (2012) performed out a systemic overview and meta-investigation of the published research, observing the studies that reflected commercial conditions of processing. They proposed a more prominent decrease in the concentration and prevalence of conventional E. coli when acid is incorporated preceding dry chill, contrasted with dry chill alone, this improved efficacy is relatively small and should be evaluated against the expanded expense of chemicals and infrastructure. There is some proof that natural acids may improve the shelf life of atmospherically modified packaged food items, probably because they increase the period of the lag phase of the microorganisms (Podolak et al., 1996). Carpenter et al. (2011) reported that acid washing with acetic acid hindered the development of residual E. coli O157:H7 (a most hazardous strain of E.coli) for around 2 days, on an acid-treated meat plate. Nonetheless, detrimental sensory changes have been observed when meat was treated with lactic acid. Warm carcass surfaces treated with OA regularly showed some discoloration of tissue or fat surfaces. However, with boiling water pasteurization, this often vanishes or becomes less apparent after chilling (Carpenter et al., 2011).

Disadvantages of OA use in diets of poultry

There are some downsides of introducing OA in the poultry diets one of which is the refusal of feed due to change in palatability. Bacterial agents have been shown to develop resistance against the OA provided acidic environment when they had prolonged exposure. This leads to bacteria proliferating even when the birds fed with OA owing to the gradual resistance produced against the acidic environment. Anti-microbial compounds do not interact well with OA as the efficiency of the latter is reduced. Corrosive effects were observed on metallic poultry equipment that exposed to some organic acids (Goldberg et al., 2006; Hajati, 2018).

Conclusion

As the poultry industry is facing a growing need for antibiotic-free chickens, thus analyzing an effective alternative of antibiotics is the need of the hour, one that positively modulate microbiome in poultry gastrointestinal tract. It is also important that the approach chosen is easily incorporated into nutrition, animal care and housing for future use. The OA have acidifying functions that could be useful in poultry feed to avoid or fight pathogenic bacterial infections, so they can promote bird health and body function. However, a nutritionist should keep in mind various significant factors i.e., age of the birds, the microbiota of intestinal tract, gut environment or pH, etc. that can buffer different nutritional elements. Without a doubt, the discovery of microbiome sequences provides a chance to mimic the GIT poultry community in OA response. Literature proclaimed that OA (e.g., butyrate) supplementation, regardless of doses could improve the GIT architecture in growing chickens therefore; the addition of OA in the diet of young birds is recommended for intestinal growth. There’s a more research is required to determine the direct effect of OA in multiple stages of poultry health to determine the appropriate amount of supplementation of organic acids. Moreover, research should be done to find the most effective ways to reduce harmful pathogens in the stomach that may antagonize the effects of OA for further improve the poultry performance, and gut histomorphology.

conflict of interest

The authors have no conflict of interest.

novelty statement

The objective of the present manuscript is to find out befits of using organic acids in broiler and layer production. Although some scientists worked on this topic there was a need to summarize all the researches in a table form. In the present study, the effect of organic acids in layer and broiler production is studied exclusively.

authors contribution

Ghulam Abbas, Muhammad Arshad, Maria Arshad, Muhammad Saeed and Muhammad Saeed Imran designed the project/study. All authors critically revised the manuscript for significant intellectual contents and approved the final version.

References

Abbas G, Khan SH, Rehman H U (2013). Effects of formic acid administration in the drinking water on production performance, egg quality and immune system in layers during hot season.  Avian Biol. Res. 6(3): 227-232. https://doi.org/10.3184/175815513X13740707043279.

Abbas G, MA Jabbar, MA Javid (2020). Dietary Inclusion of Azolla (Azolla Pinnata) Meal as a Protein Source in Poultry Feed. Int. J. Anim. Husband. Vet. Sci. 5 (3): 2455-8567.

Abbas G (2020). Role of Poultry Production to Feed the Humanity on the Planet”. EC Agriculture. 6.2 (2020): 01.

Abbas G. S. Mahmood, A ulHaq, H Nawaz (2021). Effect of dietary inclusion of sodium bicarbonate on production performance of caged layers during summer. Pak. J. Zool. 54: 1-9.DOI: https://dx.doi.org/10.17582/journal.pjz/20190705200740.

Abbas G., M. Arshad, A. J. Tanveer , M. A. Jabbar, M. Arshad, D. K. A. AL-Taey, A. Mahmood, M. A. Khan, A. A. Khan, Y. Konca, Z. Sultan, R. A. M. Qureshi, A. Iqbal, F. Amad, M. Ashraf, M. Asif1, R. Mahmood, H. Abbas, S. G. mohyuddin, M. Y. Jiang (2022). Combating heat stress in laying hens a review. Pakistan J. Sci. 73 (4 ): 633-655.

Abbas G, Sohail HK, Habib-Ur R (2013). Effects of formic acid administration in the drinking water on production performance, egg quality and immune system in layers during hot season. Avian Biol. Res. 6(3):227–232. https://doi.org/10.3184/175815513X13740707043279.

