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<journal-meta>
<journal-id>0120-0690</journal-id>
<journal-title><![CDATA[Revista Colombiana de Ciencias Pecuarias]]></journal-title>
<abbrev-journal-title><![CDATA[Rev Colom Cienc Pecua]]></abbrev-journal-title>
<issn>0120-0690</issn>
<publisher>
<publisher-name><![CDATA[Facultad de Ciencias Agrarias, Universidad de Antioquia]]></publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id>S0120-06902015000200002</article-id>
<article-id pub-id-type="doi">10.17533/udea.rccp.v28n2a01</article-id>
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<article-title xml:lang=""><![CDATA[]]></article-title>
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<aff id="A01">
<institution><![CDATA[,Chung-Ang University  ]]></institution>
<addr-line><![CDATA[ ]]></addr-line>
<country>Republic of Korea</country>
</aff>
<aff id="A02">
<institution><![CDATA[,Chung - Ang University  ]]></institution>
<addr-line><![CDATA[ ]]></addr-line>
</aff>
<pub-date pub-type="pub">
<day>00</day>
<month>06</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub">
<day>00</day>
<month>06</month>
<year>2015</year>
</pub-date>
<volume>28</volume>
<numero>2</numero>
<fpage>109</fpage>
<lpage>123</lpage>
<copyright-statement/>
<copyright-year/>
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</front><body><![CDATA[  <font size="2" face="Verdana, Arial, Helvetica, sans-serif">     <p align="right"><b>LITERATURE REVIEW </b></p>     <p align="right">&nbsp;</p>     <p align="right">doi: <a href="http://dx.doi.org/10.17533/udea.rccp.v28n2a01" target="_blank" >10.17533/udea.rccp.v28n2a01</a></p>      <p align="center"><font size="4"><b>Dietary organic acids for broiler chickens: a review<sup><a href="#a1" a name="a0">&curren;</a></sup></b></font></p>     <p align="center">&nbsp;</p>     <p align="center"><font size="3"><i><b>&Aacute;cidos org&aacute;nicos en la dieta de pollos de engorde: revisi&oacute;n de literatura</b></i></font></p>     <p align="center">&nbsp;</p>     <p align="center"><font size="3"><i><b>Dietas &aacute;cidos org&acirc;nicos sobre frangos de corte: revis&atilde;o de literatura</b></i></font></p>     <p align="center">&nbsp;</p>     ]]></body>
<body><![CDATA[<p align="center">&nbsp;</p>     <p align="left"><b>Jong Woong Kim, AnSc, MS; Jong Hyuk Kim, AnSc, MS; Dong Yong Kil<sup><a href="#a3" a name="a4">*</a></sup>, AnSc, PhD.</b></p>     <p align="left">&nbsp;</p>     <p align="left"><i>Department of Animal Science and Technology, Chung-Ang University, Anseong-si, Gyeonggi-do 456-756, Republic of Korea.</i></p>     <p align="left">&nbsp;</p>     <p align="left"><a href="#a4" a name="a3">*</a>Corresponding author: Dong Yong Kil, Department of Animal Science and Technology, Chung - Ang University, Anseong-si, Gyeonggi-do 456-756, Republic of Korea. Tel:+82 316703028, Fax:+82 316762196. Email: <a href="dongyong@cau.ac.kr" target="_blank">dongyong@cau.ac.kr</a></a></p>     <p align="left">&nbsp;</p>     <p align="left">Received: April 8, 2013; accepted: March 30, 2014</p>     <p align="left">&nbsp;</p> <hr size="1">     <p align="left"><b>Summary</b></p>     ]]></body>
<body><![CDATA[<p align="left">The objective was to summarize and describe the possible mode of action of dietary organic acids and their effects on growth performance of broiler chickens. Previous experiments have suggested that dietary organic acids decrease pH in diets and subsequently reduce pH in the proximal and distal intestine, increase nutrient utilization, and inhibit pathogenic bacterial growth in the gastrointestinal tract (GIT). The degree of pH reduction is usually greater in the upper part of the GIT (crop, proventriculus, and gizzard) than in the lower part of the GIT (duodenum, jejunum, ileum, and cecum). Bactericidal effects of dietary organic acids have been observed for pathogenic bacteria and even for beneficial bacteria to some extent. However, few significant results regarding bacterial modulation in the GIT have been reported. Dietary organic acids can improve dry matter and protein utilization in some experiments, but the extent of improvement in nutrient utilization is smaller than has been anticipated. Growth performance is likely improved, but results have been inconsistent due to variations in sources and inclusion levels of dietary organic acids. Differences in other dietary components and experimental environments among previous experiments likely contribute to the variable results. This review suggests that the effects of dietary organic acids on broiler chickens are not fully understood. Further experiments are required to reliably demonstrate the mode of action of dietary organic acids and their growth-promoting effects on broiler chickens.</p>     <p align="left"><b>Keywords:</b> <i>acidifiers, gastrointestinal pH, growth performance, microbial population, nutrient utilization.