Use of Organic Acids as Potential Feed Additives in Poultry Production Текст научной статьи по специальности «Животноводство и молочное дело»

JWPR

Journal of World's Poultry Research

© 2016, Scienceline Publication

J. World Poult. Res. 6(3): 105-116, September 25, 2016

Review, PII: S2322455X1600015-6

License: CC BY 4.0

Use of Organic Acids as Potential Feed Additives in

Poultry Production

Muhammad Waseem Mirza1*, Zaib-Ur-Rehman2 and Nasir Mukhtar2

1Research scientist at NIPH, Harper Adams University, Shropshire, TF10 8NB, United Kingdom 2Department of Poultry Science, Faculty of veterinary and Animal Sciences, PMAS-Arid Agriculture University Rawalpindi, Pakistan

*Corresponding author's Email: wmirza@harper-adams.ac.uk

Received: 05Aug. 2016 Accepted: 02Sep. 2016

ABSTRACT

Historically organic acids (OA) have been used by humans as natural food preservatives and hygiene promoters with regard to the microbial growth and to enhance freshness and shelf-life of edible food items. This characteristic of microbial growth inhibition of OA also makes them suitable replacement to antibiotic growth promoters in poultry. OA are chemically weak acids, which prevent or completely seize the proliferation and colonization of pathogenic bacteria in the intestine of birds. Thus, reducing the competition for the nutrients as well as production of harmful microbial metabolites. This in turn improves bird's performance and enhances the specific and non-specific immunity by improving the bird's intestinal epithelial layer. OA also help improving absorptive capacity of the intestinal cells by improving the crypt-villus structures as well as by improving the digestive secretions, thus influencing a boost in the digestion of proteins, carbohydrates and especially the minerals. This results in enhanced growth rate and feed efficiency in poultry. This comprehensive review about dynamics of OA revealed that this potential feed additive will be used as performance modifier in commercial poultry production, functioning as gut microbial modifier, immune modulator and nutrients digestion enhancer. This review updates the last decade's developments about OA in poultry production.

Key words: Organic acid, Antimicrobial activity, Digestibility, Performance, Poultry

INTRODUCTION

Increased growth rate and improved feed efficiency (Miles et al., 2006) along with prevention of sub clinical diseases are the main reasons why dietary antibiotic growth promoters (AGP) have been practiced

they were allowed to be used as feed additive by the European Union (Adil et al., 2010). Moreover, most of the research during last decade shows that OA are excellent promoters of growth performance and gut

during the last 50 years in poultry production. However, their constant use at low dosage develops resistance in the bacteria (Collignon, 2003) and residues in the animal products.There was a fear of transferring these antibiotic-resistant bacteria to humans via food chain (Dibner and Buttin, 2002), therefore, European Union (EU) banned the use of AGP in animal nutrition in 2006 (European Union, 2003 and 2005). Ban on the use of AGP in poultry feed resulted in a poorer production performances and there was a change in the microbial ecology in gastrointestinal tract of birds. However, Danish industry evidence showed little effects of this ban on the productive performance. This situation therefore, compelled animal nutritionists and researchers to search for other non-therapeutic alternatives for poultry feed such as organic acids (OA) (Panda et al., 2009), plant extracts, (Taylor, 2001) enzymes, probiotics, prebiotics, herbs and essential oils (Islam, 2012). The use of OA and their salts in the poultry production were considered as safe therefore,

health in commercial poultry production (Sohail and Javid, 2016). Therefore, it is important to understand and highlight their importance, impact and mode of action, to be able to maximize the benefits when included in poultry diets.

Organic acids

Any substance that contains the R-COOH group in its structure and has acidic properties is called an Organic Acid (OA) and hence include fatty acid and amino acid. Chemically they are weak acids and contrary to mineral acids they do not dissociate completely in water. The pKa is a logarithmic measure of the acid dissociation constant, the most important property that categorizes the strength and affects the activity of OA. The lower or more negative the number, the stronger and more dissociable the acid. It is important for OA's antimicrobial properties that its pKa value should be in the range of 3-5 (Dibner and Buttin, 2002).Due to this partial dissociation, not allOA's have

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

the ability to influence gut microflora or have antimicrobial properties. OA are short chained acids (C1-C7), consisting of either a simple monocarboxylic acids i.e. formic, acetic, propionic and butyric acids or ones containing carboxylic group at the alpha carbon like tartaric, lactic, malic, and citric acids, which exhibit antimicrobial properties. Acids like fumaric and sorbic acid also have antifungal properties. The OAs and their salts do not exhibit their beneficial effects solely through their antimicrobial activity in feed and GIT of birds but also act as performance enhancers in many ways (Al-Kassi and Mohssen, 2009). These include an improvement in the growth rate through increase in the digestion and absorption of different nutrients, improvement in crypt-villus structure i.e., crypt depth and villus height and width and stimulation of the digestive secretion of different organs.

Antimicrobial activity of organic acids

Major objective of the dietary acidification in poultry is to reduce the pathogenic bacteria (Partanen and Mroz, 1999; Griggs and Jacob, 2005) or increase beneficial bacteria number, both in the feed and by influencing the gut or intestinal environment (Ewing, 2009), so as to support enteric health and growth performance. However, their magnitude of microbial activity in the gut depends on the physiological status of the organism as well as physicochemical characteristics of the environment (Ricke, 2003). Most common bacteria that affect the intestinal health of poultry are Salmonella, Escherichia coli (E. coli), Clostridium, etc. Though a very small effect but these bacteria compete with the host for the nutrients and produce different types of metabolites like ammonia and amines, possibly a result of amino acid deamination, hence leading to reduced growth of the poultry birds. So, by reducing the number of these bacteria, growth rate gets enhanced. OA can provide control over E. coli, Campylobacter and Salmonellachallenges in poultry (Chaveerachet al., 2002 and Heres et al., 2003). Salmonella infection in poultry mainly spreads through contaminated feed (Ao, 2005), therefore, an in-feed addition of OA will prevent the foodborne Salmonella species (Broek et al., 2003). Likewise, OA can be added in the water to keep it free from all type of microorganisms. Albuquerque et al. (1995) reported that out of 136 feed ingredient samples studied for the incidence of Salmonella,19.85% were contaminated with Salmonella. Acid-intolerant species such as E. coli, Campylobacter and Salmonella families are particularly affected by the actions of OA (Al-Kassi and Mohssen, 2009). Hinton et al. (2000) reported that low pH and higher number of lactobacilli lower the incidence of the Salmonella in crop of broiler chicks. Similarly in feed addition of formic acid reduces the

foodborne infections of poultry (Humphrey and Lanning, 1988 and Rouse et al., 1988). The pH value in crop decreased (P<0.05) in the broiler chicken fed OA based diets (Adil et al., 2011). Dietary supplementation of formic and propionic acid laying hens also resulted in lowering of the pH of the crop and gizzard, this lowered pH has also been shown to kill the Salmonella in-vitro (Thompson and Hinton, 1997).As a consequence fowl typhoid can be prevented/controlled (Berchieri and Barrow, 1996). Izat et al. (1990) documented that dietary acidification with buffered propionic acid lessen the number of E. coli in the small intestine. A mixture of OA significantly lowers the total bacterial count especially gram negative bacteria in broilers (Gunal et al., 2006). The RCOO- anions produced from OA can hinder bacterial genetic regulation i.e., DNA and protein synthesis. Van Immerseel et al. (2006) reported that at low dose butyric acid can suppress genes responsible for the Salmonella invasion. In an in-vitro study Entani et al. (1998) reported that a media containing 0.1 percent acetic acid inhibited the growth of 17 strains of the bacteria including Salmonella typhimurium and eight strains of E. coli. Adil et al. (2011) reported addition of OA to the diets of broiler chicken significantly decreased (P<0.05) the caecal viablecoliform counts compared to the unsupplemented group. Butyric acid supplementation decreases the colonization of salmonella in the liver and spleen in broilers (Fernández-Rubio et al., 2009). Maribo et al. (2000a) found that benzoic acid supplementation in the feed of pigs resulted in significantly lower counts of lactic acid bacteria, lactobacilli, coliform and yeast throughout the entire GIT.

