The Potential of Spirulina Platensis To Substitute Antibiotics in Japanese Quail Diets - Impacts On Growth, Carcass Traits, Antioxidant Status, Blood Biochemical Parameters, and Cecal Microorganisms

The potential of Spirulina platensis to substitute antibiotics in Japanese quail
diets: impacts on growth, carcass traits, antioxidant status, blood biochemical

parameters, and cecal microorganisms
Mashail A. Alghamdi,* Fayiz M. Reda,y Hemat K. Mahmoud,z Safia M. A. Bahshwan,x Heba M. Salem,#
Wafaa Ahmed Alhazmi,k Abel-Fattah Salah Soror,{ Nadeen G. Mostafa,** Sally Attia,**
Mazhar D. A. Mohamed,yy Ahmed M. Saad,zz Khaled A. El-Tarabily ,xx,1 and Asmaa Sayed Abdelgeliel##
Biology Department, Faculty of Science, King Abdulaziz University, Jeddah 21589, Saudi Arabia; yPoultry
*
Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt; zDepartment of Animal Production,
Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt; xBiological Sciences Department, College of Science and
Arts, King Abdulaziz University, Rabigh 21911, Saudi Arabia; #Department of Poultry Diseases, Faculty of Veterinary
Medicine, Cairo University, Giza 12211, Egypt; kDepartment of Medical Laboratory Sciences, Faculty of Applied Medical
Sciences, King Abdulaziz University, Jeddah 21589, Saudi Arabia; {Botany and Microbiology Department, Faculty of
Science, Zagazig University, Zagazig 44519, Egypt; **Department of Agricultural Microbiology, Faculty of Agriculture,
Zagazig University, Zagazig 44511, Egypt; yyAgricultural Microbiology Department, Faculty of Agriculture, Sohag
University, Sohag 82524, Egypt; zzBiochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511,
Egypt; xxDepartment of Biology, College of Science, United Arab Emirates University, Al Ain 15551, United Arab Emirates;
and ##Department of Botany and Microbiology, Faculty of Science, South Valley University, Qena 83523, Egypt
ABSTRACT The development of antibiotic-resistant antioxidant profile, immunological parameters, and cecal
microorganisms prompted the investigation of possible anti- microorganism’s count. There were no significant changes in
biotic substitutes. As a result, the purpose of the current the percentage of carcasses, liver, and total giblets among all
study is to assess the effect of dietary Spirulina platensis the 5 groups. Only gizzard percentage showed a significant
extract as an antibiotic alternative on Japanese quail increase in G2 compared to birds in G1. In addition, intesti-
(Coturnix japonica) growth, antioxidant status, blood nal pH showed a significant drop in G2 and G5 compared to
parameters, and cecal microorganisms. There was a total of birds in G1. After cooking the quail meat, the juiciness and
150 Japanese quails used in this study, divided equally tenderness increased as S. platensis extract levels increased,
among 5 experimental groups (10 birds per group with 3 rep- whereas aroma and taste declined slightly as S. platensis
licates): group 1 (G1) received a basal diet without any S. extract levels increased. Furthermore, when a high concen-
platensis extract, group 2 (G2) received a basal diet supple- tration of S. platensis extract was used, the lightness of the
mented with 1 mL S. platensis extract/kg, group 3 (G3) meat reduced while its redness and yellowness increased.
received a basal diet supplemented with 2 mL S. platensis The disk diffusion assay showed that S. platensis extract
extract/kg, group 4 (G4) received a basal diet supplemented had significant antibacterial activity against Staphylococcus
with 3 mL S. platensis extract/kg, and group 5 (G5) aureus, Listeria monocytogenes, Campylobacter jejuni, and
received a basal diet supplemented with 4 mL S. platensis Salmonella typhi, with inhibition zones ranging from 16 to
extract/kg from d 7 until d 35. The results showed that com- 42 mm. This activity may be attributable to the volatile
pared to the control birds in G1, Japanese quail supple- chemicals in S. platensis extract, of which Geosmin and 2-
mented with 4 mL of S. platensis extract/kg of diet (G5) methylisoborneol are the primary components. In the diet of
had significantly better live body weight, body weight gain, Japanese quails, it is possible to draw the conclusion that the
feed intake, feed conversion ratio, digestive enzymes, blood extract of S. platensis can be utilized as a feed additive and
parameters, liver and kidney functions, lipid profile, as an alternative to antibiotics.
Key words: antibiotic alternative, cecal microorganisms, Japanese quail, liver and kidney functions, Spirulina
platensis
2024 Poultry Science 103:103350
https://doi.org/10.1016/j.psj.2023.103350
Ó 2023 The Authors. Published by Elsevier Inc. on behalf of Poultry Accepted December 1, 2023.