</i></p> <hr size="1">     <p align="left"><b>Resumen</b></p>     <p align="left">El objetivo fue resumir y describir el posible modo de acci&oacute;n de los &aacute;cidos org&aacute;nicos en la dieta y sus efectos sobre el crecimiento de los pollos de engorde. Experimentos previos sugieren que los &aacute;cidos org&aacute;nicos dietarios disminuyen el pH de la dieta y posteriormente reducen el pH en el intestino proximal y distal, aumentan la utilizaci&oacute;n de los nutrientes, e inhiben el crecimiento de bacterias pat&oacute;genas en el tracto gastrointestinal (GIT). El grado de reducci&oacute;n del pH es generalmente mayor en la parte superior (buche, proventr&iacute;culo y molleja) que en la parte inferior del GIT (duodeno, yeyuno, &iacute;leon y ciego). Se han observado efectos bactericidas de los &aacute;cidos org&aacute;nicos sobre bacterias pat&oacute;genas e incluso sobre bacterias beneficiosas en cierta medida. Sin embargo, se han reportado algunos resultados significativos con respecto a la modulaci&oacute;n bacteriana en el GIT. Los &aacute;cidos org&aacute;nicos en la dieta pueden mejorar la utilizaci&oacute;n de la materia seca y la prote&iacute;na en algunos experimentos, pero el grado de mejora en la utilizaci&oacute;n de los nutrientes es m&aacute;s bajo que lo esperado. El crecimiento probablemente mejora, pero los resultados han sido inconsistentes debido a las variaciones en las fuentes y a los niveles de inclusi&oacute;n de los &aacute;cidos org&aacute;nicos en la dieta. Las diferencias en otros componentes de la dieta y entornos experimentales entre los ensayos anteriores probablemente contribuyen a la variacion en los resultados. Esta revisi&oacute;n sugiere que los efectos de los &aacute;cidos org&aacute;nicos en la dieta de pollos de engorde no son totalmente comprendidos. Se requieren m&aacute;s experimentos para demostrar de manera fiable el modo de acci&oacute;n de los &aacute;cidos org&aacute;nicos dietarios y sus efectos sobre la promocion del crecimiento en pollos de engorde.</p>     <p align="left"><b>Palabras clave:</b><i> acidificantes, desempe&ntilde;o del crecimiento, pH gastrointestinal, poblaci&oacute;n microbiana, utilizaci&oacute;n de nutrientes.</i></p> <hr size="1">     <p align="left"><b>Resumo</b></p>     <p align="left">Este estudo se fez para resumir e descrever o poss&iacute;vel modo de a&ccedil;&atilde;o dos &aacute;cidos org&acirc;nicos na dieta e seus efeitos sobre o desempenho do crescimento de frangos de corte. Pesquisas feitas nesta &aacute;rea tem descrito que   os &aacute;cidos org&acirc;nicos nas dietas diminuem o pH da dieta e subsequentemente diminuem o pH no intestino proximal e distal, aumentam a utiliza&ccedil;&atilde;o de nutrientes e inibem o crescimento de bact&eacute;rias patog&eacute;nicas no trato gastrointestinal (GIT). O grau de redu&ccedil;&atilde;o do pH &eacute; normalmente maior na parte superior do GIT (colheita, proventr&iacute;culos e moela) do que na parte inferior do GIT (duodeno, jejuno, &iacute;leo e ceco). Com a inclus&atilde;o de &aacute;cidos org&acirc;nicos nas dietas tem-se observado efeitos bactericidas tanto sobre as bact&eacute;rias patog&eacute;nicas quanto para as bact&eacute;rias ben&eacute;ficas, em certa medida. Por&eacute;m, tem-se reportado alguns resultados significativos enquanto &agrave; modula&ccedil;&atilde;o bacteriana no GIT. A adi&ccedil;&atilde;o de &aacute;cidos org&acirc;nicos na dieta pode melhorar o aproveitamento de mat&eacute;ria seca e prote&iacute;na em alguns testes, mas o grau de melhora na utiliza&ccedil;&atilde;o dos nutrientes &eacute; menor do que o esperado. Provavelmente melhora o crescimento, mas os resultados t&ecirc;m sido inconsistentes, devido as varia&ccedil;&otilde;es nas fontes e aos n&iacute;veis de inclus&atilde;o de &aacute;cidos org&acirc;nicos na dieta. As diferen&ccedil;as em outros componentes da dieta e os lugares onde se fazem os testes contribuem para a varia&ccedil;&atilde;o dos resultados. Esta an&aacute;lise sugere que os efeitos dos &aacute;cidos org&acirc;nicos nas dietas de frangos de corte n&atilde;o s&atilde;o totalmente compreendidos. Precisam-se mais pesquisas para demonstrar uma maneira fi&aacute;vel do modo de a&ccedil;&atilde;o dos &aacute;cidos org&acirc;nicos inclu&iacute;dos na dieta e seus efeitos sobre a promo&ccedil;&atilde;o do crescimento em frangos de corte.</p>     <p align="left"><b>Palavras chave:</b> <i>acidificantes, desempenho produtivo, pH gastrointestinal, popula&ccedil;&atilde;o microbiana, utiliza&ccedil;&atilde;o de nutriente.</i></p> <hr size="1">     <p align="left">&nbsp;</p>     <p align="left">&nbsp;</p>     ]]></body>
<body><![CDATA[<p align="left"><b><font size="3">Introduction</font></b></p>     <p align="left">Antibiotic growth promoters (AGPs) have been widely used in poultry diets for years. The use of AGPs, however, has been either regulated or banned because of public concerns over possible antibiotic residual problems and the development of antibioticresistant bacteria (Leeson, 2007). Consequently, many researchers have searched for potential alternatives to AGPs. Organic acids, organic minerals, bacteriophages, probiotics, and prebiotics have been suggested as a useful dietary means for compensating the loss in productive performance when AGPs are removed from poultry diets (Jackson <i><i>et al.,	</i></i>	 2004; Yan <i><i>et al.,	</i></i>	 2012). Among these alternatives, dietary organic acids have gained great attention because of their antimicrobial activity against pathogenic bacteria and the fact that these compounds can induce a pH reduction in the gastrointestinal tract (GIT), which can improve nutrient utilization in poultry diets (Eidelsburger <i><i>et al.,	</i></i>	 1992; Boling <i><i>et al.,	</i></i>	 2000; Partanen, 2001; Kil <i><i>et al.,	</i></i>	 2011a).