Egypt. Poult. Sci. Vol.

(44) (I): (87-110) (2024) (2403-1280)

Egyptian Poultry Science Journal

http://www.epsj.journals.ekb.eg/

ISSN: 1110-5623 (Print) – 2090-0570 (Online)

GROWTH PERFORMANCE, NUTRIENT DIGESTIBILITY, AND
BLOOD PARAMETERS OF BROILER CHICKENS FED A DIET
SUPPLEMENTED WITH ORGANIC ACIDS
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
1
Dep. of Anim. and Poult. Prod,, Fac. of Agric., Damanhour Univ.
2
Dep. of Poult. Prod., Fac. of Agric., New Valley Univ.
* Corresponding author: M. I. El-Kelawy Email: [email protected]
Received: 03/03/2024 Accepted: 30 /03/2024
ABSTRACT:The study aimed to assess the impact of different levels of organic acids
(formic, acetic, and citric) on broiler chickens’ growth performance, nutrient
digestibility, carcass traits, blood parameters, bacterial count, antioxidant status,
immune response, and economic efficiency. Two hundred and ten unsexed (Cobb 500)
day-old chicks were randomly divided into seven groups, each with five replicates of six
birds. The first group was used as the control for comparison purposes. Birds in groups
2 and 3 were fed a diet containing formic acid (0.5% and 1.0%), while birds in groups 4
and 5 were fed a diet containing acetic acid (0.5% and 1.0%). Birds in groups 6 and 7
were fed a diet containing citric acid (2.0% and 3.0%). Weekly weighing, feed
consumption recording, and calculation of growth parameters were recorded.
Additionally, biochemical, hematological, and immune parameters were analyzed, along
with evaluating the microbial activity of the digestive system. Enhanced growth
parameters, including final weight and body weight gain, were noted with formic,
acetic, and citric acid supplementation, along with improved feed conversion ratios.
Dressing percentage was increased, while abdominal fat was decreased with all
supplementation groups. Hematological analysis revealed improved blood parameters,
albeit with reduced red blood cell count and hemoglobin levels, in chickens
supplemented with acetic and citric acid. Lipid and protein profiles were positively
influenced, with lowered serum lipids and increased protein levels. Additionally,
antioxidant and immunological status were enhanced, characterized by heightened
antioxidant enzyme activity and immune responses. Moreover, supplementation led to
favorable shifts in the gut microbiota, with increased Lactobacillus levels and decreased
bacterial counts, including Escherichia coli and Proteus. In conclusion, incorporating
organic acids as alternatives to antibiotics in broiler chicken diets significantly improves
production performance and enhances economic efficiency while maintaining optimal
health.

Keywords: Productive performance, broiler chickens, organic acids, growth promoters.

Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
INTRODUCTION positively influence the growth of both
The poultry industry is experiencing rapid animals and broiler chickens.
growth globally, with feed additives Specifically, organic acids such as butyric
being recognized as essential for acid, acetic acid, citric acid, formic acid,
optimizing performance and productivity fumaric acid, and propionic acid were
in modern poultry production (Shahid et found to have a beneficial impact on
al., 2015). Consequently, there is a growth in these species.
continuous search within the poultry Organic acids have been observed to
sector for new feed additives aimed at impact various aspects of animal growth
enhancing feed efficiency and the health and nutrition, including final weight gain,
of poultry birds. average daily weight gain, total feed
This quest intensified after the prohibition intake, feed-to-gain ratio, daily protein
of antibiotic growth promoters in the EU intake, protein efficiency ratio, total water
since 2006 due to concerns over emerging consumption, average daily water intake,
microbial resistance and residues in meat and water-to-feed ratio. Additionally,
and eggs (Leeson, 2007; Cakir et studies have shown that organic acids can
al., 2008; Dhama et al., 2015; Ullah et enhance nutrient utilization, promote
al., 2022). growth, and improve feed conversion
In response, researchers have sought efficiency (Denli et al., 2003).
alternatives to antibiotic growth Furthermore, organic acids have been
promoters to maintain growth and feed found to stimulate pancreatic juice
efficiency in farm animals (Attia et secretion and promote the growth of
al., 2012; Alzawqari et al., 2016; epithelial cells in the intestinal wall
Abudabos et al., 2018; Scicutella et (Langhout and Sus, 2005). Additionally,
al., 2021). Studies have suggested that they have been shown to modify gut
organic acids, bacteriophages, organic morphology by increasing villi height,
minerals, probiotics, prebiotics, and thereby enhancing the absorption area for
enzymes could serve as viable substitutes nutrients (Dibner and Buttin, 2002).
for antibiotic growth promoters. The Therefore, the aim of this study was to
consumption of these feeds has been assess the impact of varying levels of
suggested as a suitable dietary option for organic acids (citric, formic, and acetic)
offsetting the decline in performance on the growth performance, digestibility
effectiveness that occurs when antibiotic of nutrients, carcass characteristics,
growth promoters are removed from certain blood parameters, bacterial count,
animal diets (Jackson et al., 2004; Yan et antioxidant status, immune response, and
al., 2012). economic efficiency of broiler chickens.
One such alternative is the use of organic MATERIALS AND METHODS:
acids as feed additives in animal This study was carried out at the Poultry
production. Research has shown that Research Unit (El-Bostan Farm),
organic acid supplementation improves Department of Animal and Poultry
the performance of Japanese quails Production, Faculty of Agriculture,
(Fouladi et al., 2018) and broilers (Ishfaq Damanhour University, Damanhour,
et al., 2015; Emami et al., 2017; Tomar et Egypt during year 2023. The main
al., 2017). Furthermore, Onunkwo et al. objective was to evaluate different levels
(2021) discovered that organic acids of organic acids (OA) on growth
88
Productive performance, broiler chickens, organic acids, growth promoters.
performance, nutrient digestibility, days of age, and the BWG (g/chick) was
carcass traits, some blood parameters, calculated. Feed consumption was
bacterial count, antioxidant status, the recorded for each replicate (g/chick), and
immune response, and the economic thereby FCR (g feed/g gain) was
efficiency of broilers. Two hundred and calculated. The economic evaluation for
ten unsexed day-old chicks obtained from all experimental treatments was made
a commercial hatchery, were randomly (Zeweil, 1996) as below:
distributed into seven groups; each group
contained five replicates, six birds each.
Chickens were allocated to the following
dietary treatments: the first group was fed Where:
a basal diet without supplementation Total revenue = BW × Meat Price
(control), the 2nd and 3rd groups were fed Total cost = Feed cost + Addition cost +
basal diets supplemented with 0.5 and Other cost
th th
1.0% of formic acid (FA), the 4 and 5 The European production efficiency
groups were fed the same basal diets index (EPEI) was measured throughout
supplemented with 0.5 and 1.0% acetic the experimental period (7-35 days of
acid (AA), and the 6th and 7th groups were age), according to the Hubbard broiler
fed the same basal diets supplemented management guide (1999), as below.
with 2.0 and 3.0% citric acid (CA). The Where:
experimental diets were formulated
EPEI = European Production Efficiency
according to the NRC (1994). Ingredients
Index; BW = body weight (kg).
and chemical composition of the
SR = survival rate (100% - mortality); PP
experimental basal diets (% as fed basis)
= production period (days).
fed during the two phases (starter from
FCR = feed conversion ratio (kg feed/ kg
days 7 to 20 and grower from days 21 to
gain).
35) are shown in Table 1.
At 35 days of age, the apparent
Chicks were housed in wire cages (60 cm
digestibility of nutrients and ash retention
length × 50 cm depth × 40 cm height)
were measured using five birds per
provided with galvanized feeders and
treatment housed individually in
automatic nipple drinkers in a semi-
metabolic cages or treatments using the
opened room equipped with two exhaust
total collection method as cited by Abou-
fans to maintain normal ventilation.
Raya and Galal (1971). The DM, CP and
Chicks were fed the experimental diets ad
EE of feed and excrement were
libtium and given free access to water. A
determined according to (AOAC, 2004)
light schedule similar to commercial
th and expressed on dry matter basis.
conditions was applied until the 7 day,
At the end of experiment, five chicks
with 23 h of light followed by 20 h of
th were taken randomly from each group
light from the 8 day until 3 days before
and slaughtered after 8 hours of fasting,
the slaughter test (8-32 days of age). The
processed, and the weight of the carcass
brooding temperature (indoor) was 32,
and internal organs (dressing, total edible
30, 27, and 24-21 °C during 1-7, 8-14, 15-
parts, abdominal fat, spleen, bursa, and
20, and 21-35 days of age (declined
thymus) was taken and expressed as the
gradually). Chicks in each replicate were
percentage of live BW. Five blood
weighed (g) weekly between 7 and 35
samples (about 3 ml) from each treatment
89
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
were collected before slaughter from the (g/dl) (Henry et al., 1974), albumin (g/dl)
wing vein for hemato-biochemical (Doumas, 1971), globulin (g/dl) (Coles,
analysis. Heparin was utilized as an 1974), and different types of globulins (α-
anticoagulant; however, a portion of the globulin, β-globulin, and γ-globulin) were
samples was maintained without heparin determined according to Bossuyt et al.
to acquire serum. Non-coagulated blood (2003). Glucose concentration (mg/dl)
was used to test shortly after collection was measured according to Trinder
for estimating blood picture. Serum was (1969). Thyroid hormones: tri-
separated by centrifuging the blood at iodothyronine (T3) and thyroxin (T4)
3,000 rpm for 20 minutes and then stored were measured according to Sharp et al.
at −20°C until biochemical analysis. (1987). The activity of malondialdehyde
(MDA) in the blood was measured using
Red blood cells, White blood cells, and
the method of Placer et al. (1966). Total
different subclasses of WBC's
antioxidant capacity (TAC) was
(lymphocytes, heterocytes percentages)
determined according to Koracevic et al.
were counted according to Feldman et al.
(2001), superoxide dismutase activity
(2000). Packed cell volume (PCV) was
(SOD) (Misra and Fridovich, 1972),
measured by a microhaematocrit capillary
glutathione peroxidase activity (GSH-Px)
tube using a Hemocrit reader.
(Paglia and Valentine, 1967) and
The transaminase enzymes alanine
glutathione activity (GSH) (Ellman,
aminotransferase (ALT) and aspartate
1959).
aminotransferase (AST) were determined
Measurements were conducted according
according to the calorimetric method of
to the manufacturer’s instructions. The
Retiman and Frankel (1957). Alkaline
lymphocyte transformation test (LTT)
phosphatase (ALP) concentration was
was determined following the method
determined according to the colorimetric
described by Balhaa et al. (1985). Serum
method of Belfield and Goldberg (1971).
bactericidal activity (BA) of the
Kidney functional enzyme (creatinine)
Aeromonas hydrophila strain was
was determined according to Fabiny and
determined according to Rainger and
Ertingshausen, (1971), while uric acid
Rowley (1993). Serum lysozyme activity
was determined according to the method
(LA) was measured with the turbidimetric
of Patton and Crouch (1977). In addition,
method described by Engstad et al.
serum samples were assigned for the
(1992), and the results are expressed as
determination of creatinine and uric acid
one unit of lysozyme activity that is
(Bartles et al., 1972). Serum total lipids
defined as a reduction in absorbance at
and triglyceride concentrations were
0.001/min. Lysozyme activity = (A0 -
determined by means of a
A)/A.
spectrophotometer according to Chabrol
Phagocytic activity and index were
and Charonnat (1973) while total
determined according to Kawahara et al.
cholesterol was determined according to
(1991). Phagocytic activity (PA) =
the recommendation of Stein (1986).
percentage of phagocytic cells containing
High-density lipoprotein (HDL) was
yeast cells.
measured according to Lopez-Virella
Phagocytic index (PI)= number of yeast
(1977), and low-density lipoprotein
cells phagocytized/number of phagocytic
(LDL) was calculated by the formula of
cells. Also, immunoglobulins (IgA, IgG,
Friedwald et al. (1972). Total protein
90
Productive performance, broiler chickens, organic acids, growth promoters.
and IgM) were determined using 11.11% and 11.62%, 15.15% and 6.57%,
commercial ELISA according to Bianchi and 9.60% and 7.07%, respectively.
et al. (1995). Nevertheless, there were no notable
The effect of dietary treatments on the variations in feed consumption among
microbial activity of the digestive system the different levels of supplementation.
was evaluated by measuring the total Additionally, broiler chickens
bacterial count (TBC) and also counting supplemented with these additives in the
some pathogenic bacteria harboring the basal diet showed markedly improved
intestine, such as Salmonella, economic efficiency and production
Lactobacillus, E.coli, and Proteus spp., index compared to the control group.
according to methods described by Particularly noteworthy, broilers fed the
ICMSF (1980). basal diet with 2% CA exhibited the
Data obtained were analyzed using the highest economic efficiency and
GLM procedure of the Statistical Analysis production index among all experimental
System (SAS, 2002), using one-way ANOVA groups.
as in the following model: The apparent digestibility of the
Yik= µ + Ti + eik nutrients and ash retention
Where Y is the dependent variable; µ is The impact of varying concentrations of
the general mean; T is the effect of OA on the apparent digestibility of
experimental treatments; and e is the essential nutrients in broiler chickens is
experimental random error. Before outlined in Table 3. Incorporating
analysis, all percentages were subjected organic acid supplements into the diet
to a logarithmic transformation (log10x+1) resulted in notable increases in the
to normalize the data distribution. The digestibility of OM, DM, CP, and EE
differences among means were determined compared to the control group.
using Duncan’s new multiple range test Nevertheless, the analysis revealed no
(Duncan, 1955). significant influence of different
RESULTS supplement levels on the digestibility of
Growth Performance CF or apparent ash retention.
The influence of various concentrations Carcass characteristics and relative
of OA on the production performance of weight of immune organs
broiler chickens is summarized in Table The impact of different levels of OA on
2. In the overall phase of the study, the carcass characteristics of broiler
dietary supplementation with varying chickens is presented in Table 4.
concentrations of FA (0.5% and 1.0%), Incorporating organic acid supplements
AA (0.5% and 1.0%), and CA (2.0% and into the diet led to an enhanced dressing
3.0%) led to increases (p < 0.05) in final percentage, while concurrently reducing
weight by 13.51% and 9.73%, 12.43% the percentage of abdominal fat
and 2.70%, and 11.89% and 3.78%, compared to the control group. In
respectively. These supplements also contrast, it was observed that chickens
resulted in notable enhancements (P < receiving the basal diet supplemented
0.05) of BWG by 14.95% and 10.72%, with 1% AA or 3% CA exhibited
13.82% and 3.04%, and 13.04% and significantly lower dressing% compared
4.23%, respectively. Furthermore, FCR to other supplemented groups.
was significantly improved (P < 0.05) by Furthermore, no significant effects of
91
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
different supplement levels were levels (Table 7). Furthermore, diets
observed on the percentages of spleen, supplemented with OA led to increased
bursa, and thymus. levels of total protein, globulin, and γ-
Hematological traits and liver and globulin compared to the control group.
kidney functions Conversely, chickens fed a basal diet
The impact of different levels of OA on supplemented with 1% AA and 3% CA
the hematological traits of broiler displayed significantly lower levels of
chickens is summarized in Table 5. total protein, globulin, and γ-globulin
Incorporating different supplements into than other supplemented groups.
the diet led to increases in RBC, HB Nonetheless, no significant effects of
levels, WBC, and lymphocyte count different supplement levels were detected
while concurrently decreasing the on albumin, α-globulin, and β-globulin
heterophil to lymphocyte ratio compared levels (Table 8). Moreover,
to the control group. Furthermore, supplementation with OA resulted in
chickens receiving the basal diet elevated levels of glucose, T3, and T4
supplemented with 1% AA and 3% CA compared to the control group.
exhibited significantly lower RBC and Additionally, chickens fed a basal diet
HB levels than other supplemented supplemented with 1% AA and 3% CA
groups. However, no significant effects of exhibited significantly lower levels of T3
different supplement levels were and T4 than other supplemented groups
observed on PCV percentage and (Table 9).
heterophils percentage. Additionally, no Indicators of antioxidant status and
significant effects of varying supplement immunological status
levels were observed on liver and kidney The impact of different levels of OA on
function, as depicted in Table 6. indicators of antioxidative and
Blood biochemical analysis immunological status in broiler chickens