Abbas G, MA Iqbal, M Riaz, M. Sajid, O Zahid, SW Abbas, H Saeed, AI Raza, MZ Ali (2018). Comparative Effect of Different Levels of Probiotics (Protexin) on Hemato-chemical Profile in Broilers, Adv. Zool. Bot. 6(3): 84-87. https://dx.doi.org/10.13189/azb.2018.060302.

Abdel-attah SA, EI-Sanhoury MH, EI-Mednay NM, Abdul-Azeem F (2008). Thyroid activity of broiler chicks fed supplemental organic acids. Int. J. Poult. Sci. 7: 215-222.

Abdelli N, F Pérez José, Vilarrasa Ester, Melo-Duran Diego, Cabeza Luna Irene, Karimirad Razzagh, Solà-Oriol David (2021). Microencapsulation Improved Fumaric Acid and Thymol Effects on Broiler Chickens Challenged With a Short-Term Fasting Period. Frontiers Vet. Sci. 8:1154. https://dx.doi.org/10.3389/fvets.2021.686143.

Açkgöz Z, Bayraktar H, Altan Ö (2011). Effects of formic acid administration in the drinking water on performance, intestinal microflora and carcass contamination in male broilers under high ambient temperature.Asian-Aus J. Anim. Sci. 24(1):96–102 . https://dx.doi.org/10.5713/ajas.2011.10195.

Açkgöz Z, Bayraktar H, Altan Ö (2011). Effects of formic acid administration in the drinking water on performance, intestinal microflora and carcass contamination in male broilers under high ambient temperature. Asian-Aus J. Anim. Sci. 24(1):96–102. https://dx.doi.org/10.5713/ajas.2011.10195.

Adil S, Banday MT, Bhat GA., Qureshi SD, Wani SA (2011a). Effect of supplemental organic acids on growth performance and gut microbial population of broiler chicken. Livest. Res. Rural Develop. 23(1): 241-149.

Adil S, Banday T, Ahmad Bhat G, Salahuddin M., Raquib M, Shanaz S (2011b). Response of broiler chicken to dietary supplementation of organic acids. J. Central European Agric. 12(3): 0-0.

Adil S, Banday T, Bhat GA, Mir MS, Rehman M (2010). Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and serum biochemistry of broiler chicken.  Vet. Med. Int. 2010. https://doi.org/10.4061/2010/479485.

Afsharmanesh M, Pourreza J (2005). Effects of calcium, citric acid, ascorbic acid, vitamin D 3 on the efficacy of microbial phytase in broiler starters fed wheat-based diets I. Performance, bone mineralization and ileal digestibility. Int. J. Poult. Sci.

Al-Natour MQ, Alshawabkeh KM (2005). Using Varying Levels of Formic Acid to Limit Growth of Salmonella gallinarum in Contaminated Broiler Feed. Asian-Australasian Journal of Animal Sciences. Asian Australasian Assoc. Anim. Prod. Societ. https://doi.org/10.5713/ajas.2005.390.

AndinoDubón AG (2014). Molecular mechanisms associated with survival of Salmonella enterica in broiler feed are serovar and strain dependent.

Andrews, W (1992). Manual of food quality control, 4. rev. 1: microbiological analysis.

Andrys R, Klecker D, Zeman L, Marecek E (2003). The effect of changed pH values of feed in isophosphoric diets on chicken broiler performance. Czech J. Anim. Sci. 48(5): 197-206.

Antongiovanni, M., Buccioni, A., Petacchi, F., Leeson, S., Minieri, S., Martini, A., Cecchi R (2007). Butyric acid glycerides in the diet of broiler chickens: effects on gut histology and carcass composition. Italian J. Anim. Sci., 6(1): 19-25. https://doi.org/10.4081/ijas.2007.19.

Ao, T., Cantor, A. H., Pescatore, A. J., Ford, M. J., Pierce, J. L., & Dawson, K. A. 2009. Effect of enzyme supplementation and acidification of diets on nutrient digestibility and growth performance of broiler chicks. Poult. Sci. 88(1): 111-117.https://doi.org/10.3382/ps.2008-00191.

Association of Official Analytical Chemists (AOAC).Official method of the Association of Official Analytical Chemists.Vol.1, 16th ed. AOAC International, Arlington, USA.1995.

Atapattu NSBM, Nelligaswatta CJ (2005). Effects of citric acid on the performance and the utilization of phosphorous and crude protein in broiler chickens fed on rice by-products based diets. Int. J. Poult. Sci., 4(12): 990-993.

Bradley, G. L., Savage, T. F., &Timm, K. I.1994. The effects of supplementing diets with Saccharomyces cerevisiae var. boulardii on male poult performance and ileal morphology. Poult. Sci, 73(11): 1766-1770. https://dx.doi.org/10.3382/ps.0731766.

Baghernejad, B (2011). “Application of p-toluenesulfonic Acid (PTSA) in Organic Synthesis”. Curr. Organic Chem. 15 (17). https://dx.doi.org/10.2174/138527211798357074.

Banday, M.T., S. Adil, A.A. Khan and MadeehaUntoo, 2015.A Study on Efficacy of Fumaric Acid Supplementation in Diet of Broiler Chicken. Int. J. Poult. Sci., 14: 589-594.