</p>     <p align="left">Dietary acids for poultry diets are classified as inorganic and organic acids. However, organic acids have been more often used for poultry diets. Organic acids can be defined as carboxylic acids including fatty acids, which have the chemical structure of R-COOH with acidic properties. However, not all organic acids have been used as feed additives in poultry diets. Short chain fatty acids such as formic (C1), acetic (C2), propionic (C3), and butyric acid (C4), and other carboxylic acids such as lactic, malic, tartaric, fumaric, and citric acid have been most commonly used in the poultry industry because their chemical and physical properties are applicable to poultry diets (Dibner and Buttin, 2002). Previously, several reviews have discussed the effects of dietary organic acids on broiler chickens (Dibner and Buttin, 2002; Ricke, 2003; Anjum and Chaudhry, 2010; Islam, 2012). However, previous reviews have not provided a complete evaluation of the potential mechanisms, and have not compiled the effects of dietary organic acids on broiler performance with the recent data. The objective of this review, therefore, was to summarize and describe the possible mode of action of dietary organic acids for broiler chickens and the effects of dietary organic acids on the growth performance of broiler chickens.</p>     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">Potential mode of action of dietary organic acids</font></b></p>     <p align="left">The mode of action of organic acids in animal diets has not been clearly elucidated; this incomplete understanding has limited the application of organic acids in broiler diets. However, several possible mechanisms have been proposed and most of them have been associated with: (1) decreased pH in diets and subsequent reduction of the pH in the GIT, (2) improved nutrient utilization in diets by increasing nutrient retention, and (3) inhibition of pathogenic bacterial growth (Afsharmanesh and Pourreza, 2005; Mroz, 2005). Further research has been performed to elucidate the mode of action of dietary organic acids in various animal species, but the results remain controversial.</p>     <p align="left"><i>Effects on the pH of the gastrointestinal tract (GIT)</i></p>     <p align="left">The degree of pH reduction in diets and digesta by dietary organic acids is likely dependent of both the pKa values of the respective organic acids and the pH conditions of the GIT (Kim <i><i>et al.,	</i></i>	 2005). As expected, the pH of broiler diets was clearly decreased with increasing inclusion levels of dietary organic acids in a dose-dependent manner (<a href="/img/revistas/rccp/v28n2/v28n2a02t1.jpg" target="_blank">Table 1</a>), as was also observed in pig diets (Kil <i><i>et al.,	</i></i>	 2011a). Subsequently, the addition of organic acids to broiler diets resulted in the pH reduction of digesta in various parts of the GIT. In general, the degree of pH reduction was usually greater in the upper part of GIT (crop, proventriculus, and gizzard) as compared to the lower part of the GIT (duodenum, jejunum, ileum, and cecum). In seven previous experiments, 11 of 13 organic acid-supplemented groups showed decreased crop pH compared with the control groups, with 7 of 11 observations being significant. Three experiments reported that the pH reductions in the crop were dosedependent. The average pH reduction in the crop was 0.37 (standard error [SE] = 0.10) and it is likely that, of all locations in the GIT, the crop showed the greatest pH reduction. This observation may be related to the short transit of the acids to the crop in addition to the less acidic conditions of the crop (Thompson and Hinton, 1997). </p>      <p align="center"><a name="t1"></a><a href="/img/revistas/rccp/v28n2/v28n2a02t1.jpg" target="_blank">Table 1</a></p>       <p align="left">In four previous experiments (Paul <i><i>et al.,	</i></i>	 2007; Samanta <i><i>et al.,	</i></i>	 2008; Panda <i><i>et al.,	</i></i>	 2009a; Salgado-Tr&aacute;nsito <i><i>et al.,	</i></i>	 2011), 6 out of 10 organic acid-supplemented groups showed pH reduction in the proventriculus compared with the control groups. However, the reduction achieved statistical significance in only one experiment (Panda <i><i>et al.,	</i></i>	 2009a). The average pH reduction in the proventriculus was 0.12 (SE = 0.07), which was less than the pH reduction as observed in the crop. In the lower part of the GIT, the effects of dietary organic acids on digesta pH were more variable than in the upper part of the   GIT. Samanta <i>et al.</i>	 (2008), Panda <i>et al.</i>	 (2009a), and Nourmohammadi <i>et al.</i>	 (2011) reported a significant pH reduction in the duodenum, whereas other studies found no significant pH reductions in the duodenum. Similar tendencies for pH reduction were observed in the jejunum, ileum, and cecum. It has been reported that only small amounts of added organic acids in diets may reach the lower part of the GIT because organic acids are very readily absorbed in the upper part of the GIT (Hume <i><i>et al.,	</i></i>	 1993). This may explain the lack of pH reduction in the lower part of the GIT as a result of dietary organic acids. Taken together, the data indicate that the effects of dietary organic acids on the pH of the GIT may be limited to the upper part of the GIT in broiler chickens.</p>     ]]></body>