Mycotoxinsthat are the metabolites of fungi are the major threat to the poultry industry as these suppress the immune system; reduces the dietary energy contents as well as causing poor feed conversion and less growth rate etc. A variety of OA such as acetic acid, lactic acid, propionic acid, or blends of acids are used to help control mold contamination (Higgins and Brinkhaus, 1999 and Santin, 2010). For the in-vitro assay, paper discs soaked in a spore solution were placed on the surface of agar plates containing increasing concentrations of the respective OA. In-vitro efficacy of propionic, acetic, lactic, undecylenic, butyric, valeric, benzoic, and sorbic acid against the Aspergillus spp., Geotrichum spp., Mucor spp, Fusarium spp., Penicillium spp., and Scopulariopsis spp. indicated that mold inhibiting property of the valeric acid is highest, followed by propionic acid and butyric acid. These three acids completely inhibit the growth of above mentioned mold at the concentrations of not higher than 0.35%. All the other OA showed fewer mold inhibiting activity and the least activity was

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

shown by the lactic acid. Fusarium was the most susceptible mold when comparing the efficacy of different OA on different molds (Higgins and Brinkhaus, 1999). Propionic acid and butyric acid with effective inclusion rates of 0.1% and 0.2% were equal in their efficacy to inhibit Aspergillus spp. and Fusarium spp., respectively. Maribo et al. (2000b) compared bactericidal activities of six different acids in the stomach and small intestine of pigs against coliforms. The order of bactericidal activities of different OA were as follows from higher to lower order: benzoic acid >fumaric acid > lactic acid > butyric acid > formic acid > propionic acid.

Antimicrobial activity of OA is highly affected by the surrounding pH as pH affects the dissociation of the OA (Cherrington, 1991). When pH is low, ionization of the OA will also be less. Undissociated forms of OA are lipophilic and can diffuse across cell membranes of bacteria and fungi (Partanen, 2001). Once internalized into the more alkaline pH of the cell cytoplasma they dissociate quickly into their constituent ions resulting in lowering of the pH (Young and Foegeding, 1993) and as a consequence disrupting the nutrient transport system and enzymatic reactions (Cherrington, 1991). Concentration of the hydrogen ions due to dissociation

of the acids increases and bacteria try to pump out these protons (hydrogen ions) from the cell. This process requires energy, so the availability of energy for the proliferation lessens, resulting in bacteriostasis (Luckstadt and Mellor, 2011; Suiryanrayna and Ramana, 2015). This direct antimicrobial activity makes OA an excellent choice as feed and food preservatives as well as hygiene promoters.

Coccidiosis, an important manage mental disease of poultry, causing more than $3 billion worth of economic losses to the world poultry industry annually (Dalloul and Lillehoj, 2006) is caused by the Emeria; a genus of protzoal parasite. Abbas et al. (2011) studied the anticoccidal effects of acetic acid against the Eimeriatenella by using 1, 2 and 3 percent acetic acid; and 125 ppm amproliumin drinking water. Results showed that acetic acid lowered the oocyte score, lesion score and mortality percentage in broilers. These effects were more prominent at 3%level of acetic acid but there was no difference between 3% acetic acid and amprolium in preventing the coccidiosis. Further studies are necessary in this regard for understanding the anticoccidial effects of other OA. Microbial growth inhibitory properties of some OA are presented in table 1 and table 2.

Table 1. The inhibitory effect of some organic acids used in animal nutrition on microbial growth.

Organic acid

Properties1

Molecular formula

Acid dissociation constant (pKa)

Growth inhibitory

Bacteria

Yeast

Mould

Formic acid Lactic acid Acetic acid Propionic acid Citric acid Sorbic acid Benzoic acid

HCOOH

CH3CHOHCOOH

CH3COOH

CH3CH2COOH

C3H5O(COOH)

C6H8O2

C6H5COOH

3.75

3.86

4.76

4.87 3.1G-5.4G

4.7б 4.2G

++++ + ++ ++

n.a.

+++

+++

+++ +++

n.a.

++++

++++

+++ +++

n.a.

++++

++++

1Adapted from Pölönen and Wamberg (2007); 2adapted from Lassén (2007)

Table 2. Effects of different organic acids on various types of bacteria.

Organic Acid Bacteria Sample tested Effect Reference

Butyric acid Salmonella enteritidis Caecal colonization Decreased total count Van Immerseel et al. (2GG4)

Formic acid Salmonella Cloacal swabs and content Not detected Hinton et al. (1985)

Formic, propionic and acetic acid Campylobacter Boiler Feed Decrease total count Chaveerach et al. (2GG2)

Buffered propionic acid Escherichia coli Boiler Feed Decreased the count Izat et al. (199G)

Butyric acid Escherichia coli Caecum, small intestine and crop Decreased the count Panda et al. (2GG9)

Organic acid mixture Coliform Ileum and caecum Decreased the count Pirgozliev et al. (2GG8)

Malic acid Escherichia coli Intestine Decreased the count Moharrery and Mahzonieh (2GG5)

+

+

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

б(3): 1G5-116.

Table 3. Effectof different organic acids on the gastrointestinal tract of monogastric animals.

