Animal Health Research Applications of butyric acid in poultry

Reviews
production: the dynamics of gut health,
cambridge.org/ahr performance, nutrient utilization, egg quality,
and osteoporosis‡
Review Mohamed T. El-Saadony1, *, Muhammad Umar Yaqoob2, *, Faiz-ul Hassan3,
*These authors contributed equally to this Mahmoud Alagawany4, Muhammad Arif5, Ayman E. Taha6, Shaaban S. Elnesr7 ,
manuscript.
Khaled A. El-Tarabily8,9 and Mohamed E. Abd El-Hack4
‡
This article was originally published with an
1
incorrect author name. A correction notice has Department of Agricultural Microbiology, Faculty of Agriculture, Zagazig University, Zagazig, 44511, Egypt;
2
been published and the error corrected in the College of Animal Science, Zhejiang University, Hangzhou, 310058, P. R. China; 3Institute of Animal and Dairy
HTML and PDF versions. Sciences, University of Agriculture, Faisalabad, Pakistan; 4Poultry Department, Faculty of Agriculture, Zagazig
University, Zagazig, 44511, Egypt; 5Department of Animal Sciences, College of Agriculture, University of Sargodha,
Cite this article: El-Saadony MT, Umar Yaqoob
Sargodha, Punjab, Pakistan; 6Department of Animal Husbandry and Animal Wealth Development, Faculty of
M, Hassan F, Alagawany M, Arif M, Taha AE,
Veterinary Medicine, Alexandria University, Edfina, 22758, Egypt; 7Department of Poultry Production, Faculty of
Elnesr SS, El-Tarabily KA, Abd El-Hack ME
(2022). Applications of butyric acid in poultry Agriculture, Fayoum University, Fayoum, 63514, Egypt; 8Department of Biology, College of Science, United Arab
production: the dynamics of gut health, Emirates University, Al-Ain, 15551, United Arab Emirates and 9Harry Butler Institute, Murdoch University, Murdoch,
performance, nutrient utilization, egg quality, 6150, Western Australia, Australia
and osteoporosis. Animal Health Research
Reviews 23, 136–146. https://doi.org/10.1017/
Abstract
S1466252321000220
Due to the increasing demand for antibiotic-free livestock products from the consumer side
Received: 9 June 2021 and the ban on the use of antibiotic growth promoters, the poultry feed industry is increas-
Revised: 16 October 2021
Accepted: 22 December 2021
ingly interested in developing more alternatives to cope with this problem. Organic acids
First published online: 14 November 2022 (butyric acid) have many beneficial effects on poultry health, performance, and egg quality
when used in their diet, thus they can be considered for the replacement of antibiotics in livestock
Key words: production systems. Butyric acid is most efficacious against pathogenic bacteria such as
Butyric acid; gut health; nutrient utilization;
Salmonella spp. and Escherichia coli, and stimulates the population of beneficial gut bacteria. It
osteoporosis; performance
is a primary energy source for colonocytes and augments the differentiation and maturation of
Authors for correspondence: the intestinal cells. Collectively, butyric acid should be considered as an alternative to antibiotic
Shaaban S. Elnesr, growth promoters, because it reduces pathogenic bacteria and their toxins, enhancing gut health
E-mail: [email protected];
thereby increasing nutrient digestibility, thus leading to improved growth performance and
Khaled A. El-Tarabily,
E-mail: [email protected] immunity among birds. The possible pathways and mechanisms through which butyric acid
enhances gut health and production performance are discussed in this review. Detailed informa-
tion about the use of butyric acid in poultry and its possible benefits under different conditions are
also provided, and the impacts of butyric acid on egg quality and osteoporosis are noted.

Introduction
Butyric acid is one of the short short-chain fatty acids (SCFAs) generated at millimolar levels
in the bird cecum, which is the major site for microbial fermentation of unabsorbed starch
(Liu et al., 2017). Butyric acid in its unprotected form is rapidly absorbed in the upper gastro-
intestinal tract (GIT), suggesting that protection is needed to positively affect the small intes-
tine (Kaczmarek et al., 2016; Elnesr et al., 2020; Silva et al., 2020).
Due to bans on using in-feed antibiotic growth promoters, the poultry industry has been
focused on finding new ways to improve performance through improving nutrient and energy
utilization while maintaining and potentially improving the health of poultry without using
antibiotic growth promoters. The uses of organic acids for improving performance parameters
in both layers and broilers have been increasingly explored. Organic acids, including butyric
© The Author(s), 2022. Published by acid and its salts, have shown positive effects on growth performance, egg production, and
Cambridge University Press. This is an Open egg quality due to the source of the acid, diet composition and environment (Soltan, 2008;
Access article, distributed under the terms of
Elnesr et al., 2019; Maty and Hassan, 2020).
the Creative Commons Attribution licence
(http://creativecommons.org/licenses/by/4.0/), Organic acids, such as butyric acid, improve gut health by providing carbon sources for villi
which permits unrestricted re-use, distribution growth, promoting the growth of beneficial bacteria (lactobacilli and Bifidobacteria), and
and reproduction, provided the original article decreasing harmful bacteria (Salmonella, Clostridium, and Escherichia coli) by decreasing
is properly cited. luminal pH. Improved gut health is theorized to allow increased absorption, resulting in
increased nutrient and energy utilization in poultry, thereby improving performance
(Qaisrani et al., 2015; Maty and Hassan, 2020).
In layer farming, egg production and egg quality are of great economic concern. Improved
egg quality can be identified as improving eggshell strength while maintaining a good egg size.