<body><![CDATA[<p align="left"><i>Effects on nutrient utilization</i></p>     <p align="left">Reduced pH in the upper part of the GIT may increase nutrient digestibility, and therefore, nutrient utilization in diets. In the stomach, a reduction in gastric pH activates pepsinogen and other zymogens by adjusting gastric acidity closer to that required for optimal activity (Jongbloed <i><i>et al.,	</i></i>	 2000); this increased enzyme activity can improve the digestion of proteins and possibly other nutrients. Furthermore, acidic digesta may decrease gastric emptying, and therefore provide more time for nutrient digestion in the GIT (Kidder and Manners, 1978; Mayer, 1994). Several researchers have demonstrated that dietary supplementation of organic acids can improve the retention of protein and other nutrients. The data from the five previous experiments indicated that broiler chickens fed diets containing various inclusion levels of dietary organic acids generally had greater retention of dry matter (DM) and protein than those fed control diets (<a href="#t2">Table 2</a>). Average improvements in the retention of DM and protein were 1.0% (SE = 0.60) and 1.7% (SE = 0.88), respectively. However, we excluded the data from Nezhad <i>et al.</i>	 (2011) in the calculations of the average improvements in the retention of DM and protein because of the unexpectedly high improvement in the retention of protein. Among 14 organic acid supplemented groups, 7 and 9 groups showed a numerical increase in the retention of DM and protein, respectively; however, no significant improvements were verified. In addition, it is unlikely that there were dose dependent responses of organic acids to nutrient retention. When we considered the ratio of the number of positive responses to the number of negative responses by dietary organic acid supplementation, however, broiler chickens fed diets containing organic acids may have improved nutrient retention. However, it appears that the extent of the improvements in nutrient retention may be smaller than anticipated. Surprisingly, there have been few data pertaining to the effects of dietary organic acids on amino acid digestibility in diets fed to broiler chickens compared with other animal species. Further experiments investigating standardized ileal digestibility and true ileal digestibility of amino acid are required to verify the effects of dietary organic acids on nutrient utilization especially for amino acids in diets fed to broiler chickens.</p>      <p align="center"><a name="t2"><img src="/img/revistas/rccp/v28n2/v28n2a02t2.jpg"></a></p>      <p><i>Effects on pathogenic bacteria</i>     <p>An increased population of pathogenic bacteria in   the GIT often results in reduced growth performance   of broiler chickens. Therefore, the prevention of   pathogenic bacterial over-growth in the GIT may be   one of the most important strategies for enhancing   growth performance when supplemental AGPs   are not used in animal diets. Organic acids can   easily penetrate the bacteria cell wall and disrupt   normal cellular functions, including replication and   protein synthesis of bacteria (Denyer and Stewart,   1998; Davidson, 2001). The proposed sequential   mechanisms of bactericidal action are followed as   (Mani-Lopez <i><i>et al.,	</i></i>	 2012): (1) acid form of organic   acids (protonated form) can penetrate across the   bacteria cell wall, (2) penetrated organic acids within   bacterial cells dissociate into the conjugated base form   (non-protonated form) with a concomitant reduction   in cellular pH, and (3) decreased pH creates a stressful   environment leading to cellular dysfunctions, and   thus prevents bacterial growth. Such reactions are   likely to occur mainly with pH-sensitive bacteria   species, which include the wide range of pathogenic   bacteria. Akyurek <i>et al.</i>	 (2011) reported that broiler   chickens fed diets containing organic acid blends   had less pathogenic bacterial loads such as coliforms   and Clostridia but greater beneficial bacteria such   as Lactobacilli in the ileum compared with those   fed diets containing AGPs. It is also likely that the   decreased pH in the GIT induced by dietary organic   acids may play a role in preventing bacterial transfer   from the diet or environment. However, most of   the previous experiments regarding the effects of   dietary organic acids on microbial populations in the   GIT reported few significant benefits on microbial   populations in the GIT (<a href="#t3">Table 3</a>). In our summary,   moreover, the birds fed diets containing organic acids   had slightly lower lactic acid-producing bacteria or   Lactobacilli counts in the ileum (0.44 log<sub>10</sub> &plusmn; 0.20   colony forming units [CFU]) and the cecum (0.37 &plusmn;   0.07 log<sub>10</sub> CFU) than those fed control diets although   these species are generally considered as beneficial   bacteria. This observation was inconsistent with the   findings of Akyurek <i>et al.