Organic Acid Route Effect on Intestine Reference

Butyric acid Feed Increased the villus height Adil et al. (2010)

Formic acid Feed Increased the villus height and crypt depth Garcia et al. (2007)

Citric acid Feed Lowered the pH of digesta and gastrointestinal tract Radcliffe et al. (1998)

Fumaric acid Feed Increased the villus height Adil et al. (2010)

Lactic acid Feed Increased the villus height Adil et al. (2010)

Butyric acid Feed Lowered the pH of crop and small intestine Panda et al. (2009)

Effect of organic acids on gastrointestinal tract

Being the major organ responsible for nutrient digestive and absorptive phase, gastrointestinal tract plays a vital role in the chicken growth (Amit-Romach et al., 2004). It is also the largest reservoir of commensal bacteria and other microbes in bird's body. Therefore, epithelium of the intestine is the natural obstacle to the bacteria and toxic substances entering the body. Different pathogens, chemical toxins and stress conditions alter the permeability of this natural defense (Pelicano et al., 2005), by shortening of villus height and extension of intestinal crypt resulting in lower villi height to crypt depth ratio (Mista et al., 2010), aiding the invasion of pathogens and leading to inflammatory processes at the intestinal mucosa (Podolsky, 1993). This subsequently leads to increased cell turn over, decrease in villus height, and lowering of the digestive and absorptive processes (Visek, 1978). Dietary inclusion of organic acids are known to have strong antibacterial properties and beneficial effects on intestinal acidity and histomorphology, which are imperative to support enteric health and growth performance of poultry (Geyra et al., 2001 and Loddi et al., 2004). Evident from Adil et al. (2010) and Cengiz et al. (2012) study who reported that dietary inclusion of OA in broiler diets resulted in an increase in the villus height. Mista et al. (2010) reported that these histopathological changes in the small intestine can be averted through the use of short chain fatty acids; mainlyacetate, propionate and butyrate in mice. Similarly Fukunaga et al. (2003) while working on rats reported that short chain fatty acids can accelerate gut epithelial cell proliferation, thereby increasing intestinal tissue weight and resulting in changes in mucosal morphology. Effect of different OA on the gastrointestinal tract is presented in Table 3.

The proposed mode of action of OA is related to the reduction of intestinal pH (Waldroup et al., 1995), which might be followed by alterations in the intestinal ecosystem (Canibe et al., 2001).For example butyric acid supplementation of broilers diets @ 0.2, 0.4, and 0.6 percent, significantly decreased the pH of crop, proventriculus and gizzard as compared to control and furazolidone group, maximum reduction in the pH was recorded at 0.4 and 0.6% butyrate compared with 0.2% butyrate (Panda et al., 2009). Eventhough inclusion of 0.4% and 0.8% buffered propionic acid in broiler diets resulted in decreased total number of coliforms and E. coli in the small intestine of the bird however, it had no

effect on intestinal pH (Izat et al., 1990). Likewise, acetic lactic and citric acid does not affect the pH of different intestinal segments (Abdel-Fattah et al., 2008).

OA salts such as ammonium formate and calcium propionate at the dose rate of 3 mg/kg diet can significantly improve intestinal villus height (Paul et al., 2007).Likewise, dietary organic acid in broilers at the age of 42 d resulted in a significant increase in villus width, height and area of the duodenum, jejunum and ileum region (Kum et al., 2010).

Short chain fatty acids are also believed to cause an increase in the plasma glucagon-like peptide 2 and ileal pro-glucagon mRNA, glucose trans-porter expression and protein expression, which are all signals that they can potentially mediate gut epithelial cell proliferation (Tappenden and McBurney, 1998).

Effect of organic acids on immunity

Dietary OA play an important contributory role in the immune status of the bird. Reduction of subclinical infections (Humphrey and Lanning, 1988) and stimulation of the growth of beneficial bacteria may contribute to increased nutrient digestibility and a reduction in nutrient demand by the gut-associated immune tissue and microorganisms (Dibner and Buttin, 2002).

The immune mechanisms in birds are fairly similar with the mammals and are directly influenced by genetic, physiological, nutritional, and environmental factors (Sharma, 2003). The immune system of bird is complex and is composed of several cells and soluble factors that must work together to produce a protective immune response. Major constituents of the avian immune system are the lymphoid organs. Thymus and Bursa of fabricius are of utmost importance because these are involved in the development and differentiation of the T- lymphocytes and B-lymphocytes respectively (Qureshiet al., 1998). Functional immune cells leave the primary lymphoid organs and populate secondary lymphoid organs. Secondary lymphoid organs include spleen, gut-associated lymphoid tissues, gland of Harder, bone marrow and bronchial-associated lymphoid tissues (Sharma, 2003).

Citric acid supplementation enhances the density of lymphocytes in the lymphoid organs, so enhances the non-specific immunity (Chowdhuryet al., 2009 and Haque et al., 2010). Birds having the greater density of lymphocytes have stronger immune status to combat

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

antigens (Khan et al. 2008). Wang et al., (2009) found that the dietary supplementation of phenylacetic acid increase the lymphocyte percentage in a short duration in layers. Organic acid supplementation causes hyperthyroidism and peripheral conversion of thyroxin (T4) to triiodothyronine (T3) which means that these birds have better immune competence and bursa growth (Abdel-Fattah et al., 2008). However, erythrocyte, leukocyte, eosinophil, heterophil and lymphocyte are not influenced by OA (Khosravi et al., 2010). Citric acid supplementation increases the bioavailability of Zn from the soybean meal in poultry (Boling et al., 2000b), a metal known for its immune enhancing properties (Kidd et al., 1996).

Dietary supplementation with acetic and lactic acid increases the serum globulin and decreases the albumin to globulin ratio (Rahmani et al., 2005; Abdel-Fattah et al., 2008). Globulin is a source of antibody production, so its serum level is a good indicator of immune responses and consequently better disease resistance (Griminger and Scanes, 1986). Das et al., (2011) and Houshmand et al., (2012) reported an increased antibody titer against Newcastle disease in broilers by dietary supplementation of OA.

Effect of organic acid on the nutrient digestibility

Protein and energy are the major factors influencing the performance of birds. Depending upon the regional location, protein in poultry diet can be supplied by animal and/or vegetable sources. Amongst vegetable protein sources, soybean meal remains the priority of animal nutritionists. However, there is a downside to it since it contains major anti-nutritional factors for poultry e.g., galacto-oligosaacharides, lectins and trypsin inhibitors; the major anti-nutritional factors present in soybean meal (Huisman and Jansman, 1991). Digestion of the protein in chicks is badly affected by the undigested galacto-oligosaacharides (Gdala et al., 1997) due to absence of a-1,6-galactosidase(Gitzelmann and Auricchio, 1965). Ao (2005) studied in-vitro effect of citric acid on the release of reducing sugar and a-amino nitrogen from soybean meal having different levels of protease and a-galactosidase. Results indicated that citric acid increases activity of both the exogenous galactosidase enzymes, thus enhancing the liberation of a-amino nitrogen and reducing sugars. Li et al. (1998) in an experiment using citric acid addition to the phytase supplemented swine diets reported a non significant improvement in dry matter, nitrogen, phosphorus and calcium digestibility. While other researcher (Dibner and Buttin, 2002; Omogbenigun et al., 2003; Suiryanrayna and Ramana, 2015) reported that organic acid supplementation in simple stomach animal diets resulted in an improved protein digestibility and energy availability by reducing microbial competition with the host for nutrients, endogenous nitrogen losses and production of ammonia. As OA increased the digestion of the protein, this consequently reduces the emission of ammonia and sulfur containing gases from the poultry house.

It is thought that reduction in the pH of digestadue to organic acid supplementation may increases the pepsin activity (Afsharmanesh and Porreza, 2005), resulting in enhanced protein digestibility (Gauthier, 2002).Pepsin proteolysis the proteins, thus producing the peptides which act as a strong stimulant for the release of hormones including gastrin and cholecystokinin (Hersey, 1987).These hormones then acts on pancreatic cells signaling them to release digestive enzymes. OA also act by increasing pancreatic secretions resulting in enhanced production of pancreatic juice (Smantha et al., 2009).As a consequence higher concentrations of trypsinogen, chymotrypsinogen A, chymotrypsinogen B, procarboxypeptidase A and procarboxypeptidase B are produced, which then lead to increased protein digestion (Kirchgessner and Roth 1982; Afsharmanesh and Porreza, 2005). Hume et al. (1993) studied the metabolism of propionic acid and found that 75% of this acid is used as energy source. Likewise Runho et al. (1997) reported improved metabolisable energy contents of broiler diets due fumaric acid supplementation.This proposes a correlation between energy levels and OA.