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 Animal Health Research Reviews 137

Fig. 1. Effect of butyric acid and its salts to enhance

the growth performance of poultry. +, improve or
enhance; −, lower or decrease. Butyric acid has a pro-
nounced effect on gut health through different ways. It
decreases the pH of the gut and digesta, which is gener-
ally good for beneficial bacteria (Lactobacillus and
Bifidobacterium spp.) and toxic for pathogenic bacteria
like Salmonella and Escherichia coli. Reduction in the
population of pathogenic bacteria increases the avail-
ability of nutrients to beneficial bacteria and the host.

Calcium is a major component of the layer diet and is incorpo- about 25–30% butyric acid, which is very low; therefore, future
rated into both eggshell and bone (Clunies et al., 1992; Makled research should involve means to coat butyric acid while increas-
et al., 2019) by absorption from the small intestine (Saunders- ing its concentration to maximize its benefit.
Blades et al., 2009). As the hen ages, its ability to absorb nutrients,
including calcium, declines, decreasing eggshell thickness and thus
breaking strength. This leads to increased economic losses due to
broken eggs (Molnár et al., 2018; Maty and Hassan, 2020). Butyric acid as an alternative to antibiotics
Organic acids improve the mineral absorption from the intes- In areas of the world such as the European Union and the United
tine by lowering the pH of digesta and inhibiting the formation of States, antibiotics/antibiotic growth promoters are no longer being
calcium-phytate complexes (Boling et al., 2000; Rafacz-Livingston added to poultry diets (Opinion of the Economic and Social
et al., 2005). It has been found that supplementation of butyric Committee, 1998; Ricke, 2003; Deepa et al., 2018), due to the high
acid and its salts (sodium butyrate) increases serum calcium, concentrations of antibiotic residues found in meat and meat pro-
phosphorus (Mahdavi and Torki, 2009; Adil et al., 2010; Kamal ducts, undesired changes in the microbial communities of the
and Ragaa, 2014), and magnesium levels (Kamal and Ragaa, GIT (Kulshreshtha et al., 2014), and increase in antibiotic resistance
2014). This review aims to provide current knowledge about the in pathogenic bacteria (Ricke, 2003; Raza et al., 2019).
effects of butyric acid on gut health, performance, nutrient utiliza- Ideally, alternative supplements would improve growth per-
tion, immunity, osteoporosis, and egg quality in poultry. formance by acting to improve feed efficiency and nutrient
absorption and utilization, as well as to regulate microbial popu-
lations in such a way to promote the growth of beneficial
Different formulations of butyric acid
microbes and reduce pathogenic microbes in the GIT (Biggs
The efficacy of butyric acid was improved when fed in a coated and Parsons, 2008; Deepa et al., 2018). Organic acids, specifically
form, such as encapsulation, suggesting that such protection posi- SCFAs, are considered as alternatives. Detailed interactions of
tively affected the GIT (Kaczmarek et al., 2016; Elnesr et al., 2020). butyric acid to enhance the growth performance of poultry
Previous studies showed variable results, perhaps due to factors through different systems are presented in Fig. 1. Most
such as age, nutrition, diet structure, experimental conditions, European Union member states generally regard organic acids
flock health, source of butyric acid, and inclusion rate and their salts as safe, and they have approved them for use as
(Taherpour et al., 2009; Levy et al., 2015; Qaisrani et al., 2015; feed additives for livestock and poultry production (Adil et al.,
Kaczmarek et al., 2016). 2011).
Kaczmarek et al. (2016) found that protected butyrate at vari- SCFAs can also be described as saturated straight-chain mono-
ous doses significantly improved villi height and apparent metab- carboxylic acids, fatty acids, volatile fatty acids, and weak or car-
olizable energy (AME) in broilers, while Levy et al. (2015) found boxylic acids. Originally, SCFAs were added to animal feed to
no significant effect of encapsulated butyric acid on villi height prevent fungal growth (Dixon and Hamilton, 1981). Propionate
compared to controls in broilers. These variations in findings sug- and formic acid (and various combinations) have bactericidal
gest a need for further research to determine the optimal source activity in feeds contaminated with foodborne pathogens such
and inclusion rate of butyric acid, to overcome the variation as Salmonella spp. (Ricke, 2003; Raza et al., 2019), and butyric
seen due to other potential factors. acid is thought to reduce intestinal populations of pathogenic bac-
Currently, poultry feed manufacturers tend to produce coated teria in different ways (Figs 2 and 3). Butyric acid is now increas-
types of butyric acid to overcome its odor and rapid volatility. ingly researched as a feed additive for poultry due to its proposed
However, the problem of traditional coated products is the low effectiveness to improve feed conversion efficiency, gut health,
concentration of butyric acid, as coated salts usually include and growth performance (Deepa et al., 2018; Imran et al., 2018).