</i>	 (2011). There have been     only few experiments showing a significant reduction   in coliform bacteria or Escherichia coli counts in e GIT by feeding diets containing organic acids to broiler chickens. Average reductions in the numbers of coliform bacteria or E. coli count were 0.86 &plusmn; 0.23 log<sub>10</sub> CFU for the ileum and 0.82 &plusmn; 0.22 log<sub>10</sub> CFU for the cecum. However, the average reductions in the numbers of coliform bacteria or E. coli count were greater than those of lactic acid-producing bacteria or Lactobacilli counts in the ileum or the cecum. The reason that lactic acid-producing bacteria or Lactobacilli may be less affected by dietary organic acids than coliform bacteria or E. coli may be related to the fact that coliform bacteria or E. coli are more sensitive to pH reductions than lactic acid-producing bacteria or Lactobacilli in the GIT. Because previous experiments have focused on the specific bacteria species, the effects of dietary organic acids on the change in the entire microbial populations in the GIT are still unknown. Therefore, further experiments are necessary to demonstrate the effects of dietary organic acids across the whole microbial populations. In addition, the application of molecular-based techniques such as real-time polymerase chain reaction (RT-PCR), and pyrosequencing procedures may yield more valuable and accurate results than conventional culture-based techniques (Kil and Swanson, 2011b).</p>     <p align="center"><a name="t3"><img src="/img/revistas/rccp/v28n2/v28n2a02t3.jpg"></a></p>     <p align="left"><i>Other possible effects </i>     <p align="left">Previous experiments have reported that dietary   organic acids can increase phosphorus utilization   in corn-soybean meal diets fed to broiler chickens   (Boling <i><i>et al.,	</i></i>	 2000; Esmaeilipour <i><i>et al.,	</i></i>	 2011).   Phosphorus utilization may be increased due to the   chelating properties of organic acids with calcium,   which can result in increased phytate-phosphorus   solubility, increasing their ability to be hydrolyzed   (Centeno <i><i>et al.,	</i></i>	 2007). Some researchers have also   proposed that organic acids may stimulate energy   metabolism by providing energy sources for epithelial   cells in the GIT (Ravindran and Kornegay, 1993;   Partanen and Mroz, 1999). For instance, some organic   acids such as fumaric and citric acids are intermediates   of the tricarboxylic acid cycle, and butyric acid is   the direct energy source for epithelial cells in the   GIT (Partanen and Mroz, 1999; Pryde <i><i>et al.,	</i></i>	 2002).   However, no data have elucidated the cellular roles   of organic acids sin the energy metabolism of broiler   chickens.</p>     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">Organic acids and growth performance </font></b>     ]]></body>
<body><![CDATA[<p align="left">There has been accumulating evidence that   broiler chickens fed diets containing various sources   and levels of organic acids have improved growth   performance. In the current review, we surveyed 31   recent publications and compared the effects of diets   containing various organic acids on body weight gain,   feed intake, and feed efficiency (gain to feed ratio) with   those of control diets in broiler chickens (<a href="#t4">Table 4</a>). The   results for individual organic acid are detailed below.     <p align="center"><a name="t4"><img src="/img/revistas/rccp/v28n2/v28n2a02t4.jpg"></a></p>     <p align="left"><i>Citric acid</i>     <p align="left">Citric acid (C<sub>6</sub>H<sub>8</sub>O<sub>7</sub>) is a weak organic acid and   has been used as a natural preservative. Citric acid   has been widely used as an organic acid supplement   for pigs and chickens. We examined eight previous   experiments using various inclusion levels of dietary   citric acid (<a href="#t5">Table 5</a>). The data indicated that dietary   citric acid generally led to increased body weight gain and feed efficiency but decreased feed intake of   broiler chickens; however, there was high variation   in the ratio of the number of positive responses   to the number of negative responses. The average   improvements in body weight gain and feed efficiency   were 4.7 and 6.0%, respectively. It is noteworthy that   feed efficiency in most acid-supplemented groups   was improved except for three treatment groups.   