The impact of different levels of OA on is summarized in Tables 10 and 11.
the lipid and protein profiles, as well as Incorporating different supplements of
the blood glucose and thyroid hormones OA into the diet resulted in increased
of broiler chickens, is detailed in Tables levels of TAC, reduced GSH, GSH-Px,
7, 8, and 9. All feed supplements utilized and SOD, while concurrently decreasing
in this study resulted in decreased serum levels of MDA compared to the control
levels of total lipids, cholesterol, and group. Notably, chickens fed a basal diet
LDL, alongside increased serum supplemented with 1% AA and 3% CA
triglycerides compared to the control exhibited significantly lower levels of
group. Notably, chicks fed a basal diet TAC, GSH, and SOD than other
supplemented with 0.5% and 1.0% FA, supplemented groups (Table 10).
0.5% AA, and 2.0% CA exhibited Additionally, diets supplemented with
significantly lower (P ≤ 0.01) levels of OA led to increased levels of lysozyme
total lipids, cholesterol, and LDL, activity (LA), bactericidal activity (BA),
followed by those fed a basal diet lymphocyte transformation test (LTT),
supplemented with 0.5% FA and 3% CA, phagocytic activity, phagocytic index,
compared to the control group. However, and immunoglobulins (IgG, IgM, and
no significant effects of different IgA) compared to the control group.
supplement levels were observed on HDL Furthermore, chicks fed a basal diet
92
Productive performance, broiler chickens, organic acids, growth promoters.
supplemented with 0.5% and 1.0% FA, enhancements in BW and BWG among
0.5% AA, and 2.0% CA displayed broilers, thus underscoring the potential
significantly higher (P ≤ 0.01) levels of of formic acid in fostering growth and
BA, phagocytic activity, phagocytic feed efficiency. Correspondingly, Li et al.
index, and IgA, followed by those fed a (2018) found that broilers supplemented
basal diet supplemented with 0.5% FA with acetic acid exhibited significant
and 3% CA, compared to the control improvements in BW and BWG, coupled
group (Table 11). with an enhanced FCR, indicative of
Bacterial count more effective nutrient utilization.
The impact of different levels of OA on However, the literature presents varied
the bacterial count of broiler chickens outcomes regarding CA supplementation.
gut microbiota is detailed in Table 12. While Lee et al. (2017) observed an
Incorporating different organic acid increase in BW and BWG in broilers,
supplements into the diet resulted in other studies reported no significant
increased levels of Lactobacillus and effects. The study hypothesizes that the
decreased levels of total bacterial count, observed increase in BWG among
Escherichia coli (E. coli), and Proteus ducklings is attributable to the beneficial
compared to the control group. impact of OA on gut flora. These acids
DISCUSSION likely disrupt microbial cell membrane
The current study elucidates the integrity, interfere with nutrient transport,
significant efficacy of incorporating OA- and modulate energy metabolism, thereby
specifically formic, acetic, and citric exerting a bactericidal effect (Ricke,
acid—into broiler diets, substantially 2003). The acidity introduced into the
enhancing performance metrics. This gastrointestinal tract by these OA bolsters
enhancement is particularly evident in the stomach’s defensive barrier against
growth rates, FCR, economic efficiency, pathogens and enhances digestive enzyme
and production indices as compared to activity. These acidifiers stimulate gastric
control groups. These findings are in acid secretion, lower gastrointestinal tract
harmony with prior research conducted pH, and curtail pathogenic bacteria such
by Sheikh et al. (2011), Ghazalah et al. as Salmonella and E. coli (Hume et al.,
(2011), Hassan et al. (2016), and Hossain 1993).
and Nargis (2016), which collectively The antimicrobial and pH-altering
reinforce the premise that dietary capabilities of OA are instrumental in
inclusion of OA is beneficial in suppressing pathogenic intestinal
augmenting broiler performance. bacteria, thereby reducing their metabolic
Additionally, the research conducted by demands and increasing nutrient
ELnaggar and Abo EL-Maaty (2017) availability for the host. This decrease in
underscores that ducklings consuming a toxic bacterial metabolites, due to
basal diet supplemented with OA reduced bacterial fermentation, leads to
demonstrated a notable increase in BW, enhanced protein and energy digestibility,
BWG, economic efficiency, and culminating in improved weight gain and
improved feed conversion relative to the overall performance (Ghazalah et al.,
control cohort. Specifically focusing on 2011). Furthermore, OA alters the
FA, studies by Zhang et al. (2019) and intestinal microbial balance (Al-Kassie,
Liu et al. (2020) reported marked 2009), fostering the predominance of
93
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
beneficial microbes like Lactobacillus promotion of beneficial gut microbiota by
spp. and Bifidobacterium spp., which are OA, as reported by Jin et al. (2000). This
integral to gut health. Moreover, the selective enhancement of gut health is
microbial fermentation of OA yields believed to facilitate more efficient
short-chain fatty acids (SCFAs), such as nutrient absorption and metabolism,
butyrate, which possess antioxidant and leading to improved growth performance
anti-inflammatory properties, thereby metrics such as body weight gain.
safeguarding the intestinal mucosa Naghmeh and Jahanian (2012) have
(Abdelqader et al., 2013). The acid- supported this notion, suggesting that the
induced low pH environment augments enhancement in FCR is likely a result of
pancreatic enzyme secretion, including improved nutrient utilization efficiency.
amylase, lipase, and protease, thereby Additionally, the antibacterial properties
facilitating nutrient breakdown into of OA, particularly against pathogenic
absorbable forms. This acidic milieu also strains such as E. coli and Salmonella in
enhances serum calcium and phosphorus the gastrointestinal tract, further
levels (Dhawale, 2005), promoting the contribute to their beneficial effects on
absorption of essential minerals like Ca, animal health and nutrient utilization
P, Cu, and Zn. Additionally, the acidic (Dhawale, 2005). This body of evidence
environment in the intestines favors the collectively highlights the complex
absorption of vitamins A and D. OA also interplay between OA and animal
plays a pivotal role in improving villus nutrition, pointing to mechanisms that
architecture and functionality, mitigating extend well beyond pH modulation.
oxidative damage, and optimizing villus Through their capacity to chelate
height, surface area, and goblet cell minerals, selectively modulate gut
numbers, thereby augmenting nutrient microbiota, and exert antibacterial effects,
absorption (Abbas et al., 2012). OA emerge as valuable dietary
The influence of OA on animal nutrition supplements in poultry nutrition, offering
extends beyond mere pH reduction. a multifaceted approach to improving
Extensive research has elucidated the growth performance and feed efficiency.
multifaceted roles these compounds play Incorporating organic acid supplements
in enhancing nutrient uptake and overall into the diet has shown a significant
health. For instance, citric acid has been increase in OM, DM, CP, and EE levels
identified as a potent enhancer of compared to control groups. This
phosphorus bioavailability in poultry. enhancement aligns with the findings of
This is achieved through its ability to Nourmohammadi et al. (2012), who
chelate calcium ions, thereby mitigating observed that a 3% citric acid
the formation of insoluble calcium supplementation, in conjunction with
phytate complexes, a reaction detailed in microbial phytase, improved ileal nutrient
studies by Angel et al. (2001) and Snow digestibility (including CP, apparent
et al. (2004). Such a mechanism metabolizable energy (AME), calcium,
underscores the nuanced role of OA in and total phosphorus) and mineral
nutrition beyond simple acidification. retention in broiler chickens. Similarly,
Further, the observed improvements in Ghazalah et al. (2011) reported that the
feed conversion ratios (FCR) have been addition of fumaric, formic, acetic, and
partially attributed to the selective citric acids to broiler diets notably
94
Productive performance, broiler chickens, organic acids, growth promoters.
improved metabolizable energy and chymotrypsinogen, and trypsin (Adil et
nutrient digestibility metrics such as CP, al., 2010). The resultant slower digesta
EE, CF, and nitrogen-free extract (NFE). passage rates, in the presence of OA,
Van Der Sluis (2006) suggested that the enhance nutrient absorption efficiency
digestion-enhancing effects of OA are from the intestines (Abudabos et al.,
linked to a slowed feed passage through 2017). Additionally, the acidic
the digestive tract, facilitating improved environment reduces the production of
nutrient absorption and resulting in drier bacterial metabolites such as ammonia
droppings. This observation is supported and amines (Samanta et al., 2010), further
by a substantial body of literature, with improving digestibility. The efficacy of
numerous studies corroborating the OA in enhancing nutrient digestibility is
positive impact of organic acid also linked to its role in augmenting the
supplementation on nutrient digestibility release of digestive enzymes, activating
in broiler feed (Hernández et al., 2006; microbial phytase, and increasing
García et al., 2007; Rodjan et al., 2017; pancreatic activity within the gut
ELnaggar and Abo EL-Maaty, 2017; (Hernández et al., 2006). Collectively,
Sureshkumar et al., 2021). Organic acids these mechanisms underscore the
contribute to this improvement by multifaceted benefits of OA
lowering the digesta's pH and enhancing supplementation in poultry nutrition,
gastric proteolytic activity, as detailed by highlighting its capacity to improve
Khan et al. (2016). The specific pH growth performance through enhanced
modulation within different intestinal feed efficiency and nutrient utilization.
segments plays a crucial role in Dietary supplementation with various OA
promoting beneficial microbial has been observed to enhance dressing
populations, which are pivotal for percentages and total edible parts while
efficient digestion and nutrient concurrently reducing abdominal fat
absorption. This modulation is percentages in comparison to control
particularly relevant given that most groups. These findings are consistent with
pathogenic bacteria thrive at a pH close to the work of Talebi et al. (2010), who
neutral (7.0), whereas beneficial bacteria noted improvements in the relative
prefer slightly acidic conditions (pH 5.8– weights of carcass, giblets, and dressing
6.2). By reducing the intestinal pH, OA in birds fed diets supplemented with citric
creates an environment conducive to acid over those in the control group.
beneficial bacterial growth while Similarly, Ghazalah et al. (2011)
suppressing pathogenic microbes (Haque demonstrated that dietary inclusion of OA
et al., 2009), thereby optimizing nutrient enhanced the relative weights of carcass,
digestion and absorption. Furthermore, giblets, and dressing in birds
OA is thought to stimulate pepsin supplemented with citric acid at a dosage
activity, facilitating protein proteolysis of 2 g/kg relative to control birds. Further
into simpler peptides. This process supporting these observations, ELnaggar
triggers the release of digestive hormones and Abo EL-Maaty (2017) reported
such as gastrin and cholecystokinin, and significant increases in the percentages of
promotes the secretion of pancreatic juice dressing and total edible parts, alongside
enriched with digestive enzymes like a reduction in abdominal fat, with
procarboxypeptidases, supplementation of either formic or citric
95
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
acids at tested levels compared to findings of Kamal and Ragaa (2014) and
controls. In addition to physical ELnaggar and Abo EL-Maaty (2017),
characteristics, dietary supplementation who reported significant reductions in
with OA has been linked to blood total lipids, triglycerides, and
improvements in various blood cholesterol following dietary
parameters, including increases in acidification. The beneficial impact of
glucose, thyroid hormones (T3 and T4), OA on blood lipid profiles may be
total protein, globulin fractions (α- elucidated through their role in
globulin, γ-globulin), immunoglobulins diminishing microbial intracellular pH, as
(IgA, IgM, and IgG), lysozyme activity suggested by Abdel-Fattah et al. (2008).
(LA), bactericidal activity (BA), The dietary inclusion of OA also led to an
lymphocyte transformation test (LTT), increase in Lactobacillus counts while
phagocytic activity, phagocytic index, decreasing the total bacterial count of E.
RBCs, HB, WBCs, and triglycerides. coli and Proteus spp. in comparison to
Conversely, a decrease in serum total control groups. These results are in line
lipids, cholesterol, and low-density with those reported by ELnaggar and Abo
lipoprotein (LDL) levels was observed EL-Maaty (2017), who noted a reduction
when compared to the control group. in total bacterial count, Salmonella, E.
These results align with findings from coli, and Proteus spp., with all dietary
studies on broiler chicks and ducks by supplements compared to control groups.
Ghazalah et al. (2011) & ELnaggar and Such findings highlight the significant
Abo EL-Maaty (2017), respectively, role of OA in reducing both total bacterial
which highlighted that dietary OA led to and gram-negative bacterial counts in
an increased concentration of total protein broiler chickens, as demonstrated by
and globulin, indicative of an enhanced Gunal et al. (2006). Abdel-Fattah et al.
immune response and disease resistance. (2008) further elucidated that the lowered
The observed increase in globulin levels, pH fosters the proliferation of beneficial
a key indicator of immune responses and bacteria while inhibiting the growth of
a source of antibodies, suggests that pathogenic bacteria, which thrive at
supplemental OA may bolster immune relatively higher pH levels.
function. This proposition is supported by In conclusion, incorporating organic acids
Rahmani and Speer (2005), who found an as alternatives to antibiotics in broiler
elevated percentage of gamma globulin in chicken diets significantly improves
broilers receiving OA compared to those production performance, enhances
in the control group. The improvement in digestibility, reduces abdominal fat, and
immune response attributed to dietary enhances immune response. The study
acidification may stem from the recommends the use of organic acid
inhibitory effects of these compounds supplements to promote economic
against pathogenic microorganisms efficiency and production indices in
throughout the gastrointestinal tract. poultry farming while maintaining
Furthermore, the adjustments in serum optimal health.
lipid profiles and indicators of
antioxidative status corroborate the