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 138 Mohamed T. El‐Saadony et al.

Fig. 2. Indirect bactericidal effects of butyric acid.

Fig. 3. Direct bactericidal effects of butyric acid.

Sources of butyric acid 2016). Adil et al. (2011) suggested that reduced feed intake can
be observed due to reduced palatability of the feed when SCFAs
Butyric acid, along with other SCFAs, is produced in millimolar are supplemented in their acid form (properties of butyric acid
amounts in the GITs of people and animals, within locations are presented in Fig. 4).
that predominantly contain strictly anaerobic microflora (Ricke, Another advantage of butyric acid supplemented in salt form
2003). For poultry, this area is the cecum, which is the major is that it is less corrosive and more water-soluble (Khan and
site of microbial fermentation of unabsorbed starch (Liu et al., Iqbal, 2016; Silva et al., 2020). Butyric acid is quickly absorbed
2017), non-starch polysaccharides (Levy et al., 2015), and proteins and metabolized by mucosal cells. Absorption and metabolism
(Kulshreshtha et al., 2014). Butyric acid, propionic acid, and acetic of butyric acid begin in the mucosa of the crop, and this process
acid are the major byproducts of these processes (Liu et al., 2017). continues throughout the GIT. This rapid absorption limits the
Butyric acid is most effective in its undissociated (non-ionized, amount of butyric acid that will arrive in and affect the small
more lipophilic) form (Leeson et al., 2005; Wu et al., 2018), but is intestine. Butyrate can be microencapsulated to reduce rapid
often supplemented as butyrate in the diet because of its volatile absorption, thus helping improve its efficiency by allowing it to
nature (Liu et al., 2017) and pungent smell (Kaczmarek et al., stay intact until it arrives in the small intestine. A common

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 Animal Health Research Reviews 139

had an anorexic (appetite-reducing) effect, which was considered

unusual for 1 g kg−1 of supplemented butyrate (Ahsan et al., 2016;
Moquet et al., 2018). Studies have found that this anorexic effect
caused by butyrate (and other SCFAs) is modulated by colonic
L-cells that produce glucagon-like peptide 1 (GLP-1) and peptide
YY (PYY). GLP-1 is released in the presence of digested protein as
well as free fatty acids. PYY has an orexigenic
(appetite-stimulating) effect in chickens, whereas it has an anor-
exic effect in rodents. PYY acts directly on the hypothalamus
and triggers cholecystokinin (CCK), which promotes the satiety
effect via the vagus nerve, reducing rodent appetite. The mechan-
ism by which an orexigenic effect occurs in poultry is unclear
(Furness et al., 2013; Maty and Hassan, 2020).
In poultry, L-cells are located all along the distal small intes-
tine, but the colon is the main site of anorexic effects (Moquet
et al., 2018). L-cells are enteroendocrine cells that function by
stimulating carbohydrate uptake, releasing insulin, and slowing
intestine transit (Furness et al., 2013; Wu et al., 2018). Moquet
et al. (2018) reported that anorexic effects were reduced when
butyrate was delivered to the crop, gizzard, and proventriculus
in the unprotected form. It was also found that butyrate in the
Fig. 4. Properties of butyric acid. colon and ceca, in the protected form, increased total tract reten-
tion times, allowing more time for absorption and thus improved
feed efficiency. Very few studies have demonstrated a link between
method of encapsulation is stearin or vegetable fat, and it has colon motility and the butyrate effects (Moquet et al., 2018;
been found that this method has had positive effects on gut Makled et al., 2019).
morphology and reduction of pathogen colonization in the intes- SCFAs have also been found to increase ileal proglucagon
tine (Liu et al., 2017; Makled et al., 2019). mRNA, protein, and glucose transporter (GLUT-2) expression,
In a study by Liu et al. (2017), researchers created an assay to potentially improving gut epithelial cell proliferation (Adil et al.,
determine the optimal time for butyric acid release from the GIT 2010; Ahsan et al., 2016). In addition to finding which butyrate
for broilers. It was found that encapsulated butyric acid aiming to source is most effective, researchers have begun to examine
stimulate epithelial cell development and improve digestibility which diet composition and form is best suited to maximize the
should release at 30 min to 2.5 h post-ingestion; to focus on effects of butyric acid and its salts when added to different
hind gut control, and the release should be at 2.5–4 h post- diets. A portion of studies carried out by Zhou et al. (2014)
ingestion (Liu et al., 2017; Makled et al., 2019). Butyric acid and Qaisrani et al. (2015) looked at how the relationship between
needs to be in its undissociated form before it arrives at the hind- diet structure (coarse or fine) and butyric acid supplementation
gut to utilize its antimicrobial effect. Meanwhile, release in the (with or without) affected growth performance and gut morph-
small intestine should affect villi development and nutrient digest- ology in broilers. It was found that feeding a course diet supple-
ibility (Liu et al., 2017). mented with butyric acid positively affected performance,
Butyrate in its free form is used mostly as a feed sanitizer decreased crypt depth, and increased villus height to crypt
rather than as a supplement because it is quickly absorbed in depth ratio when added to a poorly digestible protein source
the crop (Leeson et al., 2005; Maty and Hassan, 2020). (Qaisrani et al., 2015).
Unprotected butyrate is active in the crop, proventriculus, and
gizzard. Tributyrin (a triglyceride of butyrate) is active in the
Gut health
small intestine and fat-coated/encapsulated butyrate is active in
the ceca and colon (Moquet et al., 2018; Deepa et al., 2018). The impact of butyric acid on gut health is presented in Fig. 5.
Butyrate facilitates passage to the lower GIT where butyrate is Gut health can be affected by nutrition, environment, or infec-
released by lipase activity (Moquet et al., 2018). Monobutyrin tious disease agents. There is a direct relationship between gut
has been used to potentially improve growth performance in health and animal performance, and many researchers have
broilers (Ahsan et al., 2016; Bedford et al., 2017). attempted to create a gut health scoring index that can be applied
A recent study by Bedford et al. (2017) found that supplement- to poultry diets (Kraieski et al., 2017). Researchers spend more
ing tributyrin alone had no significant effect on growth perform- time studying gut health because it is a major factor in the per-
ance in broilers, whereas mixtures of mainly monobutyrin and formance of both broilers and layers (Grashorn et al., 2013;
tributyrin, with some dibutyltin, had positive effects on growth Silva et al., 2020). Optimal gut health is characterized in several
performance. Sodium butyrate promotes water absorption and ways. One of them is the villi height to crypt depth ratio. A
proliferation of epithelial cells, provides energy, stimulates the high ratio indicates mature and well-functioning villi with a shal-
synthesis of gastrointestinal hormones, and stimulates intestinal low crypt that constantly provides cell renewal (Kaczmarek et al.,
blood flow in broiler chicks (Hu and Guo, 2007). 2016). Improved gut health has also been attributed to the
In a study by Moquet et al. (2018), three forms of butyrate increased length of the GIT, allowing increased absorption (Adil
were tested in a diet with a poorly digestible protein source, to et al., 2011).
investigate the effect of butyrate on various parts of the GIT. It Dietary supplementation with organic acid supports the gut
was reported that the presence of butyrate beyond the gizzard health of poultry species (Alagawany et al., 2021). Butyric acid