Thyroid hormones (Tri-iodothyronine) play a major role in regulating the oxidative metabolism in poultry. Any marked change in thyroid function (hypothyroidism or hyperthyroidism) will result in altered metabolic rate (Whittow, 2000). Abdel-Fattah et al., (2008) studied the effects of dietary organic acidification in broiler chicks using variable doses i.e., 1.5 and 3%, of lactic, citric and acetic acid to evaluate the effects on thyroid hormones and reported a significantly elevated serum Triiodothyronine (T3) concentration of organic acid fed broilers however, T4 levels were not significantly affected.

Minerals are crucial for normal physiological, structural and catalytic functioning of the body, (Underwood and Suttle, 1999) and therefore, must be supplied through feed. Minerals represent about 3.5% of the total body composition, of which 46% is calcium (Ca), 29% is phosphorus (P) and 24% included potassium (K), Sulphur (S), sodium (Na), chlorine (Cl) and magnesium (Mg). Minerals, especially Ca and P help to build bones and make them strong and rigid. Trace levels of iodine (I), iron (Fe), manganese (Mn) and zinc (Zn) are also included in the dietary mineral supplements to the poultry. OA reportedly increase the digestion of minerals in poultry. Citric acid (40 to 60 g/kg of diet) is very efficacious in improving P utilization in chickens fed on maize soybean meal diets and reduced the available phosphorus requirement by approximately 1 g/kg diet (Boling et al., 2000b). Boling et al. (2000a) also reported that the dietary citric acid supplementation increases the bioavailability of Zn to the chicks. Citric acid supplementation also increases the retention of Ca, P and Zn, thereby increased their levels in plasma (Brenes et al., 2003). Likewise acetic acid, citric acid and lactic acid increased the serum Ca and P (Abdel-Fattah et al., 2008). Adil et al., (2010) used butyric acid, fumaric acid and lactic acid in broiler diets and reported a significant increase in the serum concentration of Ca and P. Dietary supplementation of

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

OA resulted in chelation of anions of OA with the minerals making them less reactive with vitamins and more bioavailable to the birds (Li et al., 1998). There are many factors which affect the bone development e.g. genotype, age of bird, dietary Ca and P level, dietary vitamin D3, dietary fiber content and type of feed ingredients. Monogastric animals consume diets composed mostly of oilseed and cereal grains that contain high level of P present in the form of phytic acid or phytate. The P in this form is generally unavailable to poultry due to low phytase activity found in the digestive tract (Cromwell, 1992). Many studies showed that OA can increase phytate P utilisation by poultry (Boling-Frankenbach et al., 2001 and Brenes et al., 2003). Maximum activity of microbial phytasecould be reached at lower pH values, thus it could be achieved by adding OA in the diet. Benzoic acid supplementation increase the uptake of the Ca by 0.85 g per day, retention of P by 0.74 g day, retention of K by 0.77 g day and plasma levels of the P in growing pigs (Sauer et al., 2009).

Pirgozliev et al. (2008) reported that birds fed organic acid supplemented diets excreted less mucin (measured as sialic acid (SA)), an indicator of endogenous losses, than birds fed supplemented diets. Increased concentration of SA in digesta or excreta is often connected to gut health problems (Reutter et al., 1982), thus dietary organic acid supplementation improves the gut health of birds.

Bone ash is the direct indicator of mineral deposition and bone strength. Citric acid supplementation at the rate of 6% to the broiler diet resulted in an increased bone ash of up to 43% compared to the groups fed non-supplemented diets (Boling et al., 2000b). Shohl (1937) observed a 61% increase in femur ash when rats consumed Ca and P deficient diets supplemented with citric acid/sodium citrate. Perhaps citric acid, a strong chelator of Ca, removes Ca from or decreases Ca binding to the phytate molecule, thus making it less stable and more susceptible to endogenous phytase.

Effect of organic acids on performance and profitability of poultry

The effects of OA on performance are not consistent for the poultry. As stated before quoting Ricke (2003), the magnitude of the organic acid response varies due to several reasons. OA increase the average live weight, daily gain (BWG), daily feed consumption and improves the feed conversion ratio (FCR) (Al-Kassi and Mohssen, 2009). Fumaric acid significantly increases the BWG (Skinner et al., 1991) at the rate of 0.5% and 1.0% without affecting feed in take in broilers and layers. Likewise, Patten and Waldroup, (1988) recorded a higher BWG in broilers with no effect on feed utilization when fed fumaric acid supplemented diets. Adil et al. (2011) reported that dietary supplementation with the butyric acid, fumaric acid and lactic acid at the 2 and 3% level each; resulted in higher final live BWG, improved FCR in broilers. Vogt et al. (1982) studied malic, sorbic, and tartaric acids (0.5 to 2%) in broilers and reported increase in BWG, with optimal levels of 1.12 and 0.33% for sorbic

and tartaric acids, respectively and improved FCR. Izat et al. (1990) reported that formic acid, calcium formate and buffered propionic acid did not affect the feed utilization. Panda et al. (2009) studied the effect of butyric acid supplementation in broiler ration at the dose level of 0.2, 0.4 and 0.6 percent and documented improved BWG, FCR and a decrease in the weight and percentage of abdominal fat. Butyric acid was as much effective as furazolidone. Similarly body weight and FCR significantly improved by using 2% lactic acid in broiler diet (Versteegh and Jongbloed, 1999). Buffered propionic acid significantly improved the dressing percentage in female broilers and reduced abdominal fat in males at 49 days of age (Izat et al., 1990). Likewise Patten and Waldroup, (1988) suggested an increase in broiler production profitability through increased BWG when dietary supplementation of OA was adopted.

Contrary to the above findings Brown and Southern (1985) found that chick performance is not affected by the supplementation of citric acid and ascorbic acid. Supplementation of propionic acid depresses the feed intake and growth performance but similar results are not reported by the use of lactic acid (Cave, 1984). Though lacking any suggested reason for these effects, Alcicek et al. (2004) reported that dietary supplementation of the organic acid does not affect the feed intake and FCR at 21 and 42 day of age in broilers. Citric acid addition in the broiler diets does not have any significant effect on egg production, egg mass, egg size, feed efficiency, specific gravity of egg and body weight of laying hens (Boling et al., 2000a).