Science Association Inc. This is an open access article under the CC BY- 1
Corresponding author: [email protected]
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Received October 23, 2023.
1
2 ALGHAMDI ET AL.
INTRODUCTION microalgae to boost nutritional value, especially that of

n-3 fatty acids (Chaves et al., 2021).
The widespread use of antibiotics in the chicken busi- Prebiotics and other natural herbal feed additives are
ness produces a selective environment that promotes the introduced as a viable alternative to antibiotics and pro-
establishment of antibiotic-resistant bacteria (Shi et al., ductive agents that can boost growth (Samad, 2022).
2019). These microorganisms can cause illness in Spirulina is a nutrient-rich supplement that contains
humans as well as animals, and they can be transmitted high levels of protein, essential fatty acids, essential
by direct contact with infected animals or intake of amino acids, vitamins, and minerals (Cheong et al.,
contaminated poultry and livestock food products 2010; Jafari et al., 2014).
(Majumder et al., 2020). Antibiotic use in food produc- Spirulina is quickly becoming one of the most widely used
tion has resulted in antibiotic resistance, antibiotic resi- ingredients in broiler feed across the globe, particularly in
dues in food, and a decline in the diversity of normal gut the organic and natural poultry industries. This is because of
microflora (Abd El-Hack et al., 2022b,c). The presence a variety of characteristics, including its high nutritional
of antibiotic residues in chicken products, such as eggs value, ability to increase broiler performance, and potential
or meat, is detrimental to human health because these to reduce antibiotic use in poultry production (Bonos et al.,
compounds cause pathogenic microorganisms found in 2016). Spirulina belongs to cyanobacteria, a family of single-
human flora to develop resistance to these antibiotic celled organisms often called blue-green algae. Spirulina can
groups (Mancuso et al., 2023). live and grow in salt and fresh waters (El-Shall et al., 2023).
The European Union has already banned the use of Spirulina is always used as a supplementary food resource
antibiotics as growth enhancers for broilers because of and growth promoter for livestock due to its high iron con-
the rise in antibiotic-resistant microorganisms and the tent, protein, phosphorus, and all essential and nonessential
potential threat posed by drug residues in chicken (Cas- amino acids (Alaqil et al., 2023).
tanon, 2007; El-Saadony et al., 2022). The continuous Spirulina is a nutrient-rich, harmless, and nontoxic
development of poultry has resulted in the usage of anti- organism that improves the health, growth, and repro-
biotics to prevent disease and boost the production duction of mammals and birds (Alaqil et al., 2023).
potency of meat and eggs (Salem et al., 2023). Over the Feeding broilers with Spirulina as a growth enhancer
course of the past 20 yr, the use of nutritional supple- improves their performance by increasing their feed con-
ments like probiotics and prebiotics, among others, has version ratio, live body weight gain and carcass yield
been investigated as a possible replacement for antibiot- percentages than broilers consumed basal diet (Samarth
ics (Abd El-Hack et al., 2022a). et al., 2002; Kharde et al., 2012). Spirulina platensis-con-
Large amounts of attention have been paid to microal- taining diets for chickens significantly increased meat
gae because of the widespread belief that they contain production compared to control diets (Iatrou et al.,
great nutritional value (Abd El-Hack et al., 2023). As a 2022). It has also been reported that Spirulina helps
direct consequence of this, a great amount of work has with the digestion of nutrients, the absorption of miner-
been put into determining their usefulness as a source of als, and the prevention of diarrhea (Gruzauskas et al.,
atkiewicz
feed (Swi ˛ et al., 2015; Kanagaraju and Ompra- 2004). In addition, Spirulina has been shown to boost
kash, 2016). immunological response and reproduction (Qureshi et
Algae are a great source of food and trace elements and al., 1996; Khan et al., 2005). A modest amount of Spiru-
are regarded as one of the most important foods of the lina in the diet has also been shown to greatly increase
21st century (Abd El-Hack et al., 2023; El-Sheekh et al., the antigen-processing defense system (T-cell) and
2023). Algae products are good sources of protein, vita- decrease the harmful microbial community (Qureshi et
mins, enzymes, trace elements, antioxidants, pigments, al., 1996; Kaoud, 2012).
carbohydrates, and fatty acids, but most importantly, In the majority of earlier investigations, the focus was
they contain high amounts of the beneficial polyunsatu- on the effect of Spirulina on development and immunol-
rated fatty acids, that is, omega-3 fatty acids, particularly ogy; however, these studies did not find any influence on
eicosapentaenoic acid and docosahexaenoic acid (Abd El- intestinal bacteria or meat quality, particularly in Japa-
Hack et al., 2023; El-Sheekh et al., 2023). The amino acid nese quails (Coturnix japonica). Therefore, the purpose
content of a wide variety of algae has been analyzed, and of this investigation is to determine the effect of S. pla-
the results have shown that although there is a great deal tensis extract as a feed additive and alternative to anti-
of variance, overall, these algae do contain all the neces- biotics on the productivity, carcass parameters, blood
sary amino acids (Abd El-Hack et al., 2023). parameters, liver and kidney functions, lipid profile,
Algae are primarily added into poultry diets as a cecal microbial content, antioxidant level, and avian
source of long-chain n-3 polyunsaturated fatty acids. immunity of the quails that were tested.