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 140 Mohamed T. El‐Saadony et al.

Fig. 5. Impacts of butyric acid on gut health.

Fig. 6. Mode of action of butyric acid.

can improve epithelial cell development (Levy et al., 2015). ATP synthase, depleting its cellular energy (Fig. 3) (Biggs and
Butyric acid is also thought to effectively preserve cell viability Parsons, 2008; Zhou et al., 2014). The microbe is then no longer
and enhance enterocyte turnover, which may improve intestinal able to multiply efficiently (Adil et al., 2011). Butyric acid can
recovery. It has been observed that butyrate supplementation have antimicrobial effects by decreasing the luminal pH and redu-
can increase villi height and decline crypt depth in poultry and cing bacterial colonization in the intestinal wall (Panda et al.,
other non-ruminant animals, thereby increasing the absorptive 2009; Elnesr et al., 2020), resulting in less damage to epithelial
surface (Qaisrani et al., 2015; Wu et al., 2018; Elnesr et al., cells (Qaisrani et al., 2015; Wu et al., 2018).
2019). SCFAs are theorized to have several mechanisms of anti- Damaging epithelial cells can disrupt the barrier between the
microbial activity. One of the most widely accepted mechanisms internal and external environment of the lumen, allowing toxins
by which butyric acid can destroy pathogenic bacteria and express to enter the circulation and increasing the susceptibility of the
its antibacterial activity is that the acid changes the internal pH intestine to colonization by pathogenic bacteria (Abdelqader
of the microbe (depolarization) and therefore disrupts nutrient and Al-Fataftah, 2016). Butyric acid functions by inhibiting
synthesis and transport as well as energy metabolism of that Salmonella colonization in the ceca due to the improvement of
microbe (Figs 2 and 6) (Adil et al., 2011). intestinal barrier function (Abdelqader and Al-Fataftah, 2016)
Organic acids can penetrate the surrounding membranes of and downregulates Salmonella gene expression (Liu et al., 2017).
bacteria. Once inside the membrane, they will dissociate, forming Decreasing luminal pH is also beneficial because it stimulates
H+ ions as a result of the neutral pH, releasing excess protons that the growth of beneficial bacteria and hampers the growth of
will lower the pH. The microbe will then attempt to maintain a pathogenic bacteria (Adil et al., 2010). Commonly, pathogen
neutral pH by transporting excess protons outside of cells via growth is likely to occur in the GIT when the lumen of the

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 Animal Health Research Reviews 141

Table 1. Effect of various forms and levels of butyric acid supplementation on gut morphology and bacterial count in broiler compared to control group