Meat preservation

Consumer interests regarding natural and certified organic foods are increasing. These consumer preferences increased the demand for bio-preservation of the food. OA are one of the best food preservatives(Ewing, 2009). Contaminated poultry meat causes the food borne diseases in humans. More than 76 million citizens in USA became ill by ingesting food especially meat products contaminated with pathogenic bacteria (Mead et al., 1999) which resulted in 1600 deaths (Callaway et al., 2003). Short chain OA are commonly used food preservatives and there is an increasing trend of bio-preservation of food in European countries as these can be used safely without creating residual effects. Lactic or acetic acid reduced the potential of Campylobacter in carcass or meat (Cudjoe and Kapperud, 1991). Addition of formic and propionic acid in the broiler feed causes sub-lethal damage of Salmonella resulting in the incomplete colonization (Thompson and Hinton, 1997). Poultry meat is preserved in order to prevent contamination, as contaminated poultry meat cause many foodborne diseases in humans (caused by microorganisms such as E. coli, Clostritdium perfringens, Clostridium botulinum, Campylobacter jejunietc.). Some fungi like Aspergillusflavus and Aspergillus paraciticus also produce different type of diseases by producing toxins (Prange et al., 2005). Out of these, Salmonella is a major foodborne pathogen associated with poultry meat because fecal material and dirt from feathers and the

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

hide, as well as dirt of processing equipments can contaminate the carcasses during slaughtering and packaging operations. Due to high pH (5.5-6.5), water activity (0.98-0.99) and enriched nutrient profile, fresh poultry meat is highly perishable and provide favorable environment for growth of food contaminating microorganisms (Acuf, 2005). Salmonella gallinarum and Salmonella enteritidis are frequently found in poultry and poultry products but rarely cause illness in humans (Braden, 2006). Salmonella typhimuriumis the most common serotype associated with laboratory confirmed illness cases (CDC, 2009). Therefore, in this scenario OA can be used as potential hygiene promoters, where they lower the pH and also act as a complexing agent for ions, thereby inhibiting microbial growth (Ewing, 2009).

Environmental and economic challenges of using organic acid in poultry

All in all the usage of OA on the basis of above mentioned properties not only makes them a good choice for poultry production but also ensures a lower biological, environmental and economic overhead compared with other available supplements. For example enhanced nutrient digestibility will have nutrient sparing effect which along with better production performance will also lower the losses, therefore reducing the risk of environmental pollutionfrom animal production (Luckstadt and Mellor, 2011). This is particularly true for a reduction in nitrogen and mineral related environmental issues from poultry facilities (Dibner and Buttin, 2002; Riemensperger, 2012). Therefore their usage in poultry production is economically justifiable.

Possible adverse effects of using organic acid

However, there were few concern raised by the scientists regarding the adverse effects of OA supplementation on organoleptic properties (the appearance and texture) of poultry meat (Dickens and Whittemore, 1994 and Dickens et al., 1994). There is also an environmental concern for the disposal of waste water from poultry units using OA supplementation along with a fear of the emergence of acid-resistant pathogens (Fabrizio et al., 2002). Gabert and Sauer (1995) noted a reduction in ileal digestibility of both CP and amino acid when diet was supplemented with fumaric acid in growing pigs.

CONCLUSION

OA inhibit the growth of pathogenic bacteria, especially zoonotic bacteria, e.g. Campylobacter, E. coli and Salmonella, in the feed and gastrointestinal tract of poultry which is of great importance with respect to poultry health. They also cause reduction in the microbial load on poultry meat products. OA improve the mucosa growth, villus height and width, crypt depth and decrease the intestinal pH. They also boost the immune system and the digestibility of protein, carbohydrate and minerals, thus enhancing the growth performance of poultry. Therefore, OA can be

meritoriously used as a replacer of the antibiotic growth promoters in poultry.

Competing Interests

The authors declare that they have no competing

interests.

REFERENCES

Abbas RZ, Munawar SH, Manzoor Z, Iqbal Z, Khan MN, Saleemi MK, Zia MA and Yousaf A (2011). Anticoccidial effects of acetic acid on performance and pathogenic parameters in broiler chickens challenged with Eimeria Tenella. PesquisaVeterináriaBrasileira,31(2): 99-103.

Abdel-Fattah SA, Ei-Sanhoury MH, Ei-Mednay NM and Abdul-Azeem F (2008). Thyroid activity of broiler chicks fed supplemental organic acid. International Journal of Poultry Science, 7(3): 215-222.

Acuff GR (2005). Chemical decontamination strategies for meat.In J. N. Sofos (Ed.), improving the safety of fresh meat (pp. 350-363). Boca Raton, FL: (CRC Press).

Adil S, Banday MT, Bhat GA, Qureshi SD and Wani SA (2011). Effect of supplemental organic acids on growth performance and gut microbial population of broiler chicken. Livestock Research for Rural Development, 23(1): 1-8.

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

Afsharmanesh M and Porreza J (2005). Effects of calcium, citric acid, ascorbic acid, vitamin D on the efficacy of microbial phytase in broiler starters fed wheat-based diets: performance, bone mineralization and ileal digestibility. International Journal of Poultry Science, 4 (6): 418-424.

Albuquerque R, Ito NMK and Miyaji CI (1995).Ocorrencia de salmonella semin gredientes, ragoes e "swabs" de pó colhidos em fábricas industriais de ragoes. In: CONFERÉNCIA APINCO'95 DE CIÉNCIA E TECNOLOGIA AVÍCOLAS, Curitiba, 1995. Trabalhos de pesquisa. Campinas: FACTA, pp. 161-162.

Alcicek A, Bozkurt M and CABUK M (2004). The effect of a mixture of herbal essential oils, an organic acid or a probiotic on broiler performance. South African Journal of Animal Science, 34(4): 217-222.

Al-Kassi AG and Mohssen MA (2009). Comparative study between single organic acid effect and synergistic organic acid effect on broiler performance. Pakistan Journal of Nutrition, 8(6): 896-899.

Amit-Romach E, Sklan D and Uni Z (2004). Microflora ecology of the chicken intestine using 16S

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

ribosomal DNA primers. Poultry Science, 83(7): 1093-1098.

Ao T (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, University of Kentucky.

Berchieri AJR and Barrow PA (1996). Reduction in incidence of experimental fowl typhoid by incorporation of a commercial formic acid preparation into poultry feed. Poultry Science, 75(3): 339-341.

Boling S, Douglas M, Snow J, Parsons C and Baker D (2000a). Citric acid does not improve phosphorus utilization in laying hens fed a corn-soybean meal diet. Poultry Science, 79(9): 1335-1337.

Boling S, Webel D, Mavromichalis I, Parsons C and Baker D (2000b). The effects of citric acid on phytate-phosphorus utilization in young chicks and pigs. Journal of Animal Science,78(3): 682689.

Boling-Frankenbach S, Snow J, Parsons C and Baker D (2001). The effect of citric acid on the calcium and phosphorus requirements of chicks fed corn-soybean meal diets. Poultry Science, 80(6): 783788.

Braden CR (2006). Salmonella enterica serotype Enteritidis and eggs: A national epidemic in the United States. Food Safety,43(4): 512-517.

Brenes A, Viveros A, Arija I, Centeno C, Pizarro M and Bravo C (2003). The effect of citric acid and microbial phytase on mineral utilization in broiler chicks. Animal Feed Science and Technology, 110(1): 201-219.

Broek GVD, Bergh MVD, Ebbinge B, Selko BV and Tilburg (2003). Clean drinking water during production by use of organic acids. World Poultry, 19: 34-37.