Regardless of the inclusion levels of citric acid, half   of the acid-supplemented groups reported significant   increase in body weight gain (Chowdhury <i><i>et al.,	</i></i>	 2009;   Haque <i><i>et al.,	</i></i>	 2010; Nourmohammadi <i><i>et al.,	</i></i>	 2010;   Salgado-Tr&aacute;nsito <i><i>et al.,	</i></i>	 2011). However, only two   experiments reported significant improvements in feed   intake (Haque <i><i>et al.,	</i></i>	 2010; Nourmohammadi <i><i>et al.,	</i></i>	   2010) and feed efficiency (Chowdhury <i><i>et al.,	</i></i>	 2009;   Salgado-Tr&aacute;nsito <i><i>et al.,	</i></i>	 2011). It is postulated that   excessive amounts of dietary citric acid inclusion may   compromise performance because two experiments   using 60 g/kg citric acid in diets reported significant   decreases in body weight gain.     <p align="center"><a name="t5"><img src="/img/revistas/rccp/v28n2/v28n2a02t5.jpg"></a></p>     <p align="left"><i>Fumaric acid</i>     <p align="left">Fumaric acid (C<sub>4</sub>H<sub>4</sub>O<sub>4</sub>) is a weak organic acid with   a fruit-like taste. Published data from three previous   experiments (Patten and Waldroup, 1988; Skinner   <i><i>et al.,	</i></i>	 1991; Biggs and Parsons, 2008) indicated that   broiler chickens fed diets containing various inclusion   levels of fumaric acid had increased body weight gain   and feed intake, except for the data from 45 g/kg of   fumaric acid-supplemented groups of one experiment   (Biggs and Parsons, 2008; <a href="#t6">Table 6</a>). On the contrary,   Pirgozliev <i>et al.</i>	 (2008) reported that adding 5, 10,   or 15 g/kg fumaric acid to broiler diets significantly   reduced body weight gain by 7.9 to 25.7% and feed   intake by 5.9 to 41.4% compared with the control   groups. The reason for this large negative impact   on broiler performance is unclear. As a result, we   excluded the data from Pirgozliev <i>et al.</i>	 (2008) from   our calculations of the average change in the growth   performance to prevent the results of the current   study obscuring the effects of dietary fumaric acid on   the growth performance. Subsequently, the average   improvements in body weight gain and feed intake   were 1.3 and 1.9%, respectively. Feed efficiency was   slightly improved by an average of 0.2%. However, it   is difficult to conclude that dietary fumaric acid has positive effects on broiler performance because of the scarcity of data.      <p align="center"><a name="t6"><img src="/img/revistas/rccp/v28n2/v28n2a02t6.jpg"></a></p>     <p align="left"><i>Formic acid and its salts </i>     <p align="left">Formic acid (CH<sub>2</sub>O<sub>2</sub>) is the simplest carboxylic   acid. Formic acid is very volatile and has a pungent   smell. Therefore, the free form of formic acid has not   been widely used as a dietary supplement, whereas   its salts (as formates), which are less pungent and   easier to handle, have been often added to broiler   diets. We reviewed seven previous experiments using   formic acids or formates as dietary supplements for   broiler chickens (<a href="#t7">Table 7</a>). Feeding broiler chickens   with diets containing 1 to 10 g/kg of formic acid was   reported to increase body weight gain, feed intake,   and feed efficiency. The average improvements were   2.8, 0.4, and 5.3% for body weight gain, feed intake,   and feed efficiency, respectively. With the exception   of Garc&iacute;a <i>et al.</i>	 (2007) who reported that the birds   fed diets containing 5 or 10 g/kg of formic acid had   less body weight gain than those fed the control   diets, positive effects on body weight gain were   reported for all formic acid-supplemented groups.   Furthermore, clear dose-dependent positive effects   on body weight gain were also reported in some experiments (Hern&aacute;ndez <i><i>et al.,	</i></i>	 2006; Panda <i><i>et al.,	</i></i>	 2009b). However, the results for dietary formates were inconsistent. Patten and Waldroup (1988) observed decreased feed efficiency by dietary supplementation of calcium formate from 7.2 to 28.9 g/kg, whereas Paul <i>et al.</i>	 (2007) reported improved body weight gain and feed efficiency with diets containing 3 g/kg ammonium formate. The differences in the form of formates and the inclusion levels among experiments may cause these inconsistent results. It may be reasonable to conclude that the free form of formic acid has positive effects on the growth performance of broiler chickens, but the effects of formates are questionable.     ]]></body>
<body><![CDATA[<p align="center"><a name="t7"><img src="/img/revistas/rccp/v28n2/v28n2a02t7.jpg"></a></p>     <p align="left"><i>Butyric acid </i>     <p align="left">In the past decade, butyric acid (C<sub>4</sub>H<sub>8</sub>O<sub>2</sub>) has   been the most intensively studied by many poultry   researchers. Butyric acid is considered important for   the normal development of epithelial cells because   it can be used as a direct energy source by epithelial   cells and has bactericidal activity in the GIT (Pryde   <i><i>et al.,	</i></i>	 2002). We examined five previous experiments   using butyric acid (<a href="#t8">Table 8</a>). When butyric acid   was added to broiler diets, body weight gain and   feed efficiency were generally improved. Average   percentage improvements were 1.9 and 2.5% for   body weight gain and feed efficiency, respectively.   