Biggs, P., &Parsons, C. M.2008. The effects of several organic acids on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. Poultry science, 87(12), 2581-2589. https://doi.org/10.3382/ps.2008-00080.

Blanchard, P. J.2001. Minimum inhibition concentrations for propionic acid and organic acid mixtures against storage fungi.In World Mycotoxin Forum, 2001.

Blank R, Mosenthin R, Sauer WC, 1999.Effect of fumaric acid and dietary buffering capacity on ileal and fecal amino acid digestibilities in early-weaned pigs. J. Anim. Sci. 77:2974–2984.

Boling SD, Douglas MW, Snow JL, Parsons CM, Baker DH (2000). Citric acid does not improve phosphorus utilization in laying hens fed a corn-soybean meal diet. Poult. Sci. 79(9): 1335-1337. https://doi.org/10.1093/ps/79.9.1335.

Brenes A, Viveros A, Arija I (2007). The effect of citric acid and microbial phytase on mineral utilization in broiler chicks. Anim. Feed Sci. Technol. 48(4):469–479.

BROOM L (2015). Organic acids for improving intestinal health of poultry. World’s Poult. Sci. J. 71(4): 630-642. https://dx.doi.org/10.1017/S0043933915002391.

Brzoska F, Śliwiński B, Michalik-Rutkowska O (2013). Effect of dietary acidifier on growth, mortality, post-slaughter parameters and meat composition of broiler chickens/Wpływzakwaszaczadietynamasęciała, śmiertelność, wydajnośćrzeźnąiskładmięsakurczątrzeźnych. Ann. Anim. Sci. 13(1): 85-96. https://dx.doi.org/10.2478/v10220-012-0061-z.

Bureau of Indian Standard (BIS) (1992). Nutrient Requirements for Poultry. Indian Standard (IS): 13574.

Byrd JA, Hargis BM, Caldwell DJ, Bailey RH, Herron KL, McReynolds JL, Kubena LF (2001). Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poult. Sci. 80(3): 278-283. https://doi.org/10.1093/ps/80.3.278.

Byrd JA, Hargis BM, Caldwell DJ, Bailey RH, Herron KL, McReynolds JL, Brewer RL, Anderson RC, Bischoff KM, Callaway TR, Kubena LF (2001). Effect of lactic acid administration in the drinking water during pre-slaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poult. Sci. 80:278–283. https://dx.doi.org/10.1093/ps/80.3.278.

Carpenter C. E., J. V. Smith, J. R. Broadbent (2011) Efficacy of washing meat surfaces with 2% levulinic, acetic, or lactic acid for pathogen decontamination and residual growth inhibition. Meat Sci., 88(2): 256-260

Cave NAG (1978). The influence of non-esterified fatty acids on feeding activity of chicks. Poult. Sci. 57: 1124.

Chaveerach P, Keuzenkamp DA, Lipman LJ, Van Knapen F (2004). Effect of organic acids in drinking water for young broilers on Campylobacter infection, volatile fatty acid production, gut microflora and histological cell changes. Poult. Sci. 83(3):330–334. https://dx.doi.org/10.1093/ps/83.3.330.

Cherrington CA, M. Hinton, GC Mead, I Chopra (1991). Organic acids: Chemistry, antibacterial activity and practical applications. Adv. Microb. Physiol. 32:87–108.

Deng W, Wang Y, Yan N (2016).Production of organic acids from biomass resources. Curr. Opin. Green Sustain. Chem. 2: 54-58. https://doi.org/10.1016/j.cogsc.2016.10.002.

Denli M, Okan F, Celik K (2003). Effect of dietary probiotic, organic acid and antibiotic supplementation to diets on broiler performance and carcass yield. Pak. J. Nutrit., 2: 89-91.

Dhawale A (2005). Better eggshell quality with a gut acidifier. Poult. Int. 44: 18-21.

Dibner JJ, P Buttin (2002). Use of organic acids as a model to study the digestibility, immune response and intestinal morphology of male broilers fed phosphorus deficient diets supplemented with microbial phytase and organic acids. Livest. Sci. 157:506–513.

Diebold G, Eidelsburger U (2006). Acidification of diets as an alternative to antibiotic growth promoters. Antimicrobial growth promoter. The Netherlands: Wageningen Academic Publishers, 311-327.

Ding J, He S, Xiong Y, Liu D, Dai S, Hu H (2020). Effects of Dietary Supplementation of FumaricAcidon Growth Performance, Blood Hematological andBiochemical Profile of Broiler Chickens Exposed toChronic Heat Stress. Brazilian J. Poult. Sci. 22(1): 001-008. https://doi.org/10.1590/1806-9061-2019-1147.

Doerr JA, Attard FA, Doerr EA, Robey WW (1995). Possible anti-fungal effects of hydroxy-methylthio-butanoic acid (HMB). Poult. Sci. 74(Suppl 1): 23.

Doores S (2005). Organic acids. Food Sci. Technol.-New york-marcel dekker-. 145: 91.

Duncan DB (1955). Multiple range and multiple F tests. Biometrics. 11(1): 1-42.

Fascina VB, Sartori JR, Gonzales E, Carvalho FB, Souza IM, Polycarpo GD, Stradiotti AC, Pelícia VC.2012. Phytogenic additives and organic acids in broiler chicken diets. RevistaBrasileira de Zootecnia.41(10):2189-97.