Brown DR and Southern LL (1985). Effect of citric and ascorbic acids on performance and intestinal pH of chicks. Poultry Science, 64(7): 1399-1401.

Callaway TR, Anderson RC, Edrington, TS, Elder RO, Genovese KJ, Bischoff KM, Poole TL, Jung YS, Harvey RB and Nisbet DJ (2003). Pre-slaughter intervention strategies to reduce food-borne pathogens in food animals. Journal of Animal Science, 81(14): 17-23.

Canibe N, Engberg RM and Jensen BB (2001).An overview of the effect of organic acids on gut flora and gut health.Proceeding of the Workshop: Alternatives to Feed Antibioticsand Coccidiostats in Pigs and Poultry (AFAC), Norfa network, October 13-16, Oslo, Norway.

Cave NAG (1984). Effect of dietary propionic and lactic acids on feed intake by chicks. Poultry Science,63(1): 131-134.

Centers for Disease Control and Prevention (CDC) (2009). Preliminary FoodNet Data on the incidence of infection with pathogens transmitted commonly through food—10 states, 2008. Morbidity and Mortality Weekly Report59(14): 333-337.

Cengiz O, Koksal BH, Tatli O, Sevim O, Avci H, Epikmen T, Beyaz D, Buyukyoruk S, Boyacioglu

M, Uner A and Onol AG (2012). Influence of dietary organic acid blend supplementation and interaction with delayed feed access after hatch on broiler growth performance and intestinal health. VeterinarniMedicina, 57(10): 515-528.

Chaveerach P, Keuzenkamp D, Urlings H, Lipman L and Vanknapen F (2002). In vitro study on the effect of organic acids on Campylobacter jejuni/coli populations in mixtures of water and feed. Poultry Science, 81(5): 621-628.

Cherrington CA, Hinton M, Mead GC and Chopra I (1991). Organic acids: chemistry, anti-bacterial activity and practical applications. Advance Microbiology and Physiology, 32: 87-107.

Chowdhury R, Islam KMS, Khan MJ, Karim MR, Haque MN, Khatun M and Pesti GM (2009). Effect of citric acid, avilamycin and their combination on the performance, tibia ash and immune status of broiler chicks. Poultry Science, 88(8): 1616-1622.

Collignon P (2003). A review-the use of antibiotics in food production animals-does this cause problems in human health. 9th Biennial Conference of the Australasian Pig Science Association (inc.) (APSA), Fremantle, Western Australia, pp. 73-80.

Cromwell GL (1992). The biological availability of phosphorus for pigs. Pig News Information,13: 75-78.

Cudjoe KS and Kapperud G (1991). The effect of lactic acid spray on Campylobacter jejuni inoculated onto poultry carcasses. Acta Veterinaria Scandinavica, 32(4): 491-498.

Dalloul RA and Lillehoj HS (2006). Poultry coccidiosis: Recent advancements in control measures and vaccine development. Expert Review of Vaccines, 5(1): 143-163.

Das SK, Islam KMS and Islam MA (2011). Efficacy of citric acid in diet contains low levels of protein and energy on the performance and immunity of broiler.7th International Poultry Show and Seminar 2011 World's Poultry Science Association- Bangladesh Branch, 25-27 March, 2011, Dhaka, Bangladesh, pp. 318-324.

Dibner JJ and Buttin P (2002). Use of organic acid as a model to study the impact of gut microflora on nutrition and metabolism. Journal of Applied Poultry Research,11(4):453-63.

Dickens JA, Lyon BG, Whittemore AD and Lyon CE (1994). The effect of an acetic acid dip on carcass appearance, microbiological quality, and cooked breast meat texture and flavor. Poultry Science, 73(4): 576-581.

Dickens JA and Whittemore AD (1994). The effect of acetic acid and air injection on appearance, moisture pick-up, microbiological quality, and Salmonella incidence on processed poultry carcasses. Poultry Science, 73(4): 582-586

Economic and Social Committee of the European Union (2005). Laying down requirements for feed hygiene: regulation (EC) No 183/2005 of the European parliament and of the council. 453-463.

European Union (2003). Regulation (EC) No 1831/2003 of the European Parliament and of the

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

Council of 22 September 2003 on additives for use in animal nutrition. Off. J. Eur. Union L 268:29-43.

Ewing Wesley N (2009).The living gut. Nottingham University Press, pp. 143-148.

Entani E, Asai M, Tsujihata S, Tsukamoto Y and Ohta M (1998). Antibacterial action of vinegar against food-borne pathogenic bacteria including Escherichi coli O157:H7. Journal of Food Protection, 61(8): 953-959.

Fabrizio KA, Sharma RR, Demirci A and Cutter CN (2002).Comparison of Electrolyzed Oxidizing Water with Various Antimicrobial Interventions to Reduce Salmonella Species on Poultry. Poultry Science, 81(10):1598-1605.

Fernndez-Rubio C, Ordonez C, Abad-Gonzalez J, Garcia-Gallego A, Honrubia MP, Mallo JJ and Balana-Fouce R (2009). Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection. Poultry Science, 88(5): 943-948.

Fukunaga TM, Sasaki Y, Araki T, Okamoto T, Yasuoka T, Tsujikawa T, Fujiyama Y and Bamba T (2003). Effects of the soluble fibre pectin on intestinal cell proliferation, fecal short chain fatty acid production and microbial population. Digestion, 67(1-2): 42-49.

Gabert VM and Sauer WC (1995). The effect of fumaric acid and sodium fumarate supplementation to diets for weanling pigs on amino acid digestibility and volatile fatty acid concentrations in ileal digesta. Animal Feed Science and Technology, 53(3-4): 243-54.

Garcia V, Catala-Gregori P, Hernandez F, Megias M and Madrid J (2007). Effect of formic acid and plant extracts on growth, nutrient digestibility, intestine mucosa morphology, and meat yield of broilers. Journal of Applied Poultry Research, 16(4): 555-562.

Gauthier R (2002). Intestinal health, the key to productivity (The case of organic acids). XXVll Convencion ANECA-WPDSA Puerto Vallarta, Jal. Mexico, 30 April 2002.

Gdala G, Jansman AJM, Buraczewska L, Huisman J and Leeuwen PV (1997). The influence of galactosidase supplementation on the ileal digestibility of lupin seed carbohydrates and dietary protein in young pigs. Animal Feed Science and Technology, 67(2): 115-125.

Geyra A, Uni Z and Sklan D (2001). Enterocyte dynamics and mucosal development in the posthatch chick.Poultry Science, 80(6): 776-782.

Gitzelmann R and Auricchio S (1965). The handling of soy a-galactosidase by a normal and galactosemic child. Pediatrics, 36(2):231-232.

Griggs JP and Jacob JP (2005). Alternatives to antibiotics for organic poultry production. Journal of Applied Poultry Research, 14(4): 750-756.

Griminger P and Scanes CG (1986). Protein metabolism. In: STURKIE, P.D. (Ed.) Avian Physiology, 4th ed. pp. 326-345 (Springer Verlag, New York, Berlin, Heidelberg, Tokyo).