Inclusion Age
Source levels (%) (days) Response Reference

Gut morphology VL CD VL/CD Others effects

Blend of acetic acid, butyric 0.3 49 +* +* +* + Epithelium thickness Maty and Hassan (2020)
acid and formic acid + Surface area
Encapsulated butyric acid 0.05 21 +* +* +* Jazi et al. (2018)
Encapsulated sodium butyrate 0.1 11 +* +* NA Liu et al. (2017)
Protected or unprotected 0.1 21 NA NA NA No effect on gut weight Moquet et al. (2018)
butyrate and retention time
Sodium butyrate 0.1 21/35 +* NA +* Sikandar et al. (2017)
Encapsulated butyrate 0.05 42 NA NA NA + Intestinal weight* Abdelqader and
+ Epithelial cell area* Al-Fataftah (2016)
Protected calcium butyrate 0.03 42 +* +* +* + Mucosa thickness Kaczmarek et al. (2016)
Encapsulated butyric acid 0.3 42 NA NA NA No effect on surface area Levy et al. (2015)
Butyric acid 3 42 − Crop pH Adil et al. (2011)
+ GIT length
Butyric acid 3 42 +* NA Adil et al. (2010)
Sodium butyrate 0.05 42 +* +* Hu and Guo (2007)
Butyric acid 0.2 42 NA NA Leeson et al. (2005)
Gut bacteria
Sodium butyrate 0.06 21 + Lactobacilli; - Escherichia coli in Ileum Makled et al. (2019)
Encapsulated butyric acid 0.05 21 + Lactobacilli and Bifidobacterium* Jazi et al. (2018)
− Salmonella and Coliform*
Butyric acid 0.1 42 − Salmonella count in caecum Cerisuelo et al. (2014)
Butyric acid 3 42 − Caecal coliform count* Adil et al. (2011)
Free or protected sodium 0.09 42 − Salmonella enteritidis* in crop, cecum and liver Fernandez-Rubio et al.
butyrate (2009)
Sodium butyrate 0.05 42 − Lactobacilli and Escherichia coli populations* Hu and Guo (2007)
Butyric acid 0.16 42 − Salmonella in caecum Van Immerseel et al.
(2004)
VL, villus length; CD, crypt depth; VL/CD, villus length/crypt depth; GIT, gastrointestinal tract; NA, not affected; *significant effect (P < 0.05); +, enhanced/improve; −, reduced/lower.

small intestine and ceca exceed a pH of 5.8–6.0 and the large Immunity
intestine exceeds pH 6.2 (Brzóska et al., 2013). In a study by
Butyric acid has a positive impact on bird immunity through the
Adil et al. (2010), villus height was significantly different in the
improvement of gut eubiosis, increasing number of beneficial bac-
duodenum and jejunum when chicks were fed organic acids,
teria, limiting the colonization of pathogens, and improving gut
with the highest height in chicks consuming the 3% butyric
pH, and all these factors positively reflected on the birds’ immune
acid diet. It was suggested that the significant growth of the villi
responses (Sikandar et al., 2017). It was found that the inclusion
was due to a reduction in the growth of pathogenic and non-
of butyric acid in poultry ration was associated with better
pathogenic bacteria, decreasing colonization and inflammatory
cell-mediated immune responses in chickens 48 h after-
responses of the intestinal mucosa (Adil et al., 2010; Silva et al.,
phytohemagglutinin-P inoculation, improved humoral immunity,
2020).
and better antibody production after Newcastle disease vaccine
Inflammation of the intestinal mucosa due to increased
and injection of sheep red blood cells. This resulted in better thy-
pathogenic activity can lead to necrosis of the intestinal epi-
mus and spleen weight with better thymus medulla and germinal
thelium (Brzóska et al., 2013). Crypt depth was not affected
spleen centers. It also improved the intestinal villi length and
compared to broilers fed the control diet (Adil et al., 2010).
depth, and increased goblet cells containing mucins of acidic
A study by Hu and Guo (2007) found that supplemented
nature (Sikandar et al., 2017).
sodium butyrate at 2000 mg kg−1 in broilers had no effect on
jejunal villi height and crypt depth and significantly increased
Performance parameters
the villi height to crypt depth ratio when compared to the con-
trol. Table 1 shows the effect of different sources of butyric Increased absorption efficiency due to improved gut health has
acid, at varying levels, on different parameters related to gut led to various effects on performance parameters in broilers and
health. laying hens, depending on the forms of butyric acid used and

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 142 Mohamed T. El‐Saadony et al.