Fayiz M. Reda, Ismail E. Ismail, Adel I. Attia, Ahmed M. Fikry, Eman Khalifa, Mahmoud Alagawan (2021). Use of fumaric acid as a feed additive in quail’s nutrition: its effect on growth rate, carcass, nutrient digestibility, digestive enzymes, blood metabolites, and intestinal microbiota. Poult. Sci. 100(12):101493. https://doi.org/10.1016/j.psj.2021.101493.

Frankel WL, W. Zhang, A Singh, DM Klurfeld, S Don, T Sakata, JL Rombeau (1994). Mediation of the trophic effects of short chain fatty acids on the rat jejunum and colon. Gastroenterology. 106:385–390.

Freitag M (2007). Organic acids and salts promote performance and health in animal husbandry. In: Lückstädt C, editor. Acidifiers in animal nutrition-a guide for feed preservation and acidification to promote animal performance. Nottingham, UK: Nottingham University Press; p. 1–11.

Gao CQ, Shi HQ, Xie WY, Zhao LH, Zhang JY, Ji C, Ma QG (2021). Dietary supplementation with acidifiers improves the growth performance, meat quality and intestinal health of broiler chickens. Anim. Nutrit. 7(3): 762–769. https://doi.org/10.1016/j.aninu.2021.01.005.

Garciá V, Catalá-Gregori P, HernáNdez F, Megiás MD, Madrid J (2007). Effect of formic acid and plant extracts on growth, nutrient digestibility, intestine mucosa morphology, and meat yield of broilers. J. Appl. Poult. Res. 16:555–562. https://dx.doi.org/10.3382/japr.2006-00116 .

Garrido MN, Skjervheim M, Oppegaard H, Sørum H (2004). Acidified litter benefits the intestinal flora balance of broiler chickens. Appl. Environ. Microbiol., 70(9): 5208-5213. https://doi.org/10.1128/AEM.70.9.5208-5213.2004.

Ghazala AA, AM Atta, K Elkloub, MEL Mustafa, RFH Shata (2011). Effect of dietary supplementation of organic acids on performance, nutrients digestibility and health of broiler chicks. Int. J. Poult. Sci. 10(3):176–184.

Gill CO (2009). Effects on the microbiological condition of product of decontaminating treatments routinely applied to carcasses at beef packing plants. J. Food Protect. 72: 1790–1801.

Goldberg I, Rokem JS, Pines O (2006). Organic acids: old metabolites, new themes. J. Chem. Technol. Biotechnol., 81: 1601-1611. https://doi.org/10.1002/jctb.1590

Grashorn MA., R. Gruzauskas A. Dauksiene, A Raceviciute-Stupeliene, Z Zdunczyk, J Juskiewicz, V Slausgalvis (2013). Influence of organic acids supplement to the diet on functioning of the digestive system in laying hens. Arch. Geflügelk, 77: 155-159.

Greig J. D., L Waddell, B. Wilhelm, W. Wilkins, O. Bucher, S. Parker, A. Rajic. (2012). The efficacy of interventions applied during primary processing on contamination of beef carcasses with Escherichia coli: A systematic review-meta analysis of the published research. Food Control., 27: 385- 397.

Gunal M, Yayli G, Kaya O, Karahan N, Sulak O (2006). The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. Int. J. Poult. Sci. 5(2): 149-155.

Hajati H (2018). Application of organic acids in poultry nutrition. Int. J. Avian Wildlife Biol. 3(4):324-9.

Hamed DM, Hassan AMA (2013). Acids supplementation to drinking water and their effects on Japanese quails experimentally challenged with Salmonella enteritidis. Res. Zool. 3(1):15–22.

Hassan HMA, Mohamed MA, Youssef AW, Hassan ER. (2010).  Effect of using organic acids to substitute antibiotic growth promoters on performance and intestinal microflora of broilers. Asian-Aus J. Anim. Sci. 23(10):1348–1353. https://dx.doi.org/10.5713/ajas.2010.10085.

He S, Yin Q, Xiong Y, Liu D, Hu H (2020): Effects of dietary fumaric acid on the growth performance, immune response, relative weight and antioxidant status of immune organs in broilers exposed to chronic heat stress. Czech J. Anim. Sci., 65: 104-113.

HernáNdez F, Garciá V, Madrid J, Orengo J, Catalá P (2006). Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. Br Poult. Sci. 47:50–56. https://dx.doi.org/10.1080/00071660500475574.

Hernandez F, Garcia V, Madrid J, Orengo J, Catalá P, Megias MD (2006). Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. British Poult. Sci. 47(1): 50-56. https://doi.org/10.1080/00071660500475574.

Henry P, Ammerman C, Campbell D, Miles RJPS (1987). Effect of antibiotics on tissue trace mineral concentration and intestinal tract weight of broiler chicks. 66(6): 1014-1018.

Hinton M, Linton AH (1988). Control of salmonella infections in broiler chickens by the acid treatment of their feed. Vet. Rec. 123(16): 416-421. https://dx.doi.org/10.1136/vr.123.16.416.