However, the improvements in feed efficiency were   likely caused by decreased feed intake along with   no or little change in body weight gain because 6   of 10 butyric acid-supplemented groups showed decreased feed intake. No clear explanation for this   anorexic effect has been postulated. In addition, high   inclusion levels of butyric acid may have a negative   effect on feed efficiency because Aghazadeh and   TahaYazdi (2012) reported that 25 g/kg of dietary   butyric acid decreased feed efficiency by 1.0%.   Based on the current data, however, it appears that   butyric acid at low inclusion levels may have the   most promising effects on broiler performance   among dietary organic acids.      <p align="center"><a name="t8"><img src="/img/revistas/rccp/v28n2/v28n2a02t8.jpg"></a></p>     <p align="left"><i>Other organic acids</i>     <p align="left">Other sources of organic acids and mixtures (or   blends) of various organic acids have also been tested   for their utilization in broiler diets (<a href="#t9">Table 9</a>). Al-Kassi   and Mohssen (2009) reported that adding 2 g/kg of   propionic acid to broiler diets resulted in significant   improvements in body weight gain, feed intake, and   feed efficiency by 11.2, 5.1, and 6.1%, respectively.   Likewise, Paul <i>et al.</i>	 (2007) also reported that broiler   chickens fed diets containing 3 g/kg of calcium   propionate had significantly improved feed efficiency   by 6.5% compared with those fed control diets. In   recent years, there has been increasing attention on the   blending type (i.e., mixtures) of organic acids based   on the assumption that synergistically positive effects   of individual organic acid exist (Kil <i><i>et al.,	</i></i>	 2011a).   We examined six previous experiments investigating   this aspect. Al&ccedil;i&ccedil;ek <i>et al.</i>	 (2004) reported that feeding   broiler chickens with 2.5 g/kg of blends of lactic   acid, formic acid, and citric acid improved growth   performance although the improvements did not   reach statistical significance. Gunal <i>et al.</i>	 (2006) also   observed that birds fed diets containing 2 g/kg blends   of propionate salts and formates had numerically   greater body weight gain and feed intake than those   fed the control diets. Similar improvements have also   been reported by Samanta <i>et al.</i>	 (2008) who added 1 g/kg   of acid blends of formic acid, propionic acid, calcium   propionate, and ortho-phosphoric acid to broiler diets.   Kim <i>et al.</i>	 (2009) also reported that body weight gain   in acid blend-supplemented groups was increased   by from 1.8 to 3.2%, whereas feed efficiency was improved by nearly 4.0%.     <p align="center"><a name="t9"><img src="/img/revistas/rccp/v28n2/v28n2a02t9.jpg"></a></p>     <p align="left">In contrast, two previous experiments observed   negative effects of dietary acid blends on body weight   gain of broiler chickens. Swiatkiewicz and Arczewska-   Wlosek (2012) reported that broiler chickens fed diets containing 4 g/kg of acid blends had less body weight gain and feed efficiency. Similarly, Smulikowska <i>et al.</i>	 (2010) reported decreased body weight gain and feed intake of broiler chickens fed diets containing 6 g/kg of acid blends. Considering the number of positive and negative responses, the effectiveness and synergism of acid blends for broiler chickens remain unclear.     <p align="left"><i>Factors affecting inconsistent results </i>     <p align="left">The responses of broiler chickens to dietary   organic acids have shown considerable inconsistency.   There have been many successful demonstrations of   positive effects of dietary organic acids on growth   performance, whereas other studies were unable to   find beneficial effects or even reported negative effects   on growth performance. The extent of the effects was   also variable among the previous experiments using   different inclusion levels and sources of organic   acids. Several possible factors responsible for these variations can be identified.     ]]></body>
<body><![CDATA[<p align="left">One factor could be the variation in other dietary   ingredients and their chemical properties such as   buffering capacity (Mroz <i><i>et al.,	</i></i>	 1997; Partanen, 2001).   The sources and amounts of dietary protein and   minerals may affect the buffering capacity of diets,   which can influence the degree of acidification that   occurs with the inclusion of organic acids (Partanen   and Mroz, 1999). Although the related data for broiler   chickens have been limited, the effects of buffering   capacity on the effectiveness of dietary organic acids   have been reported in pigs. Ravindran and Kornegay   (1993) reported that the positive effects of dietary   organic acids on weanling pigs were greater for the   diets of low buffering capacity (simple corn-soybean   meal-based diets) than for the diets of high buffering   capacity (complex diets containing various protein   sources). Therefore, the inconsistent responses to   dietary organic acids in broiler chickens are likely   associated with the specific chemical properties   of experimental diets such as buffering capacity.   