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

Haque MN, Islam KMS, Akbar MA, Karim MR, Chowdhury R, Khatun M and Kemppainen BW (2010). Effect of dietary citric acid, flavomycin and their combination on the performance, tibia ash and immune status of broiler. Canadian Journal of Animal Science, 90(1): 57-63.

Heres L, Engel B, Van-Knapen F, De-Jong MC, Wagenaar JA and Urlings HA (2003). Fermented liquid feed reduces susceptibility of broilers for Salmonella enteritidis. Poultry Science, 82(4): 603-611.

Hersey SJ (1987). Pepsin secretion.In Physiology of the gastrointestinal tract, (L.R. Johnson, Ed.). 2: 947-957(New York, Raven Press).

Higgins C and Brinkhaus F (1999). Efficacy of several organic acids against molds. Journal of Applied Poultry Research, 8(4): 480-487.

Hinton AJR, Buhr RJ and Ingram KD (2000). Reduction of Salmonella in the crop of broiler chickens subjected to feed withdrawal. Poultry Science, 79(11): 1566-1570.

Hinton H and Linton AH (1988). Control of Salmonella infections in broiler chicken by the acid treatment of their feed. The Veterinary Record, 123(16):416-421.

Hinton M, Linton AH and Perry FG (1985). Control of salmonella by acid disinfecting of chicks food. The Veterinary Record, 116(18):502.

Houshmand M, Azhar K, Zulkifli I, Bejo MH and Kamyab A (2012). Effects of non-antibiotic feed additives on performance, immunity and intestinal morphology of broilers fed different levels of protein. South African Journal of Animal Science, 42(1): 22-32.

Huisman J and Jansman AJM (1991). Dietary effects and analytical aspects of antinutritional factors in peas and soybeans in monogastric farm animals. A literature review. Nutrition Abstracts and Reviews, 61: 901-921.

Hume ME, Corrier DE, Ivie GW and Deloach JR (1993). Metabolism of propionic acid in broiler chicks. Poultry Science, 72(5): 786-793.

Humphrey TJ and Lanning DG (1988).The vertical transmission of Salmonellas and formic acid treatment of chicken feed.A possible strategy for control. Epidemiology and Infection, 100(01):43-49.

Islam K (2012). Use of citric acid in broiler diets. World's Poultry Science Journal, 68(01): 104118.

Izat A, Tidwell N, Thomas R, Reiber M, Adams M, Colberg M and Waldroup PW (1990). Effects of a buffered propionic acid in diets on the performance of broiler chickens and on microflora of the intestine and carcass. Poultry Science, 69(5): 818-826.

'aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

Kidd MT, Ferket PR and Qureshi MA (1996). Zinc metabolism with special reference to its role in immunity. World's Poultry Science Journal, 52(03): 309-324.

Kirchgessner M and Roth FX (1982).Fumaric acid as a feed additive in pig nutrition. Pig News Information, 3: 259-263.

Khan MZI, Akter SH, Islam MN, Karim MR, Islam MR and Kon Y (2008). The effect of selenium and vitamin E on the lymphocytes and immunoglobulin containing plasma cells in the lymphoid organ and mucosa-associated tissue of broiler chick. Anatomia, Histologia, Embryologia,37(1): 52-59.

Khosravi A, Boldaji F, Dastar B and Hasani S (2010). Immune response and performance of broiler chicks fed protexin and propionic acid. International Journal of Poultry Science, 9(2): 188-191.

Kum S, Eren U, Onol A and Sandikci M (2010). Effects of Dietary Organic Acid Supplementation on the Intestinal Mucosa in Broilers. Revue De Medecine Veterinaire, 10: 463-468.

Langhout P (2000). New additives for broiler chickens. World Poultry, 16:22-27.

Lassen TM (2007). Acidified raw materials and acids in fur animal feed: Acid preservation of raw materials intended for fur animal feed. Workshop Nordiske Jordbrugs forskeres Foreign (NJF) Subsection for Fur Animals 37-65.

Li D, CheX, Wang Y, Hong C and Thacker P (1998). Effect of microbial phytase, vitamin D3, and citric acid on growth performance and phosphorus, nitrogen and calcium digestibility in growing swine. Animal Feed Science and Technology, 73(1): 173-186.

Loddi MM, Moraes VMB, Nakaghi LSO, Tuca FM, Hannas MI and Ariki J (2004). Mannan oligosaccharide and organic acids on performance and intestinal morphometric characteristics of broiler chickens.In proceedings of the 20th annual symposium. World's Poultry Congress, Istanbul, Turkey.Suppl, vol. 1, p. 45.

Luckstadt C and Mellor S (2011). The use of organic acids in animal nutrition, with special focus on dietary potassium diformate under European and Austral-Asian conditions. In Recent Advances in Animal Nutrition - Australia,18:123-130.

Maribo H, Jensen BB and Hedemann MS (2000a). Different doses of organic acids to piglets. Danish Bacon and Meat Council, no. 469: 23-28 (In Danish).

Maribo H, Olsen LE, Jensen BB and Miquel N (2000b).Produkter til smagrise: combinationen af mslkesyre og myresyre og benzoesyre. Meddelelse 490. Landsudvalget for Svin, pp. 13 (in Danish).

Mead PS, Slutsker L, Dietz V, Mccraig LF, Bresee JS, Shapiro C, Griffin PM and Tauxe RV (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5(5): 607625.

Miles RD, Butcher GD, Henry PR and Littell RC (2006). Effect of antibiotic growth promoters on broiler performance intestinal growth parameters, and quantitative morphology. Poultry Science, 85(3): 476-485.

Mista D, Piekarska J, Houszka M, Zawadzki W and Gorczykowski M (2010). The influence of orally administered short chain fatty acids on intestinal histopathological changes and intensity of Trichinella spiralis infection in mice.Veterinarni Medicina, 55(6): 264-274.

Moharrery A and Mahzonieh M (2005). Effect of malic acid on visceral characteristics and coliform counts in small intestine in the broiler and layer chickens. International Journal of Poultry Science, 4(10): 761-764.

Mroz Z, Jongbloed AW, Partanen KH, Verman K, Kemme PA and Kogut J (2000). The effects of calcium benzoate in diets with or without organic acids on dietary buffering capacity, apparent digestibility, retention of nutrients and manure characteristics in swine. Journal of Animal Science, 78(10): 2622-2632.

Omogbenigun FO, Nyachti CM and Solminski BA (2003). The effect of supplementing microbial phytase and organic acids to corn-soybean based diet fed to early-weaned pigs. Journal of Animal Science, 81(7): 1806-1813.

Riemensperger A (2012). Organic Acid-Based Products - Market Evaluation and Technical Comment. Available at:

http://www.thepoultrysite.com/articles/2372/organic-acidbased-products-market-evaluation-and-technical-comment; Accessed on 15-03-2015.

Panda A, Rao SVR, Raju M and Sunder GS (2009). Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Sciences, 22(7): 1026-1031.

Partanen K (2001). Organic acids their efficacy and modes of action in pigs.in Gut Environment of Pigs. A. Piva, K. E. Bach Knudsen, and J. E. Lindberg, eds. pp. 201 (Nottingham University Press, Nottingham, UK).

Partanen KH and Mroz Z (1999). Organic acids for performance enhancement in pig diets. Nutrition Research Reviews, 12(1): 1-30.