Hinton M, Linton AH (1988). Control of salmonella infections in broiler chickens by the acid treatment of their feed. Vet. Rec. 123(16): 416-421. https://dx.doi.org/10.1136/vr.123.16.416 

Hofstad MS (1972). Editor, Diseases of Poultry. 6th ed. Ames: The Iowa State University Press, pp. 1176.

Humphery TJ, DG Laning (1988). The vertical transmission of salmonellas and formic acid treatment of chicken feed. A possible strategy for control. Epidemiol. Infect. 100: 43-49.

Humphrey TJ, Lanning DG (1988). The vertical transmission of salmonellas and formic acid treatment of chicken feed: a possible strategy for control. Epidemiol. Infect.  100(1): 43-49.  https://doi.org/10.1017/S0950268800065547.

Hunter PA, Dawson S, French GL, Goossens H, Hawkey PM, Kuijper EJ, Piddock LJ (2010). Antimicrobial-resistant pathogens in animals and man: prescribing, practices and policies. https://doi.org/10.1093/jac/dkp433.

Huyghebaert G (1999). The influence of the addition of organic acid preparations on the zootechnical performances of broiler chickens. Report: CLO-DVV. Institut. Anim. Sci. Health, Lelystad, Netherlands.

Iji PA, Tivey DR (1998). Natural and synthetic oligosaccharides in broiler chicken diets. World’s Poult. Sci. J.  54(2): 129-143. https://doi.org/10.1079/WPS19980010

Islam KMS, Schuhmacher A, Aupperle H, Gropp JM (2008). Fumaric acid in broiler nutrition: a dose titration study and safety aspects. Int. J. Poult. Sci., 7(9): 903-907.

Izat AL, Adams MH, Cabel MC, Colberg M, Reiber MA, Skinner JT,Waldroup PW (1990). Effects of formic acid or calcium formate in feed on performance and microbiological characteristics of broilers. Poult. Sci. 69(11): 1876-1882. https://doi.org/10.3382/ps.0691876.

Izat AL, Adams MH, Cabel MC, Colberg M, Reiber MA, Skinner JT, Waldroup PW (1990a). Effects of formic acid or calcium formate in feed on performance and microbiological characteristics of broilers. Poult. Sci. 69(11): 1876-1882. https://doi.org/10.3382/ps.0691876.

Izat AL, Tidwell NM, Thomas RA, Reiber MA, Adams MH, Colberg M, Waldroup PW (1990b). Effects of a buffered propionic acid in diets on the performance of broiler chickens and on microflora of the intestine and carcass. Poult. Sci. 69(5): 818-826. https://doi.org/10.3382/ps.0690818.

Jones DL (1998). Organic acids in the rhizosphere–a critical review. Plant Soil. 205(1): 25-44. https://doi.org/10.1023/A:1004356007312

Kadim IT, Al-Marzooqi W, Mahgoub O, Al-Jabri A, Al-Waheebi SK (2008). Effect of acetic acid supplementation on egg quality characteristics of commercial laying hens during hot season. Int J. Poult. Sci. 7(10):1015–1021.

Kaniawati S, Skinner JT, Waldroup PW, Izat AL, Colberg M (1992). Effects of feeding organic acids to broilers on performance and Salmonella Colonization of the caeca and/or contamination of the carcass. Poult. Sci. 71 (suppl. 1): 159.

Khattak FM, Acamovic T, Sparks N, Pasha TN, Joiya MH, Hayat Z, Ali Z (2012). Comparative efficacy of different supplements used to reduce heat stress in broilers. Pak. J. Zool. 44(1):31–41.

Lagua, E, Ampode KM (2021). Turmeric powder: potential alternative to antibiotics in broiler chicken diets. J. Anim. Health Prod. 9(3): 243-253.

Leeson S, H Namkung M, Antongiovanni, EH. Lee (2005). Effect of butyric acid on the performance and Carcass yield of broiler chickens. Poult. Sci., 84:1418-1422. (in text Leeson et al., 2005) 1422

Liem A, Pesti GM, Edwards Jr HM (2008). The effect of several organic acids on phytate phosphorus hydrolysis in broiler chicks. Poult. Sci. 87(4): 689-693. https://doi.org/10.3382/ps.2007-00256.

Lillie RD (1965). Histopathological technique and practical histochemistry.3rd ed. McGraw Hill Book Company, New York.pp. 117.

Lückstädt C, Mellor S (2011). 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. Aus. 18:123–130.

Loddi MM, Maraes VMB, Nakaghi ISO, Tucci FM, Hannas M, Ariki JA (2004). Mannan oligosaccharide and organic acids on performance and intestinal morphometric characteristics of broiler chickens. Proceedings of the 20th Annual Symposium.

Lückstädt C (2014). Effects of dietary potassium diformate on growth and gastrointestinal health in weaned piglets in Vietnam. Conference on International Research on Food Security, Natural Resource Management and Rural Development organized by the Czech University of Life Sciences Prague, 2014 Sept 17–19. 

Lückstädt C, Theobald P (2009). Effect of a formic acid-sodium formatepremixture on Salmonella, Campylobacter and further gut microbiota in broilers. In Proceedings and abstracts of the 17th european symposium on poultry nutrition (Vol. 246).