Table 2. Effect of various forms and levels of butyric acid supplementation on growth performance of broiler compared to control group

Feed intake Weight

(%) gain (%)
Inclusion Age +, % increase;
Source levels (%) (days) −, % decrease FCR Reference

Blend of acetic acid, butyric 0.9 49 −34.54* +0.98 Improved (−1.09)* Maty and Hassan (2020)
acid and formic acida
Butyric acid 0.2 42 −1.1 −4.57 Improved (−0.08) Nari and Ghasemi (2020)
Sodium butyrate 0.06 42 +2.38 +1.57 Poor (+0.02) Makled et al. (2019)
Encapsulated butyric acid 0.05 21 −1.55* −7.16* Poor (+0.08)* Jazi et al. (2018)
Monobutyrin 0.3 35 – +7.17 Improved (−0.07) Bedford et al. (2017)
Combined monobutyrin/ 0.05/0.2 +9.27 Improved (−0.07)
tributyrin
Encapsulated sodium butyrate 0.1 11 – +17.01 Improved (−0.42) Liu et al. (2017)
Fat-coated butyrate 0.1 21 −6.36 +1.47 Improved (−0.07) Moquet et al. (2018)
Sodium butyrate 0.1 35 −9.86* +18.87* Improved (−0.26) Sikandar et al. (2017)
Encapsulated butyrate 0.05 42 −1.64 +2.82 Improved (−0.07) Abdelqader and
Al-Fataftah (2016)
Protected calcium butyrate 0.04 42 −2.98 +3.08 Improved (−0.08)* Kaczmarek et al. (2016)
0.03 +3.13 +9.42* Improved (−0.09)*
Encapsulated sodium butyrate 0.025 42 – +0.7 Poor (+0.06) Abd El-Ghany et al.
(2016)
Butyric acid 0.25 42 +2.32 +5.29 Improved (−0.03) Dehghani-Tafti and
Jahanian (2016)
Butyric acid 0.3 42 +8.19 Improved (−0.09) Lakshmi and Sunder
(2015)
Encapsulated butyric acid 0.03 42 +0.46 +3.15* Improved (−0.04)* Levy et al. (2015)
0.05 – +2.05* Improved (−0.04)*
Encapsulated sodium butyrate 0.07 42 – +5.7 Improved (−0.06) Chamba et al. (2014)
Butyric acid 3 42 −1.05 +9.41* Improved (−0.21)* Adil et al. (2011)
Butyric acid 3 42 +0.06 +9.26* Improved (−0.17)* Adil et al. (2010)
Butyric acid 0.2 42 10.98* +8.05* Improved (−0.35)* Taherpour et al. (2009)
Sodium butyrate 0.05 42 +1.23 +3.03 Improved (−0.03) Hu and Guo (2007)
Butyric acid 0.2 42 +0.67 +2.32 Improved (−0.03) Leeson et al. (2005)
0.1 −4.44 +0.57 Improved (−0.09)
FCR, feed conversion ratio.
a
Experimental bird was Japanese quail.
*Significant difference (P < 0.05).

the inclusion rate. Researchers have found that butyric acid sup- diet and the forms of butyrate (calcium salt, sodium salt, glycer-
plementation had positive effects on body weight gain (BWG) ide, etc.) (Leonel and Alvarez-Leite, 2012; Kaczmarek et al., 2016).
and feed conversion rate (FCR) in broilers (Leonel and In a study by Kaczmarek et al. (2016) with broilers, researchers
Alvarez-Leite, 2012; Liu et al., 2017). Detailed data regarding attempted to find a ‘matrix value’ for butyrate in poultry diets to
the effects of butyric acid on different growth performances are maximize its efficacy. The experiment showed that butyric acid
presented in Table 2. positively affected FCR and BWG, and the addition of 0.2 g
Several studies have shown that butyric acid does not signifi- kg−1 of butyrate improved FCR, 0.3 g kg−1 improved FCR regard-
cantly affect feed consumption. A significant difference in FCR less of the age of birds. In comparison, 0.4 g kg−1 decreased feed
and BWG was seen in favor of organic acids, suggesting better intake (FI) and significantly increased FCR. This study indicated
absorption and nutrient utilization than birds on the control that the 0.3 g kg−1 provided produced the most positive effects
diet (Adil et al., 2010). It was also found in this study that compared to the control and other butyrate doses. Leeson et al.
there were higher serum calcium and phosphorus concentrations (2005), found contradictory results, when 0.2 g kg−1 butyrate
when compared to the control (Adil et al., 2010). When research- was supplemented as a glyceride. This addition maintained the
ing butyric acid, there are often contradiction due to the type of performance and carcass quality in vaccinated broilers challenged

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 Animal Health Research Reviews 143

Fig. 7. Impacts of adding butyric acid in poultry feed.