96
Productive performance, broiler chickens, organic acids, growth promoters.
Table (1): Ingredients and chemical composition of the experimental basal diets.
Ingredients (%) Starter Grower
Yellow corn 53.85 61.63
Soybean meal (44% CP) 34.28 27.50
Vegetable oil 3.00 3.00
Gluten meal 5.00 4.00
Dicalcium phosphate 1.69 1.69
Limestone 1.45 1.45
L-Lysine 0.03 0.03
DL-Methionine 0.10 0.10
Vit+min premix1 0.30 0.30
NaCl 0.30 0.30
Total 100 100
Calculated and determined composition,
DM,%2 86.16 86.26
3
DM,% 86.34 86.33
ME (Cal/kg) 3 3016 3116
2
CP,% 22.89 19.96
CP,% 3 23.01 20.09
Crude Fat, %2 5.32 5.53
Crude Fat, %3 5.45 5.66
Crude fiber, %2 3.83 3.42
3
Crude fiber, % 3.72 3.39
Lysine, %3 1.13 0.96
3
Methionine, % 0.50 0.46
Calcium, %3 1.06 1.04
3
Av. Phosphorus, % 0.46 0.45
Ash, %2 5.10 5.34
1
Vit+Min mix. provides per kilogram of the diet: Vit. A, 12000 IU, vit. E (dl--
tocopherol acetate) 20 mg, menadione 2.3 mg, Vit. D3, 2200 ICU, riboflavin 5.5 mg,
calcium pantothenate 12 mg, nicotinic acid 50 mg, Choline 250 mg, vit. B12 10 g, vit.
B6 3 mg, thiamine 3 mg, folic acid 1 mg, d-biotin 0.05 mg. Trace mineral (mg/ kg of
diet): Mn 80 Zn 60, Fe 35, Cu 8, and Selenium 0.1 mg. 2Analyzed values. 3Calculated
values.