Lückstädt C, Şenköylü N, Akyürek H, Aĝma A (2004). Acidifier--a modern alternative for anti-biotic free feeding in livestock production, with special focus on broiler production. Veterinarijairzootechnika. 27(49).

Lückstädt C (2011). Standards for Acidifiers: Principles for the Use of Organic Acids in Animal Nutrition: Proceedings of the 1st International Acidifier Summit. Nottingham University Press.

Mahdavi AH, Rahmani HR, Pourreza J (2005). Effect of probiotic supplements on egg quality and laying hens performance. Int. J. Poult. Sci. 4:488–492. doi: 10.3923/ijps.2005.488.492.

Makkink C (2001). Acid binding capacity in feedstuffs. Feed Int. 22(10): 24-27.

Martinez-Amezcua C, Parsons CM, Baker DH (2006). Effect of microbial phytase and citric acid on phosphorus bioavailability, apparent metabolizable energy, and amino acid digestibility in distillers dried grains with solubles in chicks. Poult. Sci., 85(3): 470-475. https://doi.org/10.1093/ps/85.3.470.

Mathew AG (1991). Effect of a propionic acid containing feed additives on performance and intestinal microbial fermentation of ten weanling pig. In Proceeding of 5^<th> International symposium on digestive physiology in pigs. Wageningen, Netherlands. 1991.

Mattey M (1992). The production of organic acids. Crit. Rev. Biotechnol., 12(1-2): pp.87-132.

Mikkelsen LL, Vidanarachchi JK, Olnood CG, Bao YM, Selle PH, Choct M (2009). Effect of potassium diformate on growth performance and gut microbiota in broiler chickens challenged with necrotic enteritis. Brit. Poult. Sci., 50(1): 66-75. https://doi.org/10.1080/00071660802613252.

Mikkelsen LL, Vidanarachchi JK, Olnood CG, Bao YM, Selle PH, Choct M. (2009). Effect of potassium diformate on growth performance and gut microbiota in broiler chickens challenged with necrotic enteritis. Br Poult. Sci. 50:66–75. https://dx.doi.org/10.1080/00071660802613252

Moghadam AN, Pourreza J, Samie AH (2006). Effect of different levels of citric acid on calcium and phosphorus efficiencies in broiler chicks. Pak. J. Biolog. Sci., 9(7) 1250-1256.

Mroz Z (2005). Organic acids as potential alternatives to antibiotic growth promoters for pigs. Adv. Pork Prod. 16(1): 169-182.

Nursey I (1997). Control of salmonella. Kraftfutter. 10: 415-422.

Omara F, Aziz SA, El-Sheikh SM, Said MAA (2021). Ascorbic acid attenuated the hepatic parenchymal necrosis induced by azithromycin- etoricoxib interaction in rats. J. Anim. Health Prod. 9(s1): 42-48.

Panda AK, RamaRao SV, Raju MVLN, Shyam GS (2009). Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Aust. J. Anim. Sci. 22(7):1026–1031. https://doi.org/10.5713/ajas.2009.80298

Papatsiros VG, Christodoulopoulos G, Filippopoulos LC (2012). The use of organic acids in monogastric animals (swine and rabbits). J. Cell Anim. Biol., 6(10): 154-159.

Park JH, GH Park, KS Ryu (2009). Effect of feeding organic acid mixture and yeast culture on performance and egg quality of laying hens. Kor. J. Poult. Sci. 29:109–115.

Partanen KH, Mroz Z (1999). Organic acids for performance enhancement in pig diets. Nutrit. Res. Rev.12(1):117‒145.

Paul SK, Halder G, Mondal MK, Samanta G (2007). Effect of organic acid salt on the performance and gut health of broiler chicken. J. Poult. Sci., 44(4): 389-395. https://dx.doi.org/10.2141/jpsa.44.389.

Paul SK, Halder G, Mondal MK, Samanta G (2007). Effect of organic acid salt on the performance and gut health of broiler chicken. J. Poult. Sci. 44:389–395. https://dx.doi.org/10.2141/jpsa.44.389.

Pelicano ERL, Souza PA, Souza HBA, Figueiredo DF, Boiago MM, Carvalho SR, Bordon VF (2005). Intestinal mucosa development in broiler chicken fed natural growth promoters. Braz J. Poult. Sci. 7(4):221–229.

Pelicano ERL, Souza PA., Souza HBA, Figueiredo DF, Boiago MM, Carvalho SR, Bordon VF (2005). Intestinal mucosa development in broiler chickens fed natural growth promoters. Brazilian J. Poult. Sci.,  7: 221-229. https://doi.org/10.1590/S1516-635X2005000400005.

Pinchasov Y, Jensen LS (1989). Effect of short-chain fatty acids on voluntary feed of broiler chicks. Poult. Sci.,  68(12): 1612-1618. https://doi.org/10.3382/ps.0681612

Podolak R. K., J. F. Zayas, C. L. Kastner, D. Y. C. Fung. (1996). Reduction of bacterial populations on vacuum-packaged ground beef patties with fumaric and lactic acids. J. Food Protect. 59: 1037-1040.