with coccidia. It was also found that butyrate in the glyceride form for intermediary metabolism (Adil et al., 2011). Butyric acid can
caused FI depression similar to that of 0.4 g kg−1 in the increase the feed solubility, digestion, and nutrient absorption
Kaczmarek et al. (2016) experiment. Abdelqader and (Rahman et al., 2008; Leonel and Alvarez-Leite, 2012).
Al-Fataftah (2016) found that 0.5 g of butyric acid kg−1 diet recov- With fewer pathogenic bacteria, due to organic acids, there is a
ered intestinal epithelia and improved integrity in heat-stressed reduced microbial metabolic need, thereby allowing more nutri-
broilers compared to controls. ents to be available for absorption by the host. The decrease in
A study by Taherpour et al. (2009) showed that broilers sup- the toxins produced by harmful bacteria can also cause an
plemented with butyric acid glyceride showed improved BWG increase in energy availability and protein digestibility (Adil
compared to the control. In this study, the contradiction of et al., 2010; Silva et al., 2020). Adil et al. (2011) suggested that
these results compared to other studies was attributed to differ- increased protein digestibility because feeding organic acids in
ences in preparation of the diet composition or particle size and the diet reduces gastric pH resulting in increased pepsin activity.
experimental conditions. Like the studies above, FCR improved Pepsin proteolysis of proteins releases peptides that trigger hor-
while FI was increased in favor of butyric acid glyceride. There mones such as CCK and gastrin to be released. These hormones
was no significant difference in mortality in this study. Brzóska play a significant role in the digestion and absorption of proteins
et al. (2013) suggested that the use of organic acids in the diet pro- (Adil et al., 2011).
motes the production of prebiotics and probiotic lactic acid bac- Goodarzi Boroojeni et al. (2014) noted that the effects of
teria in young birds. organic acids on digestibility were debatable due to multiple fac-
Brzóska et al. (2013) and Zhou et al. (2014) noted that, in sev- tors affecting the results. There was no significant effect found for
eral studies, organic acids, including butyric acid, significantly nutrient digestibility in this study compared to the control for
reduced mortality when compared to controls. Finally, the per- broilers. Kaczmarek et al. (2016) found that, 0.2, 0.3, and 0.4 g
formance improvement may be attributed to the role of butyric kg−1 of butyrate increased the AME compared to the control
acid in the control of the intestinal barrier, supplying energy to diet for broilers, due to the significant increase in villi height
the colonocytes, augmenting the differentiation and maturation and numerically increased mucosal thickness observed in this
of the intestinal cells, thus nutrient utilization, feed efficiency, study.
and the positive immune response of birds. The impacts of adding
butyric acid in poultry feed are illustrated in Fig. 7.
Egg quality
Improved egg quality can be identified as improving eggshell
Metabolizable energy and nutrient utilization
strength while maintaining a good egg size. Laying hens must
Organic acids have been found to increase the digestibility of cal- consume the correct ratio of manganese, vitamin D, calcium,
cium, phosphorus, magnesium, zinc, and protein (Adil et al., and phosphorus to produce strong eggshells. As the hen ages,
2010). Supplementation of organic acids in broiler diets enhanced mucosal cells in the duodenum have weakened villi, which
serum calcium and phosphorus concentrations. These results begin to shorten, and absorption in the small intestine decreases,
were credited with the notion that acidic ions form a complex resulting in reduced eggshell quality (Sengor et al., 2007). Sengor
with minerals such as calcium and phosphorus, thereby increas- et al. (2007) suggested that butyrate can function in maintaining
ing their digestibility (Table 3). Organic acids also act as substrates the mucosa and epithelial cells. In this study, improvements in

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 144 Mohamed T. El‐Saadony et al.

Table 3. Effect of various forms and levels of butyric acid supplementation on nutrient digestibility of broiler compared to control group

Inclusion levels Age

Source (%) (days) Nutrient digestibility coefficient Reference

Butyric acid 0.2 42 No significant effect on DM, CP, EE, Ca, P, and AME Nari and Ghasemi
(2020)
Encapsulated butyric acid 0.05 21 No significant difference in intestinal digestive enzyme Jazi et al. (2018)
(amylase, protease, and lipase) activities
Encapsulated sodium 0.1 11 Significantly improved ileal energy digestible coefficient Liu et al. (2017)
butyrate
0.05 or 0.1 42 Significantly improved ileal energy digestible coefficient
Protected or unprotected 0.1 21 No significant effect on DM, OM, Nitrogen, and NPN Moquet et al.
butyrate (2018)
Protected calcium 0.04 42 Significantly improved total tract digestibility and AME Kaczmarek et al.
butyrate (2016)
0.03 Significantly improved fat and AME digestibility
DM, dry matter; OM, organic matter; CP, crude protein; EE, ether extract; Ca, calcium; P, phosphorus; AME, apparent metabolizable energy; NPN, non-protein nitrogen.