97
 Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
Table (2): Effect of dietary inclusion with different levels of organic acid (citric, formic, and
acetic) on productive performance, economic efficiency and production index of Cobb 500
broiler chicks
BWG FC FCR
BW 7 BW REE EPEI
Traits (7-35 (7- (7-35d) EEF*
d 35d (%) ** ***
d) 35d)
Control 0 171 1850c 1679c 3320 1.98a 0.359c 100 267d
0.5 % 170 2100a 1930a 3400 1.76c 0.457b 127 341b
Formic
1.0 % 171 2030a 1859a 3260 1.75c 0.448b 125 331b
0.5% 169 2080a 1911a 3210 1.68c 0.539b 150 354b
Acetic
1% 170 1900b 1730b 3200 1.85b 0.417b 116 293c
2.0 % 172 2070a 1898a 3390 1.79c 0.745a 207 401a
Citric
3.0 % 170 1920b 1750b 3220 1.84b 0.415b 115 298c
SEM 2.09 18.98 12.98 16.90 0.087 0.070 -- 4.01
P value 0.087 0.001 0.002 0.072 0.001 0.001 -- 0.001
a,b
Means in the same column followed by different letters are significantly different at
P ≤ 0.05. SEM; Standard error of mean. BW: Body weight, BWG: Body weight gain,
FC: Feed consumption, FCR: Feed conversion ratio, * EEF: Economic efficiency= Net
Revenue/ Total cost, ** REE: Relative economic efficiency; Assuming the REE of the
control= 100, *** EPEI = European Production Efficiency Index

Table (3): Effect of dietary inclusion with different levels of organic acid (citric, formic, and
acetic) on the apparent digestibility of the nutrients and ash retention of broiler chicks.

Dietary Apparent Ash

OM DM CP EE CF
supplementations retention
Control 0 59.5c 63.90b 72.87c 68.13c 18.00 34.00
0.5 % 66.4b 68.30a 83.00a 88.70a 16.20 33.90
Formic
1.0 % 68.6b 69.11a 87.12a 89.71a 17.88 32.48
0.5% 67.9b 69.90a 89.90a 86.61a 18.89 34.93
Acetic
1% 66.9b 64.76ab 79.30b 78.89b 18.01 30.02
2.0 % 71.7a 70.76a 87.98a 86.67a 16.89 32.09
Citric
3.0 % 65.3b 65.9ab 89.4a 77.18b 17.09 33.00
SEM 2.09 1.98 2.77 2.66 1.89 5.09
P value 0.002 0.003 0.001 0.002 0.072 0.087
a, b
Means in the same column followed by different letters are significantly different at P ≤
0.05; SEM, Standard error of means. OM: Organic matter, DM: Dry matter, CF= Crude
fiber, EE= Ether extract, CP= Crude protein,

98
 Productive performance, broiler chickens, organic acids, growth promoters.

Table (4): Effect of dietary inclusion with different levels of organic acid (citric- formic-
acetic) on carcass characteristics and relative weight of immune organs to live body weight
of broiler chickens

Traits Dressing, Abdominal Bursa, Thymus,

Spleen, %
% fat, % % %
Control 0 63.71c 0.157a 0.188 0.617 0.617
0.5 % 71.00a 0.139b 0.143 0.569 0.569
Formic
1.0 % 73.20a 0.127b 0.184 0.675 0.575
0.5% 69.00a 0.119b 0.162 0.644 0.600
Acetic
1% 65.12b 0.120b 0.177 0.555 0.605
2.0 % 72.70a 0.111b 0.167 0.601 0.608
Citric
3.0 % 67.00ab 0.112b 0.198 0.611 0.589
SEM 0.602 0.087 0.087 0.087 0.098
P value 0.001 0.001 0.065 0.076 0.088

Means in the same column followed by different letters are significantly different at P ≤ 0.05;
a, b

SEM, Standard error of means.

Table (5): Effect of dietary inclusion with different levels of organic acid (citric- formic- acetic) on
hematological traits of broiler chicks.