Podolsky DK (1993). Regulation of intestinal epithelial proliferation: a few answers, many questions. American J. Physiology-Gastrointest. Liver Physiol., 264(2): G179-G186. https://doi.org/10.1152/ajpgi.1993.264.2.G179.

Quinn PJ, Carter ME, Markey BK, Carter GR (1992). Clinical Veterinary Microbiology. Mosby-year book Europe limited Lynton House. 7-12 Tavistock square, London. pp. 61-65. https://doi.org/10.1111/j.2042-3306.1995.tb03032.x.

Rafacz-Livingston KA, Parsons CM, Jungk RA (2005). The effects of various organic acids on phytate phosphorus utilization in chicks. Poult. Sci., 84(9): 1356-1362. https://doi.org/10.1093/ps/84.9.1356.

Rahman MS, MAR Howlider, M Mahiuddin, MM Rahman (2012). Effect Of Supplementation Of Organic Acids On Laying Performance, Body Fatness And Egg Quality Of Hens. Bangladesh J. Anim. Sci. 37. https://dx.doi.org/10.3329/bjas.v37i2.9884.

Rahmani HR, Speer W (2005). Natural additives influence the performance and humoral immunity of broilers. Int. J. Poult. Sci., 4(9): 713-717.

Ramasubba Reddy V (2004). The Role of Acidifers in Poultry Nutrition. Avitech Tech. Bullet.

Raza M, Biswas A, Mir N, Mandal A (2019). Butyric acid as a promising alternative to antibiotic growth promoters in broiler chicken production. J. Agric. Sci. 157(1): 55-62. https://dx.doi.org/10.1017/S0021859619000212.

Khan SH, Iqbal J (2016). Recent advances in the role of organic acids in poultry nutrition. J. Appl. Anim. Res., 44(1): 359-369.

Ricke SC, DK Dittoe, KE Richardson (2020). Formic Acid as an Antimicrobial for Poultry Production: A Review. Front. Vet. Sci., 03. https://doi.org/10.3389/fvets.2020.00563.

Refaie AM, Abd El-Maged MH, Abd El-Halim HHA, Alghonimy HRH, Shaban SAM (2022). Performance, physiological parameters and egg quality traits of laying hens as affected by dietary supplementation of date palm pollen. J. Anim. Health Prod. 10(1): 21-28.

Ricke SC (2003). Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 82(4): 632-639. https://doi.org/10.1093/ps/82.4.632.

Savage TJPS (1996). The effects of feeding a mannan oligosaccharide on immunoglobulins, plasma IgG and bile IgA, of Wrolstad MW male turkeys. 75: 143-148.

S. Samanta, S. Haldar, T.K. Ghosh (2010). Comparative efficacy of an organic acid blend and bacitracin methylene disalicylate as growth promoters in broiler chickens: effects on performance, gut histology, and small intestinal milieu Vet. Med. Inter: 645150. https://doi.org/10.4061/2010/645150

SA AF, El-Sanhoury MH, El-Mednay NM, Abdel-Azeem F (2008). Thyroid activity, some blood constituents, organs morphology and performance of broiler chicks fed supplemental organic acids. Int. J. Poult. Sci. 7(3): 215-222.

Saeed M, G Abbas, M Alagawanyd, AA Kamboh, ME Abd El-Hack, AF Khafaga, S Chao (2019). Heat Stress Management in Poultry Farms: A comprehensive overview. J. Thermal Biol. 84: 414-425.

Salazar PCR., GV Polycarpo, JC Dadalt, PAP Ribeiro, MFC Burbarelli, VCC Polycarpo, R Albuquerque (2018). Lactic and butyric acids, isolated and associated, as alternatives toavilamycin on the immune response of broiler chickens to Newcastle disease. Jaboticabal. 46(2): 194–198. http://dx.doi.org/10.15361/1984-5529.2018v46n2p194-198.

Salvi PS, Cowles RA (2021). Butyrate and the intestinal epithelium: Modulation of proliferation and inflammation in homeostasis and disease. Cells. 10(7): p.1775.

D Nataraja, V Malathi, JN Sreedhara, Jayanaik, B Kavitha Rani (2020). Effect of Butyric Acid Supplementation on Gut Health in Broiler Chicken. Int. J. Curr. Microbiol. App. Sci. 9(2): 2521-2532.

Sebastian S, Phillip LE, Fellner V, Idziak ES (1996). Comparative assessment of bacterial inoculation and propionic acid treatment of aerobic stability and microbial populations of ensiled high-moisture ear corn. J. Anim. Sci. 74(2): 447-456. https://doi.org/10.2527/1996.742447x.

Selle PH, Huang KH, Muir WI (2004). Effects of potassium diformate inclusion in broiler diets on growth performance and nutrient utilisation. In Proceedings of the 16th Australian Poultry Science Symposium, Sydney, New South Wales, Australia, 9-11 February 2004 (pp. 55-58). Poultry Research Foundation.

Smulikowska S., J Czerwiński, A Mieczkowska (2010). Effect of an organic acid blend and phytase added to a rapeseed cakecontaining diet on performance, intestinal morphology, caecalmicroflora activity, and thyroid status of broiler chickens. J. Anim. Physiol. Nut; 94:15-23.