eggshell strength and increased egg production were observed and et al., 2008). Work is needed to improve the perception of
attributed to the healing of damaged epithelial cells in addition to the effects of butyric acid on egg quality and what can be done
increased villi growth (Sengor et al., 2007; Sikandar et al., 2017). in the future to better utilize butyric acid as an antibiotic
Maintaining a high eggshell breaking strength is needed to alternative.
protect the egg from penetration by pathogenic bacteria. Broken
shells are a significant source of economic losses for producers
(Świątkiewicz et al., 2010). The formation of a normal (not mis- Osteoporosis
shapen) eggshell requires minerals to be released from the shell Osteoporosis can be described as an increased porosity and
gland in the right proportions, at the right time, to ensure good reduced bone thickness, which is a major bone-related disease
eggshell quality. There must be adequate absorption and metabol- that can occur when there is an increased demand for calcium
ism of nutrients to achieve this physiologic state (Sengor et al., from the medullary bone for the eggshell formation and mainten-
2007). Butyrate has improved calcium metabolism and absorption ance of eggshell quality. This reduced thickness can result in bone
by increasing villi growth (Rahman et al., 2008). breakage. In hens, osteoporosis manifests as cage layer fatigue
Sengor et al. (2007) suggested that weakness in the eggshell in (Webster, 2004; Khan and Iqbal, 2016). Cage layer fatigue can
older hens can be altered with butyrate, if supplemented at 285 be identified by the inability of hen to stand or walk. These
mg kg, resulting in increased eggshell strength and decreased mal- hens tend to have a willingness to eat or drink. The hen will die
formed eggs. Świątkiewicz et al. (2010) reported that one of the if cage layer fatigue is not treated. Cage layer fatigue can be clas-
main concerns is a decrease in eggshell quality as the hen ages sified as peracute and acute. Peracute fatigue occurs when the hen
due to an increase in egg weight without an increase in the dies suddenly with no visible symptoms, and acute fatigue is when
amount of calcium carbonate deposited in the shells. They the hen experiences leg paralysis and can potentially recover with
found a positive effect of the organic acids on some eggshell qual- assistance (Bell and Siller, 1962). Young hens that are in peak
ity parameters in older hens, probably due to their beneficial production are most likely to develop osteoporosis.
effect on calcium absorption. Bell and Siller (1962) also concluded that some genetic lines of
It was also determined that lowering the pH of the diet can layers were more susceptible to osteoporosis than others.
benefit eggshell quality (Świątkiewicz et al., 2010). Butyric acid Medullary bone development and the end of structural bone
and its salts have shown different results for egg quality and egg remodeling occur simultaneously with the beginning of hen
production. This difference has been attributed to the source of sexual maturity. The medullary bone stores large amounts of
butyric acid, the inclusion rate, and the environmental conditions calcium, which is released later in the formation of the eggshell
and diet composition (Soltan, 2008; Sikandar et al., 2017). when calcium is absent or cannot be readily absorbed from the
Rahman et al. (2008) reported a significant increase in egg pro- digestive tract. Osteoporosis will occur if not enough calcium is
duction in 67–74 weeks old hens when fed on a diet supplemen- absorbed from the intestine to remodel the structural bone after
ted with various concentrations of organic acids, including it provides calcium to the medullary bone (Webster, 2004;
calcium butyrate, compared to the control diet. They illustrated Khan and Iqbal, 2016).
that the mixture of fumaric acid, salts of butyric, propionic, Studies done in ovariectomized rats suggest that organic acids
and lactic acids, did not affect egg weight and eggshell%. In con- can prevent osteoporosis by reducing the amount of bone turn-
trast, the egg size and albumen% were increased and yolk% was over due to lowering gut pH and improving calcium absorption,
decreased with dietary supplementation of organic acids. solubility, and utilization, and could further improve osteoporosis
Also, organic acids significantly increased the eggshell thick- and egg quality (Kamal and Ragaa, 2014). It has also been sug-
ness (Rahman et al., 2008; Sunkara et al., 2011). These findings gested that osteoporosis cannot be avoided in the caged modern
are in agreement with Soltan (2008) but contrary to the study per- hybrid laying hen due to confinement and its high egg production
formed by Yesilbag and Colpan (2006), using an organic acid (Webster, 2004). This situation necessitates the use of additives to
mixture that did not include butyric acid or its salt (Rahman mitigate adverse effects on birth, health, and production.

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 Animal Health Research Reviews 145

Conclusion Deepa K, Purushothaman MR, VasanthaKumar P and Sivakumar K (2018)

Butyric acid as an antibiotic substitute for broiler chicken–A review.
Butyric acid has enhanced nutrient/energy utilization, gut Advances in Animal and Veterinary Sciences 6, 63–69.
health, and production performance in poultry, by improving Dehghani-Tafti N and Jahanian R (2016) Effect of supplemental organic
mineral absorption, immunity, and reducing the populations acids on performance, carcass characteristics, and serum biochemical meta-
and products of pathogenic bacteria. Our findings suggest that bolites in broilers fed diets containing different crude protein levels. Animal
the high stability of tributyrin in the feed and stomach should Feed Science and Technology 211, 109–116.
increase the efficacy of butyric acid, thereby improving the effi- Dixon RC and Hamilton PB (1981) Effect of feed ingredients on the antifun-
ciency of gut health and absorption of nutrients, leading to gal activity of propionic acid. Poultry Science 60, 2407–2411.
Elnesr SS, Ropy A and Abdel-Razik AH (2019) Effect of dietary sodium
improved performance. However, further investigations are
butyrate supplementation on growth, blood biochemistry, haematology
required to explore the effect of butyric acid and its salts on and histomorphometry of intestine and immune organs of Japanese
poultry immunity. quail. Animal 13, 1234–1244.
Elnesr SS, Alagawany M, Elwan HA, Fathi MA and Farag MR (2020) Effect
Conflict of interest. None.
of sodium butyrate on intestinal health of poultry – a review. Annals of
Animal Science 20, 29–41.
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