Dietary Hematological White blood cells and differential

supplementations parameters leukocytes counts
RBCs Hb PCV WBCs Hetero. Lympho. H/L
6 3 3 3
(10 /mm ) (g/dl) % (10 /mm ) (%) (%) ratio
Control 0.00 3.25c 9.89c 23.89 21.88 b
13.88 41.90 b
0.331a
0.5 % 4.14a 12.56a 25.98 24.89a 12.98 44.98a 0.289b
Formic a
1.0 % 4.26 13.01a 27.98 27.87 a
11.99 43.89 a
0.273b
0.5 % 3.99a 12.97a 28.88 26.89a 12.09 44.98a 0.269b
Acetic
1.0 % 3.54b 11.76b 24.89 25.89a 12.12 43.09a 0.281b
2.0 % 4.01a 12.34a 26.89 27.76a 12.34 46.00a 0.268b
Citric
3.0 % 3.76b 11.56b 24.09 26.93a 12.78 45.67a 0.280b
SEM 0.987 4.90 6.99 8.65 1.23 4.99 0.087
P value 0.001 0.002 0.087 0.003 0.087 0.002 0.003
a, b
Means in the same column followed by different letters are significantly different at P ≤ 0.05; SEM, Standard
error of means. HB: Hemoglobin; RBCs: red blood cell; PCV: packed cell volume; WBCs: white blood cells

99
 Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
Table (6): Effect of dietary inclusion with different levels of organic acid (citric- formic- acetic) on
liver and kidney function of broiler chicken.

Dietary Liver function Kidney function

supplementations AST ALT ALK Creatinine Uric acid
(U/L) (U/L) (U/L) (mg/dl) (mg/dl)
Control 0 60.98 40.09 12.09 0.780 2.44
0.5 % 61.11 38.90 11.89 0.809 2.30
Formic
1.0 % 59.89 36.49 12.34 0.766 1.99
0.5% 62.89 35.55 12.15 0.801 2.09
Acetic
1% 60.43 36.91 11.98 0.776 2.17
2.0 % 61.00 37.87 12.04 0.811 2.10
Citric
3.0 % 58.79 39.00 12.25 0.821 2.21
SEM 4.89 2.67 4.98 0.017 0. 981
P value 0.098 0.076 0.098 0.076 0.076

Means in the same row followed by different letters are significantly different at P ≤ 0.05;.
a,b,c

SEM= Standard error of means. AST=aspartate amino transferase; ALT=alanine amino transferase;
Alk =Alkaline phosphatase;

Table (7): Effect of dietary inclusion with different levels of organic acid (citric- formic- acetic) on
lipid profile of broiler chickens
Dietary Total lipids Cholesterol Triglycerides HDL LDL
supplementations (mg/ dl) (mg/ dl) (mg/ dl) (mg/ dl) (mg/ dl)
Control 0.0% 411a 199a 86.98b 45.90 131.70a
0.5 % 356c 123c 99.98a 60.99 42.01c
Formic
1.0 % 362c 120c 109.9a 61.56 36.46c
0.5% 350c 119c 104.98a 59.99 38.01c
Acetic
1.0 % 397b 160b 94.67a 50.98 90.08b
2.0 % 344c 132c 100.98a 59.44 52.36c
Citric
3.0 % 398b 189b 95.99a 52.34 117.46b
SEM 12.89 13.90 21.09 9.98 29.89
P value 0.001 0.002 0.001 0.081 0.001

Means in the same row followed by different superscripts are significantly different at P ≤ 0.05; SEM=
a,b,c

Standard error of means, Chol.= total cholesterol; TG= triglycerides; HDL=high-density lipoprotein;
LDL=low-density lipoprotein,

100
 Productive performance, broiler chickens, organic acids, growth promoters.

Table (8): Effect of dietary inclusion with different levels of organic acid (citric- formic- acetic) on
Protein profile (g/dl) of broiler chickens.

Dietary α–globulin β– γ-
Total
supplementations Albumin Globulin (µg/dl) globulin globulin
protein
(µg/dl) (µg/dl)
Control 0.0% 3.59c 1.11 2.48c 0.970 0.956 0.954c
0.5 % 4.44a 1.09 3.35a 0.840 0.644 1.86ab
Formic
1.0 % 4.98a 1.04 3.94a 0.899 0.899 2.14a
0.5% 4.97a 1.02 3.95a 0.766 0.820 2.36a
Acetic 4.21b
1% 1.01 3.20ab 0.780 0.799 1.62b
2.0 % 4.89a 1.12 3.77a 0.690 0.760 2.32a
Citric
3.0 % 4.09b 1.14 2.95b 0.654 0.822 1.47b
SEM 1.11 0.987 0.987 0.092 0.022 0.920
P value 0.001 0.087 0.002 0.0871 0.0917 0.001

Means in the same row followed by different letters are significantly different at P ≤ 0.05;
a,b,

SEM, Standard error of mean.

Table (9): Effect of dietary inclusion with different levels of organic acid (citric-
formic- acetic) on blood glucose and thyroid hormones of broiler chicks.

Dietary
Glucose (mg/dl) T3 (ng/dl) T4 (ng/dl)
supplementations
Control 0.0 176b 2.59c 9.91c
0.5 % 199a 3.99a 12.01a
Formic
1.0 % 201a 3.87a 11.90a
0.5% 189a 3.90a 12.03a
Acetic
1% 186a 3.00b 10.9b
2.0 % 192a 3.82a 12.34a
Citric
3.0 % 189a 3.01b 11.01b
SEM 11.90 0.980 2.98
P value 0.001 0.001 0.002

Means in the same column followed by different letters are significantly different at P ≤ 0.05;
a, b

SEM, Standard error of means. T3= triiodothyronine; T4=thyroxine.

101
 Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
Table (10): Effect of dietary inclusion with different levels of organic acid (citric-
formic- acetic) on indicators of antioxidative status of broiler chicks.

Dietary Indicators of antioxidative status in blood (mg/dl)

supplementations MDA TAC GSH GSH-Px SOD
(mol/L) (nmol/L) (mmol/L) (mmol/L) (U/ml)
a
Control 0 35.90 2.09c 6.43c 2.98b 1.09c
0.5 % 32.11b 3.02a 9.11a 3.66a 1.98a
Formic
1.0 % 31.76b 2.99a 9.98a 3.76a 1.89a
0.5% 30.09b 3.04a 10.02a 3.80a 1.95a
Acetic
1% 29.99b 2.39b 8.90b 3.66a 1.56b
b a a
2.0 % 32.81 2.98 9.87 3.23a 1.97a
Citric
3.0 % 33.04b 2.50b 8.67b 3.55a 1.70b
SEM 5.90 0.987 1.98 0.981 0.087
P value 0.001 0.002 0.001 0.002 0.002

a, b Means in the same column followed by different letters are significantly different at P ≤ 0.05;
SEM, Standard error of means. TAC=total antioxidant capacity; ; GSH-Px =glutathione peroxidase;
SOD=superoxide dismutase, MDA= malondialdehyde

Table (11): Effect of dietary inclusion with different levels of organic acid (citric- formic-
acetic) on immunological status of broiler chicks

Immunological status Immunoglobulines (mg/dl)

Dietary LA BA LTT PA PI IgG IgM IgA
supplementations
Control 0 0.680b 31.11c 19.99b 17.09c 1.56c 801.93c 211.23b 62.98c
0.5 % 0.820a 37.87a 22.01a 25.09a 1.76a 884.01a 229.0a 90.91a
Formic
1.0 % 0.823a 38.9a 23.42a 26.91a 1.79a 896.26a 228.0a 89.76a
0.5% 0.798a 39.00a 24.09a 24.22a 1.81a 876.40b 249.5a 87.76a
Acetic
1% 0.790a 33.09b 24.00a 20.19b 1.68b 881.80a 236.9a 76.5b
2.0 % 0.811a 37.61a 23.98a 25.76a 1.80a 842.56b 245.8a 86.5a
Citric
3.0 % 0.802a 34.01b 25.02a 21.99b 1.69b 890.90a 240.9a 70.98b
SEM 0.065 3.90 4.09 3.98 0.098 5.78 3.92 4.01
P value 0.001 0.001 0.001 0.002 0.002 0.001 0.002 0.001

Means in the same column followed by different letters are significantly different at P ≤ 0.05;
a, b

SEM, Standard error of means. IgG= Immunoglobulin G; IgA= Immunoglobulin A IgM=

Immunoglobulin M . LA= Lysosome activity; BA= Bactriocide activity ; LTT= Lymphocyte
transformation test; PA= Phagocyte activity; PI = Phagocytic index.

102
 Productive performance, broiler chickens, organic acids, growth promoters.

Table (12): Effect of dietary inclusion with different levels of organic acid (citric- formic-
acetic) on bacterial count of broiler chicks.
Dietary E.Coli Proteus.
TBC Lactobacillus
supplementations (cfu x 103) (cfu x 103)
(cfu x 106) (cfu x 103)
Control 0.0 4.23a 1.66c 1.70a 0.99a
0.5 % 3.59b 2.13a 0.94b 0.76b
Formic
1.0 % 3.51b 2.39a 0.92b 0.66b
0.5% 3.37b 2.60a 0.68c 0.31c
Acetic
1% 3.43b 2.16a 0.97b 0.68b
2.0 % 3.20c 2.11b 0.68c 0..45c
Citric
3.0 % 3.19c 2.03b 0.98b 0.65b
SEM 0.156 0.087 0.078 0.064
P value 0.001 0.002 0.002 0.002

a, b Means in the same column followed by different letters are significantly different at P ≤ 0.05;
SEM, Standard error of means. TBC = Total Bacterial Count

REFERENCES humoral immune response of broilers.