Another possible factor causing variation in results   may be experimental conditions such as the sanitation level of the environment. Dietary organic acids may   affect the microbial population in the GIT. It may be   expected, therefore, that the antimicrobial effects of   organic acids would be more pronounced when birds   are exposed to less sanitary conditions (Kil <i><i>et al.,	</i></i>	   2010). Therefore, difference in sanitary conditions   among experiments may be the possible reason for   the inconsistent results. In addition, based on the data   we have reviewed, feed palatability is likely affected   by the sources and inclusion levels of dietary organic   acids, and therefore appears to influence the efficacy   of dietary organic acids. More research is required to   determine the effects of dietary organic acids on feed   palatability or feed choice in broiler chickens.</p>     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">Conclusions </font></b>     <p align="left">Dietary organic acids have been considered as   potential alternatives to AGPs for improving growth   performance and health status of broiler chickens.   The possible mode of action of organic acids supports   the notion that they could be effective in broiler   chickens. The pH reduction in the GIT through diet   acidification leads to an increase in nutrient utilization   and inhibition of pathogenic bacterial growth. Direct   growth-inhibiting effects on pathogenic bacteria have   also been identified. However, the effects of various   sources and inclusion levels of organic acids on the   pH of the GIT appear to be limited to the upper part   of the GIT because these acids are highly absorbable,   and thus little amounts of dietary organic acids may   reach the lower part of the GIT. A protected form of   dietary organic acids may overcome this problem and   further experiments are needed to study the effects   of the protected forms of organic acids on the pH of   the GIT. It is also difficult to confirm the effects of   organic acids on nutrient utilization because the extent   of improvements in nutrient retention appears to be   smaller than anticipated. As previous reviews have   reported, we observed that most dietary organic acids   improve growth performance of broiler chickens,   despite some inconsistent results. However, the   appropriate inclusion levels are unknown, and no   clear dose-dependent responses to dietary organic   acids are available. Differences in dietary ingredients,   physical and chemical properties of the diets, and   rearing conditions are most likely responsible for   these variations. Therefore, it is difficult to conclude whether dietary organic acids have consistently   positive effects on growth performance, and whether   they are promising alternatives to AGPs for broiler   chickens. Further studies are needed to elucidate   the mode of action of dietary organic acids and their   effects on growth performance of broiler chickens.</p>     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">Acknowledgements</font></b></p>     <p align="left">This research was carried out with the support of the Cooperative Research Program for Agriculture Science and Technology Development (ID: PJ010932042015), Rural Development Administration, Republic of   Korea. This research was also supported by the   Chung-Ang University Research Scholarship Grants in 2015.</p>     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">Conflicts of interest</font></b></p>     <p align="left">The authors declare they have no conflicts of interest with regard to the work presented in this report.</p>     ]]></body>
<body><![CDATA[<p align="left">&nbsp;</p> <hr size="1">     <p align="left"><b><font size="3">Notes</font></b></p>     <p align="left"><font size="4"><b><a name="a1"><a href="#a0">&curren;</a></a></b></font>To cite this article: Kim JW, Kim JH, Kil DY. Dietary organic acids for broiler chickens: a review. Rev Colomb Cienc Pecu 2015; 28:109-123.</p> <hr size="1">     <p align="left">&nbsp;</p>     <p align="left"><b><font size="3">References</font></b></p>     <p align="left">Afsharmanesh M, Pourreza J. Effects of calcium, citric acid,   ascorbic acid, vitamin D<sub>3</sub> on the efficacy of microbial phytase   in broiler starters fed wheat-based diets I. Performance, bone   mineralization and ileal digestibility. Int J Poult Sci 2005; 4(6):418-424.</p>     <p align="left">Aghazadeh AM, TahaYazdi M. Effect of butyric acid   supplementation and whole wheat inclusion on the performance and carcass traits of broilers. S Afr J Anim Sci 2012; 42:241-248.</p>     <p align="left">Akyurek H, Ozduven ML, Okur AA, KocF, Samli HE. The effect   of supplementing an organic acid blend and/or microbial phytase   to a corn-soybean based diet fed to broiler chickens. Afr J Agric Res 2011; 6:642-649.</p>     <p align="left">Al&ccedil;i&ccedil;ek A, Bozkurt M, &Ccedil;abuk M. The effect of a mixture of   herbal essential oils, an organic acid or a probiotic on broiler performance. S Afr J Anim Sci 2004; 34:217-222.</p>     <p align="left">Al-KassiAG, Mohssen MA. Comparative study between single   organic acid effect and synergistic organic acid effect on broiler performance. Pak J Nutr 2009; 8:896-899.</p>     ]]></body>
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</article>