Patten JD and Waldroup PW (1988). Use of organic acids in broiler diets. Poultry Science, 67(8): 1178-1182.

Paul SK, Halder G, Mondal MK and Samanta G (2007). Effect of organic acid salt on the performance and gut health of broiler chicken. Journal of Poultry Science, 44(4): 389-395.

Pelicano ERL, Souza PA, Souza HBA, Figueiredo DF, Boiagom M, Carvalho SR and Bordon VF (2005). Intestinal mucosa development in broiler chicken fed natural growth promoters. Brazilian Journal of Poultry Science, 7(4): 221-229.

Pirgozliev V, Murphy TC, Owens B, George J and Mccann ME (2008). Fumaric and sorbic acid as

aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

additives in broiler feed. Research in Veterinary Science, 84(3): 387-94.

Podolsky DK (1993). Regulation of intestinal epithelial proliferation: a few answers, many questions. Animal Journal Physiologic, 264(2): 179-186.

Polonen I and Wamberg S (2007). Acidified raw materials and acids in fur animal feed:Workgroup II - Effects of acid on animal health. Workshop Nordiske Jordbrugs forskeres Foreign (NJF) Subsection for Fur Animals 116-133.

Prange A, Birzele B, Hormes J and Modrow H (2005). Investigation of different human pathogenic and food contaminating bacteria and mould grown on selenite/selenate and tellurite/tellurate by x-ray absorption spectroscopy. Food Control, 16(8): 713-728.

Qureshi MA, Hussain I and Heggen CL (1998). Understanding immunology in disease development and control. Poultry Science, 77(8): 1126-1129.

Radcliffe J, Zhang Z and Kornegay E (1998).The effects of microbial phytase, citric acid, and their interaction in a corn-soybean meal-based diet for weanling pigs. Journal of Animal Science, 76 (7): 1880-1886.

Rahmani HR, Speer W and Modirsanei M (2005). The effect of intestinal pH on broiler performance and immunity. Proceedings of the 15th European Symposium on poultry nutrition, Balatonfured, Netherlands: World's Poultry Science Association (WPSA), Hungary (25-29 September), pp. 338340.

Reutter W, Kottgen E, Bauer C and Wolfgang G (1982). Biological significance of sialic acids. In: Shauer, R. (Ed.), Sialic Acids, Chemistry, Metabolism, and Function. Springer-Verlag, New York, NY, pp. 263-305.

Ricke SC (2003). Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Science, 82(4): 632-639.

Rouse J, Rolow A and Nelson CE (1988). Research Note: Effect of chemical treatment of Poultry feed on survival of Salmonella. Poultry Science, 67(8): 1225-1228.

Runho RC, Sakomura NK, Kuana S, Banzatto D, Junqueira OM and Stringhini JH (1997). Use of an organic acid (fumaric acid) in broiler rations. Revista da Sociedade Brasileirade Zootecnia-Journal of the Brazilian Society of Animal Science, 26: 1183-1191.

Santin E (2010). Mycotoxins threaten the immune system. World Poultry, pp. 8-10.

Sauer W, Cervantes M, Yanez J, Araiza B, Murdoch G, Morales A and Zijlstra RT (2009). Effect of dietary inclusion of benzoic acid on mineral balance in growing pigs. Livestock Science, 122(2): 162-168.

Sharma JM (2003). The avian immune system. In Y. M. Saif, Diseases of Poultry.11th ed. pp 5-16 (Iowa State University Press, Ames).

Shohl AT (1937). The effect of the acid-base content of the diet upon the production and cure of rickets

with special reference to citrates. Journal of Nutrition, 14: 69-83.

Skinner JT, Izat AL and Waldroup PW (1991). Fumaric acid enhances performance of broiler chickens. Poultry Science, 70(6): 1444-1447.

Samanta S, Haldar S and Ghosh TK (2009). 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. Veterinary medicine international, 2010: 1-8.

Sohail HK and JavidIqbal (2016). Recent advances in the role of organic acids in poultry nutrition. Journal of Applied Animal Research, 44(1): 359369.

Suiryanrayna Mocherla VAN and Ramana JV (2015). A review of the effects of dietary organic acids fed to swine. Journal of animal science and biotechnology, 6(1): 1-13.

Tappenden KA and Mcburney MI (1998). Systemic short-chain fatty acids rapidly alter gastro intestinal structure, function, and expression of early response genes. Digestive Diseases and Sciences, 43(7): 1526-1536.

Taylor DJ (2001). Effects of antimicrobials and their alternatives. British Poultry Science, 42: 67-68.

Thompson JL and Hinton M (1997). Antibacterial activity of formic and propionic acids in the diet of hens on salmonellas in the crop. British Poultry Science, 38(1): 59-65.

Tyler JW, Hancock DD, Parish SM, Rea DE, Besser TE, Sanders SG and Wilson LK (1996). Evaluation of 3 assays for failure of passive transfer in calves. Journal of Veterinary Internal Medicine, 10(5): 304-307.

Underwood EJ and SuttleNF (1999). The mineral nutrition of livestock. pp. 67-149. (CAB International).

Van IF, Fievez 1V, Buck JD, Pasmans F, Martel A, Haesebrouck F and Ducatelle R (2006). Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with salmonella enteritidis in young chickens. Poultry Science, 83(1): 69-74.

Van-IF, Buck DE, Boyen J, Bohez F, Pasmans L, Volf F, Sevcik J, Rychlik M, Haesebrouck F and Ducatelle R (2004). Medium-chain fatty acids decrease colonization and invasion shortly after infection with Salmonella Enteritidis in chickens through hilA suppression. Applied and Environmental Microbiology, 70(6): 3582-3587.

Versteegh HAJ and Jongbloed AW (1999).The effect of supplementary lactic acid in diets on the performance of broilers.ID-DLO Rep. No. 99.006. Institute for Animal Science and Health, Branch Runderweg, Lelystad, The Netherlands.

Visek WJ (1978). The mode of growth promotion by antibiotics. Journal of Animal Science, 46(5): 1447-1469.

Vogt H, Matthes S and Harnisch S (1982). Effect of organic acids in rations on the performances of broilers. Archiv Fur Geflugelkunde, 46: 223-227.

'aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.

Waldroup A, Kaniawati S and Mauromoustakos A (1995). Performance characteristics and microbiological aspects of broilers fed diets supplemented with organic acids. Journal of Food Protection, 58(5): 482-489.

Wang JP, Yoo JS, Lee JH, Zhou TX, Jang HD, Kim HJ and Kim IH (2009). Effects of phenyllactic acid on production performance, egg quality parameters, and blood characteristics in laying hens. Journal of Applied Poultry Research, 18(2): 203-209.

Whittow GC (2000). Sturkie's avian physiology. Academic Press San Diego.

Young KM and Foegeding PM (1993). Acetic, lactic and citric acids and pH inhibition of Listeria monocytogenes Scott A and the effect on intracellular pH. Journal of Applied Bacteriology, 74(5): 515-520.

'aseem Mirza M, Rehman ZU and Mukhtar N. 2016. Use of Organic Acids as Potential Feed Additives in Poultry Production. J. World's Poult. Res.

6(3): 105-116.