A.O.A.C.2004. Official Methods of Asian J. Poult. Sci. 7: 102-113.
Analysis. 15th Association of Official Abou-Raya, A. K. and Galal, A. G. H.
Analytical Chemists Washington, D.C. 1971. Evaluation of poultry feeds in
digestion trials with reference to some
Abbas, R. Z.; Munir, M; Anjum, M. S.;
factors involved. ARE Journal of
Gazar, M. A.; Sohail, M. S.; Animal Production, 11: 207-221.
Rehman, A. U. and Mahmood, S. Abudabos, A.M.; Alyemni, A.H.;
2012. Effect of formic acid on Dafalla, Y.M. and Khan, R.U. 2017.
enhancing the gut health and Effect of organic acid blend and
performance of broiler chickens. Bacillus subtilis alone or in
combination on growth traits, blood
Pakistan Vet. J. 32: 398-402.
biochemical and antioxidant status in
Abdel Fattah, S. A.; El-Sanhoury, M. broilers exposed to Salmonella
H.; El-Mednay, N. M.; and Abdel typhimurium challenge during the
Azeem, F. 2008. Thyroid activity, starter phase. Journal of Applied
some blood constituents, organs Animal Research, 45:538–542.
morphology and performance of https://doi.org/
broiler chicks fed supplemental 10.1080/09712119.2016.1219665.
organic acids. International Journal of
Abudabos, A.M.; Alyemni, A.H.;
Poultry Science, 7: 215–222.
Abdelqader, A.; Al-Fataftah, T.O. and Dafalla, Y.M. and Khan, R.U. 2018.
Dieckhaus, A. A. 2013. Effect of The effect of phytogenics on growth
dietary organic acid blend on traits, blood biochemical and intestinal
performance, intestinal microbiota and histology in broiler chickens exposed
103
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
to Clostridium perfringens challenge. J and turkey flocks. Tiera Rztlicheum
Appl Anim Res 46:691–695 Schau, 43: 507-508.
Adil, S.; Banday, M.T.; Bhat, G.A.; Bartles, H.; Bohmer, M. and Heierli, C.
Mir, M.S. and Rehman, M. 2010. 1972. Serum creatinine determination
Efect of dietary supplementation of without protein precipitation. Clin.
organic acids on performance, Chim. Acta 37: 193-197.
intestinal, histomorphology, and Belfield, A. and Goldberg D. 1971.
serum biochemistry of broiler
Colorimetric determination of alkaline
chicken. Veterianry Medicine
International 1–7. https://doi.org/ phosphatase activity. Enzyme,
10.4061/2010/479485. 12:561–566.
Al-Kassie, G. A. 2009. Influence of two Bianchi, A. T. J.; Moonen-Leusen, H.
plant extracts derived from thyme and W. M.; van der Heijden, P. J. and
cinnamon on broiler performance. Pak. Bokhout, B. A. 1995. The use of a
Vet. J. 29: 169-173. double antibody sandwich ELISA and
Alzawqari, M.H.; Al-Baddany, A.A.;
monoclonal antibodies for the
Al-Baadani, H.H.; Alhidary, I.A.;
Khan, R.U.; Aqil, G.M. and assessment of porcine IgM, IgG, and
Abdurab, A. 2016. Effect of feeding IgA concentrations.Vet. Immunol.
dried sweet orange (Citrus sinensis) Immunopathol., 44:309–317.
peel and lemon grass (Cymbopogon Bossuyt, X.; Lissoir, B.; Mariën, G.;
citratus) leaves on growth Maisin, D.; Vunckx, J.; Blanckaert,
performance, carcass traits, serum N. and Wallemacq, P. 2003.
metabolites and antioxidant status in
Automated Serum Protein
broiler during the finisher phase.
Environ Sci Pollut Res Int 23:17077– Electrophoresis by Capillarys. Clin.
17082. https://doi.org/10.1007/s11356- Chem. Lab. Med. ; 41(5):704–710.
016-6879-7 Cakir, S.; Midilli, M.; Erol, H.; Simsek,
Angel, R.; Dhandu, A.S.; Applegate, N.; Cinar, M.; Altintas, A.; Alp, H.;
T.J. and Chrisman, M., Altintas, L.; Cengiz, Ö. and
2001..Phosphorus sparing effect of Antalyali, A. 2008. Use of combined
phytase, 25-hydroxycholecalciferol, probiotic-prebiotic, organic acid and
and citric acid when fed to broiler avilamycin in diets of Japanese quails.
chicks. Poult. Sci. Abst., 80:133-134. Revue Méd. Vét., 11:565–569.
Attia, Y.A.; Ellakany, H.F.; Abd El- Chabrol, E. and Charonnat, R. 1973.
Hamid, A.E.; Bovera, F. and Determination of plasma total lipids.
Ghazaly, S.A. 2012. Growing and Press Medical, 45: 17131720.
laying performance of Japanese quail Coles, E. H. 1974. Veterinary Clinical
fed diet supplemented with different Pathology. IST ED. 211-213 W.B.
concentrations of acetic acid. Ital. J saunder, company, Philadelphia,
Anim. Sci. 12:e37.
London, Toronto.
Balhaa, R. L.; Hinz, H. H.; Luders, H.
and Siegmann, O. 1985.Clinical Denli, M.; Okan, F. and Celik, K. 2003.
experiences with the drugs for Effect of dietary probiotic, organic
lymphocyte transformation in chickens acid and antibiotic supplementation to
104
Productive performance, broiler chickens, organic acids, growth promoters.
diets on broiler performance and Engstad, R. E.; Robertsen, B. and
carcass yield. Pakistan Journal of Frivold, E. 1992. Yeast glucan
Nutrition. 2:89-91. induces increase in lysozyme and
Dhama, K.; Latheef, Shyma, K.; complement-mediated haemolytic
Mani, S.; Abdul Samad, H. ;
Karthik, K.; Tiwari, R.; Khan, R.U.; activity in Atlantic salmon blood. Fish
Alagawany, M.; Farag, M. R.; and Shellfish Immun. 2: 287 - 297.
Alam, G. M.; Laudadio, V. and Fabiny, D.L. and Ertingshausen, G.
Tufarelli, V. 2015. Multiple beneficial 1971. Automated reaction-rate method
applications and modes of action of of serum creatinine with the
herbs in poultry health and production- centrifichem. Clinical Chemistry,
a review. Intern J Pharmacol 11:152–
17(8):696–700
176.
Dhawale, A. 2005. “Better eggshell Feldman, B. F.; Zinkl, J. G. and Jain,
quality with a gut acidifier,‖ Poultry N. C. 2000. Schalm’s Veterinary
International, 44, 18–21. Hematology. Lippincott Williams and
Dibner, J. and Buttin, P. 2002. Use of Wilkins, Philadelphia, USA.
organic acids as a model to study the Fouladi, P.; Ebrahimnezhad, Y.;
impact of gut microflora on nutrition Aghdam Shahryar, H.; Maheri, N.
and metabolism. Journal of Applied and Ahmadzadeh, A. 2018. Effects of
Poultry Research, 11(4): 453-463. Organic Acids Supplement on
Doumas, B. 1971. Colorimetric Performance, Egg Traits, Blood Serum
determination of serum albumin. Clin. Biochemical Parameters and Gut
Chim. Acta, 31: 400-403. Microflora in Female Japanese Quail
Duncan, D.B., 1955. Multiple Range and (Coturnix coturnix japonica). Brazilian
Multiple F- test. Biometrics, 11:1- 42. Journal of Poultry Science, 20 (1):133-
Ellman, G. L. 1959. Tissue sulfhydryl 144.
groups. Arch. Biochem Biophys., 82: Friedewald, W. T.; Levy, R. T. and
70-77. Frederickson, D. S.1 1972.
ELnaggar, Asmaa, Sh. and Abo EL- Estimation of the concentration of
Maaty, Hayam, M. A.2017. Impact low-density lipoprotein cholesterol in
of using organic acids on growth plasma without use of the preparative
performance, blood biochemical and ultracentrifuge. Clinical Chemistry,
hematological traits and immune 18: 499-502.
response of ducks (Cairina García, V.; Catalá-Gregori, P.;
Moschata). Egypt. Poult. Sci. Vol Hernández, F.; Megías, M.D. and
(37), (907-925). Madrid, J. 2007. Efect of formic acid
Emami, N.K.; Daneshmand, A.; Zafari, and plant extracts on growth, nutrient
N.S.; Graystone, E.N. and Broom, digestibility, intestine mucosa
L.J. 2017. Effects of commercial morphology, and meat yield of
organic acid blends on male broilers broilers. Journal of Applied Poultry
challenged with E. coli K88: Research, 16:555–562.
Performance, microbiology, intestinal https://doi.org/10.3382/ japr.2006-
morphology and immune response. 00116.
Poultry Science, 1-10.
105
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
Ghazalah, A. A.; Atta, A.M.; Elkloub, meat yield, dressing parameters and
K.; Moustafa, M. EL. and Riry, bone development of broilers. Bang.
F.H. Shata 2011. Effect of dietary J. Anim. Sci., 45: 7-18.
supplementation of organic acids on Hume, M. E.; Kubena, L. F.;
performance, nutrients digestibility Edrington, T. S.; Donskey, C. J.;
and health of broiler chicks. Int. J. Moore, R. W.; Ricke, S. C. and
Poult. Sci., 10: 176-184. Nisbet. D. J. 1993. Poultry digestive
Gunal, M.; Yayli, G.; Kaya, O.; microflora biodiversity as indicated by
Karahan, N.; and Sulak, O. 2006. denaturing gradient gel
The effects of antibiotic growth electrophoresis. Poult. Sci. 72: 1137-
1145.
promoter, probiotic or organic acid
Ishfaq, A.; Rather, S.A.; Mir, A.H. and
supplementation on performance, Gupta, M. 2015. Effect of Acipure
intestinal microflora and tissue of (feed acidifier) on the growth
broilers. International Journal of performance, mortality and gut pH of
Poultry Science, 5: 149–155. broiler chickens. IJLR. 5(10):40-46.
Haque, M.N.; Chowdhury, R.; Islam, Jackson, M.; Geronian, K.; Knox, A.;
K. M. S. and Akbar, M.A. 2009. McNab, J and McCartney, E. 2004.
Propionic acid is an alternative to A doseresponse study with the feed
antibiotics in poultry diet. Bangladesh enzyme beta-mannanase in broilers
Journal of Anim. Sci. 38: 115-122. provided with corn-soybean meal
Hassan, Rasha, M. I.; Mosaad, G. M. based diets in the absence of antibiotic
M.; and Abd-Ellah, A. M. 2016. growth promoters. Poultry Science,
Effect of feeding citric acid on 83(12): 19921996.
performance of broiler ducks fed Jin, L. Z.; HO, Y. W.; Abdullah, N.;
different protein levels. J.adv. vet. Jalaludin, S. 2000. Digestive and
Res., 6:18-26. bacterial enzyme activities in broilers
Henry, R.; Cannon, D. and fed diets supplemented with
Winkelman, J. 1974. Clinical Lactobacillus cultures. Poult. Sci., 79:
886-891.
Chemistry, Principles And
Kamal, Azza M.; and Ragaa, Naela
Techniques. 2nd edition, Harper and M., 2014. Effect of dietary
Row, New York , USA supplementation of organic acids on
Hernández, F.; García, V. Madrid, J.; performance and serum biochemistry
Orengo, J.; Catalá, P. Megías, M.D. of broiler chicken. Nature and
2006. Efect of formic acid on Science, 12 (2): 38-45.
performance, digestibility, intestinal Khan, R.U.; Naz, S.; Dhama, K.;
histomorphology and plasma Kathrik, K.; Tiwari, R.;
metabolite levels of broiler chickens. Abdelrahman, M.M.; Alhidary,
Br Poult Sci 47:50–56. I.A. and Zahoor, A. 2016. Direct-fed
https://doi.org/10. microbial: beneficial applications,
1080/00071660500475574. modes of action and prospects as a
Hossain, M.E. and Nargis, F. 2016. safe tool for enhancing ruminant
Supplementation of organic acid production and safeguarding health.
blends in water improves growth,
106
Productive performance, broiler chickens, organic acids, growth promoters.
International Journal of Naghmeh, D. and Jahanian, R. 2012.
Pharmacology, 12:220–231. Effects of dietary organic acid
Koracevic, D.; Koracevic, G.; supplementation on immune
Djordjevic, V.; Andrejevic, S. and responses and some blood parameters
Cosic, V. 2001. Method for the of broilers fed diets with different
protein levels. World s Poultry
measurement of antioxidant activity in
Science Journal, Supplement1,
human fluids. J. Clin. Pathol., 54: 356- Expanded Abstract - Poster
361. Presentation.
Langhout, P. and Sus, T. 2005. Volatile Nourmohammadi, R. Hosseini, S.M.;
fatty acids improve performance and Farhangfar, H. and Bashtan, M.
quality. International Poultry 2012. Efect of citric acid and
Production. 13(3):17. microbial phytase enzyme on ileal
Lee, K. W., et al. 2017. Effects of dietary digestibility of some nutrients in
citric acid on growth performance, broiler chicks fed corn-soybean meal
meat quality, and intestinal microbiota diets. Ital J Anim Sci 11:36–40.
of broilers. Poultry Science, 96(11), Nourmohammadi, R.; Seyed H. M.;
3902-3909. Farhangfar, H. and Bashtani,
Leeson, S. 2007. Balancing science M.2012. ―Effect of citric acid and
versus societal issues in poultry microbial phytase enzyme on ileal
nutrition. CAB Reviews: Perspectives digestibility of some nutrients in
in Agriculture, Veterinary Science, broiler chicks fed corn-soybean meal
Nutrition and Natural Resources, diets‖. Italian Journal of Animal
2(071): 6. Science
Li, S., et al. 2018. Effects of dietary 11:1, DOI: 10.4081/ijas.2012.e7
acetic acid on growth performance, Onunkwo, DN.; Jabbar, A.; Talha, M.;
nutrient digestibility, and intestinal Rauf, A.; Javaid, H.; Munir, M.U.;
morphology of broilers. Poultry Irm, N. and Saleem, M.H.2021.
Science, 97(12), 4259-4266. Response of starter broiler chickens to
Liu, Y., et al. 2020. Effects of dietary feed diets treated with organic acids.
formic acid on growth performance, Advancements in Life Sciences,
nutrient digestibility, and intestinal 8(3):257-261.
morphology of broilers. Animals, Paglia, D. E. and Valentine, W. N.
10(1), 110. 1967. Studies on the quantitative and
Lopez-Virella, M.F.; Stone, S.; Eills, S. qualitative characterization of
and Collwel, J. A. 1977. erythrocyte glutathione peroxidase.
Determination of HDL-cholesterol The Journal of Laboratory and Clinical
using enzymatic method. Clin. Chem., Medicine, 70(1):158-169.
Patton, C. J. and Crouch, S.R. 1977.
23: 882-884.
―Enzymati colorimetric method for
Misra, H. P. and Fridovich, I. 1972. The determination of urea in serum‖. Anal.
role of superoxide anion in the Chem. 49, 464- 469
autoxidation of epinephrine and a Placer, Z.A.; Cushman, L. and
simple assay for superoxide dismutase. Johnson, B.C. 1966. Estimation of
Journal. Biol. Chem., 247: 3170–3175. products of lipid peroxidation
107
Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2
(malonyldialdehyde) in biological alternatives to antimicrobials in
fluids. Anal. Biochem. 16, 359–364. poultry rearing: a review. 10(8), 1010;
Rahmani, H. R.; and Speer, W. 2005. https://doi.org/10.3390/antibiotics1008
Natural additives influence the 1010
performance and humoral immunity Shahid, S.; Chand, N.; Khan, R.U.;
of broilers. International Journal of Suhail, S.M. and Khan, N.A. 2015.
Poultry Science, 4: 713-717. Alterations in cholesterol and fatty
Rainger, G. E. and Rowley, A. F. 1993. acids composition in egg yolk of
Antibacterial activity in the serum and Rhode Island Red x Fyoumi hens fed
mucus of rainbow trout, Oncorhyn with hemp seeds (Cannabis sativa L.).
chusmykiss following immunization Journal of Chemistry Article ID
with Aeromonas salmonicida. Fish and 362936
shellfish Immun., 3: 475-482. https://doi.org/10.1155/2015/362936
Reitman, S. and Frankel, S. 1957. A Sharp, P. J.; Calbert, J. and Wells, J. W.
Method for determination of enzymatic 1987. Variation in stored and plasma
activities. American Journal of Clinical Concentrations of androgens and
Pathology, 287: 56-58. luteinizing hormone during sexual
Ricke, S.C. 2003. Perspectives on the development in the cockerel. Journal
use of organic acids and short chain Endocrinology, 74: 467 – 476.
fatty acids as antimicrobials. Poultry Sheikh, A.; Banday, T.; Bhat, G. A.;
Sci 82(4):632–639. Salahuddin, M.; Raquib, M.; and
Rodjan, P.; Soisuwan, K.; Shanaz, S. 2011. Response of broiler
Thongprajukaew, K.; Theapparat, chicken to dietary supplementation of
Y.; Khongthong, S.; organic acids. Journal of Central
Jeenkeawpieam, J. and Salaeharae, European Agriculture,12: 498-508.
T. 2017. Effect of organic acids or Snow, J. L.; Baker, D. H.; and
probiotics alone or in combination on Parsons, C. M. 2004. Phytase, citric
growth performance, nutrient acid and 1 "-Hydrox-choleciferol
digestibility, enzyme activities, improves phytate phosphorus
intestinal morphology and gut utilization in chicks fed a corn-
microflora in broiler chickens. soybean meal diet. Poult. Sci., 83:
Journal of Animal Physiology and 1187-1192.
Animal Nutrition. 102(2):931–940. Stein, E. A. 1986. Quantitative enzymatic
Samanta, S.; Haldar, S. and Ghosh, T. colorimetric determination of total
K. 2010. Comparative efficacy of an cholesterol in serum or plasma. In:
organic acid blend and bacitracin Textbook of Clinical Chemistry. N. W.
methylene disalicylate as growth Tietz, editor. WB. Saunders,
promoters in broiler chickens: efects Philadelphia, USA Pp. 879-886.
on performance, gut histology, and Sureshkumar, S.; Park, J.H. and Kim,
small intestinal milieu. Veterinary I.H. 2021. Efects of the inclusion of
Medicine International, ID 645150, 8 dietary organic acid supplementation
pages doi:10.4061/2010/645150. with anti-coccidium vaccine on
Scicutella, F.; Mannelli, F.; Daghio, growth performance, digestibility,
M.; Viti, C. and Buccioni, A. 2021. fecal microbial, and chicken fecal
Poly- phenols and organic acids as noxious gas emissions. Brazilian
108
Productive performance, broiler chickens, organic acids, growth promoters.
Journal of Poultry Science, 23. Van Immerseel, F.; Russell, J. B.;
http://dx.doi.org/10.1590/1806-9061- Flythe, M. D.; Gantois, I.;
2020-1425. Timbermont, L.; Pasmans, F.;
Talebi, E.; Zarei, A.; and Abolfathi, Haesebrouck F. and Ducatelle, R.
M. E., 2010. Influence of three 2006. The use of organic acids to
different organic acids on broiler combat Salmonella in poultry: a
performance. Asian Journal of mechanistic explanation of the
Poultry Science, 4:7-11. efficacy. AvianPathology.35(3),182-
Tomar, J.S.; Nayak, S.; Baghel, R.P.S.; 188.
Malapure, C.D.; Govil, K. and DOI: 10.1080/03079450600711045.
Thakur, D. 2017. Organic acids Yan, L.; Hong, S.; Kim, I-H. 2012.
supplementation in the diets and Effect of bacteriophage
performance of broiler chicken. Indian supplementation on the growth
J Anim. Nutr. 34(4):458-462. performance, nutrient digestibility,
Trinder, P. 1969. Enzymatic blood characteristics, and fecal
colorimetric determination of glucose microbial shedding in growing
in serum, plasma or urine. Annals of pigs.Asian-Australasian Journal of
Clinical Biochemistry, 6: 24-26. Animal Sciences, 25(10): 1451.
Ullah, F.; Tahir, M.; Naz, S.; Khan, Zeweil, H. S. 1996. Enzyme supplements
N.A. and Khan, R.U. 2022. In vitro to diets growing Japanese quails.
efficacy and ameliorating effect of Egypt. Poult. Sci. J., 16: 535-557.
Moringa oleifera on growth, carcass, Zhang, Z. F.; Yang, X.; Ding, X. M.; et
stress and digestibility of nutrients in al. 2019. Effects of dietary formic acid
Escherichia coli-infected broilers. on growth performance, meat quality,
Journal of Applied Animal Research.
and intestinal microbiota of broilers.
https://doi.org/10.1080/09712119.2022
.2039156 Poultry Science, 98(1), 359-366.