Sobczak A., K Kozłowski (2016). Effect of dietary supplementation with butyric acid or sodium butyrate on egg production and physiological parameters in laying hens. Europ. Poult. Sci., 80. 2016, https://dx.doi.org/10.1399/eps.2016.122.

Sohail HK, J Iqbal (2016). Recent advances in the role of organic acids in poultry nutrition, J. Appl. Anim. Res. 44:1, 359-369. https://doi.org/10.1080/09712119.2015.1079527.

Soltan M (2008). Effect of Dietary Organic Acid Supplementation on Egg Production, Egg Quality and Some Blood Serum Parameters in Laying Hens. Int. J. Poult. Sci. 7(6): 613-621.  https://doi.org/10.3923/ijps.613-621.

Sugiharto, S., Yudiarti, T., Isroli, I., Widiastuti, E., Wahyuni, H.I., Sartono, T.A., Nurwantoro, N. and Al-Baarri, A.N. 2019. Effect of dietary supplementation of formic acid, butyric acid or their combination on carcass and meat characteristics of broiler chickens. J Indonesian Trop AnimAgric, 44, pp.286-294.

Suryanarayana MVAN, Suresh J, Rajasekhar MV (2006). Organic acids in swine feeding-A Review.Agric. Sci. Res. J. 2:523‒533.

Tappenden KA, McBurney MI (1998). Systemic short-chain fatty acids rapidly alter gastrointestinal structure, function, and expression of early response genes. Dig. Dis. Sci. 43(7): 1526-1536. https://doi.org/10.1023/a:1018819032620.

Teirlynck E, Bjerrum L, Eeckhaut V, Huygebaert G, Pasmans F, Haesebrouck F, Van Immerseel F (2009). The cereal type in feed influences gut wall morphology and intestinal immune cell infiltration in broiler chickens. Brit. J. Nutrit. 102(10): 1453-1461. https://doi.org/10.1017/S0007114509990407.

Thirumeigmanam D, Swain RK, Mohanty SP, Pati PK (2006). Effect of dietary supplementation of organic acids on performance of broiler chicken. Indian J. Anim. Nutrit., 23(1): 34-40.

Tuoying AO (2005). 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, The Graduate School University of Kentucky.

Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L, Pasmans F, Ducatelle R (2006). The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathol.,  35(3): 182-188.https://doi.org/10.1080/03079450600711045.

Veeramani P, Selvan ST, Viswanathan K (2003). Effect of acidic and alkaline drinking water on body weight gain and feed efficiency in commercial broilers. Indian J. Poult. Sci. 38(1): 42-44.

Visek WJ (1978). The mode of growth promotion by antibiotics. J. Anim. Sci. 46(5): 1447-1469. https://doi.org/10.2527/jas1978.4651447x.

Vogt H, Mathes S and Harnisch S. (1982). The effect of organic acids on productivity of broilers. Archiv-fur-Geflugelkunde. 46: 223-227.

Vogt H, Matthes S, Harnisch S (1981). Einfluss organischerSauren auf die Leistungen von Broilern und Legehennen. Archiv fur Geflugelkunde.= European poultry science. Revue de science avicoleeuropeenne.

Waldroup A, Kaniawati S, Mauromoustakos A (1995). Performance characteristics and microbiological aspects of broilers fed diets supplemented with organic acids. J. Food Protect. 58(5): 482-489. https://doi.org/10.4315/0362-028X-58.5.482.

Wang JP, J. S. Yoo, J.H. Lee, T.X. Z, H.D. Jang, H.J Kim, IH Kim (2009). Effects of phenyllactic acid on production performance, egg quality parameters and blood characteristics in laying hens. J. Appl. Poult. Res. 18, 203-209

Xia MS, Hu CH, Xu ZR (2004). Effects of copper-bearing montmorillonite on growth performance, digestive enzyme activities, and intestinal microflora and morphology of male broilers. Poult. Sci. 83(11): 1868-1875. https://doi.org/10.1093/ps/83.11.1868.

Yalcin S, Yalcin S, Sehu A, Sarifakiogullari K. 2000. Yumurtatavugurasyonlarindalaktikasitkullanimininbaziyumurtakaliteözelliklerineetkisi. National Animal Nutrition Congress, Isparta, Turkey. 4–6 September 2000. 600–604.

Yao F, Bai Y, Chen W, An X, Yao K, Sun P, Lin H (2004). Synthesis and characterization of functional L-lactic acid/citric acid oligomer. Euro. Polymer J. 40(8): 1895-1901. https://doi.org/10.1016/j.eurpolymj.2004.04.017.

YE N, Morodi M (2007). Influence of citric acid and microbial phytase on performance and phytate utilization in broiler chicks fed a corn-soybean meal diet.

Yesilbag D, Colpan I (2006). Effects of organic acid supplemented diets on growth performance, egg production and quality and on serum parameters in laying hens.

Youssef A.W., HMA Hassan, HM Ali, MA Mohamed. (2013). Effect of supplementation of probiotics, probiotics and organic acid on layer performance and egg quality. Asian J. Poult. Sci. 7(2):65-74.