109
‫‪Asmaa Sh. ELnaggar1 and M. I. El-Kelawy 2‬‬

‫الولخص العزبي‬
‫أداء النوو وهعاهالت هضن العناصز الغذائَة وقَاسات الذم لذجاج اللحن الوغذى علي علَقة‬
‫تحتوً علي األحواض العضوٍة‬
‫‪2‬‬
‫أسواء شوقٌ النجار ‪ ،1‬هحوود إبزاهَن الكَالوً‬
‫‪ 1‬قغٌ االّخاج اىحٍىاًّ واىذاجًْ – ميٍه اىضساعت – جاٍعه دٍْهىس‪.‬‬
‫‪ 2‬قغٌ إّخاج اىذواجِ ‪ -‬ميٍت اىضساعت ‪ -‬جاٍعت اىىادي اىجذٌذ‬

‫حهذف اىذساعت إىى حقٌٍٍ حأثٍش ٍغخىٌاث ٍخخيفت ٍِ األحَاض اىععىٌت (اىفىسٍٍل‪ ،‬اىخيٍل‪ ،‬اىغخشٌل) عيى أداء َّى‬
‫دجاج اىيحٌ‪ ،‬وهعٌ اىعْاصش اىغزائٍت‪ ،‬وصفاث اىزبٍحت‪ ،‬وبعط ٍعاٌٍش اىذً‪ ،‬وعذد اىبنخٍشٌا‪ ،‬وحاىت ٍعاداث‬
‫األمغذة‪ ،‬واالعخجابت اىَْاعٍت‪ ،‬واىنفاءة االقخصادٌت‪ .‬حٌ حىصٌع ‪ 212‬مخنىث عَش ٌىً غٍش ٍجْظ عشىائًٍا عيى عبع‬
‫ٍجَىعاث‪ ،‬حٍث ماّج مو ٍجَىعت ححخىي عيى ‪ 5‬حنشاساث بنو ٍْها ‪ 6‬مخامٍج‪ .‬حٌ اعخخذاً اىَجَىعت األوىى‬
‫مَجَىعت ٍقاسّت‪ .‬حٌ حغزٌت اىطٍىس فً اىَجَىعاث ‪ 2‬و ‪ 3‬بعيٍقت ححخىي عيى حَط اىفىسٍٍل (‪ %2.5‬و ‪،)%1.2‬‬
‫بٍَْا حٌ حغزٌت اىطٍىس فً اىَجَىعاث ‪ 4‬و ‪ 5‬بعيٍقت ححخىي عيى حَط اىخيٍل (‪ %2.5‬و ‪ .)%1.2‬وأٍا اىطٍىس فً‬
‫اىَجَىعاث ‪ 6‬و ‪ 7‬فخٌ حغزٌخها بعيٍقت ححخىي عيى حَط اىغخشٌل (‪ %2.2‬و ‪ .)%3.2‬حٌ اىىصُ األعبىعً‬
‫وحغجٍو اعخهالك اىعيف وحقذٌش األداء االّخاجً‪ .‬باإلظافت إىى رىل‪ ،‬حٌ ححيٍو اىَعاٌٍش اىبٍىمٍٍَائٍت واىهٍَاحىىىجٍت‬
‫واىَْاعٍت‪ ،‬إىى جاّب حقٌٍٍ اىْشاغ اىٍَنشوبً ىيجهاص اىهعًَ‪ .‬وقذ ىىحع ححغِ فً األداء االّخاجً‪ ،‬بَا فً رىل‬
‫اىىصُ اىْهائً وٍعذه صٌادة فً وصُ اىجغٌ‪ٍ ،‬ع اعخخذاً اظافاث حَط اىفىسٍٍل واىخيٍل واىغخشٌل‪ ،‬باإلظافت‬
‫إىى ححغِ فً ٍعذه ححىٌو اىعيف‪ .‬صادث ّغبت اىزبٍحت بٍَْا قيج ّغبت اىذهىُ اىبطٍْت ٍع االعخخذاً‪ .‬مشف اىخحيٍو‬
‫اىهٍَاحىىىجً عِ ححغِ فً ٍقاٌظ اىذً‪ .‬مَا أثشث االظافاث بشنو إٌجابً عيى ٍنىّاث اىذً ٍِ اىبشوحٍْاث‬
‫واىذهىُ‪ .‬باإلظافت إىى رىل‪ ،‬حٌ حعضٌض اىحاىت اىَعادة ىألمغذة واىَْاعٍت‪ٍَ ،‬ا ٌخجيى فً صٌادة ّشاغ اإلّضٌَاث‬
‫اىَعادة ىألمغذة واالعخجابت اىَْاعٍت‪ .‬عالوة عيى رىل‪ ،‬أدث اىَنَالث إىى حغٍٍشاث إٌجابٍت فً حشمٍبت اىبنخٍشٌا فً‬
‫األٍعاء‪ٍ ،‬ع صٌادة فً ٍغخىٌاث اىالمخىباعٍيىط واّخفاض فً عذد اىبنخٍشٌا‪ ،‬بَا فً رىل ‪ E. Coli‬واىبشوحٍىط‪.‬‬
‫فً اىخخاً‪ ،‬فإُ إظافت األحَاض اىععىٌت مبذٌو ىيَعاداث اىحٍىٌت فً حغزٌت دجاج اىيحٌ ٌعضص بشنو مبٍش أداء‬
‫اإلّخاج وحعضص اىنفاءة االقخصادٌت ٍع اىحفاظ عيى اىصحت األٍثو‪.‬‬

‫‪110‬‬