Most studies have indicated that microalgae, namely
Spirulina and Chlorella derived from defatted biomass
from biofuel production, may be used successfully as a MATERIALS AND METHODS
feed element in poultry nutrition (Saadaoui et al., 2021; Isolation of Spirulina
Abd El-Hack et al., 2023). The beneficial impact of poly-
unsaturated fatty acids on human health inspired inter- The Spirulina isolate was originally obtained from
est in supplementing chicken diets with defatted Soda Lake in Wadi El Natrun, Beheira governorate,
SPIRULINA PLATENSIS AS ANTIBIOTIC ALTERNATIVE 3
Egypt. Zarrouk’s medium (Zarrouk, 1966) was used in temperature was 280°C, and the injector was 250°C.
the process of isolating and cultivating a pure culture of Wiley 9 databases were applied to identify peaks, follow-
Spirulina, which was comprised of (g/L) K2HPO4 0.5 g; ing Saad et al. (2021a).
NaHCO3 16.8 g; NaCl 1.0 g; NaNO3 2.5 g; MgSO4¢7H2O
0.2 g; K2SO4 1.0 g; CaCl2¢2H2O 0.04 g; FeSO4¢7H2O
0.01 g; and EDTA 0.08 g. The pH was adjusted to 9.5 Experimental Design
using KOH 1 M. From the day they hatched until the completion of the
In order to obtain pure Spirulina cultures, we inoculated trial, the birds were supplemented with varying volumes
250 mL aliquots of Zarrouks medium in 500 mL screw bot- of S. platensis extract added to the prepared feed
tles with 10 mL of a 5-day-old culture. The bottles were (mash) and mixed thoroughly.
incubated for 10 d at 25°C § 2°C while being exposed to There was a total of exactly 150 Japanese quail chicks,
constant light (600−800 lux) from a 36 W white, fluores- and they were randomly divided up into 5 groups, with
cent bulb. The streaking method on Zarrouk’s medium each group having 3 replicates of 10 chicks. The control
was used to collect the pure culture of Spirulina from the group (G1) was fed with basal diet without any S. platen-
bottles. The plates were incubated below continuous illu- sis extract, while the other 4 groups from groups 2 to 5
mination (600 lux) at 25°C § 2°C. Colonies were collected (G2−G5) were fed the same basal ration supplemented
and examined under a microscope, and Spirulina colonies with 1 mL/kg of S. platensis extract, 2 mL/kg of S. pla-
were kept on slants on Zarrouk’s media. tensis extract, 3 mL S. platensis extract/kg, and 4 mL S.
platensis extract/kg, respectively, for 35 successive days.
Identification of Spirulina Isolates A completely randomized design was used, where all
chicks under study were reared on a litter model. Birds
The morphological identities of Spirulina isolates were were housed in batteries consisting of 3 decks and 2 sec-
determined by observing them under a microscope at tions of cages with automatic watering and were fed and
various stages of their growth in Zarrouk’s medium. watered ad libitum. Standard growing rations contained
24 % crude protein, 2995 kcal/kg diet metabolizable
energy (ME), 0.80 % Ca, and 0.45 % nonphytate phos-
Extraction of S. platensis Extract phate. Individual birds’ weights were recorded weekly,
Cold water was used to extract S. platensis after ini- and feed intakes for all groups were recorded daily. After
tially homogenizing 10 g of Spirulina powder in 100 mL the experiment, blood from the wing veins was collected
of distilled water at a weight-to-weight ratio of 1:10. After into EDTA- vials for further examination. This project has
that, a pellet was formed by rapidly freezing the suspen- received ethical approval from the Research Ethics Commit-
sion in a refrigerator set to a temperature of 20°C to tee, Faculty of Science, South Valley University, Qena,
form a pellet. After defrosting the pellets at 4°C, they Egypt, (REC-FScSVU) with Code number (006/10/23).
were centrifuged to collect the supernatant. The superna-
tant was dried into a powder containing the physiologi- Determination of Growth Performance
cally active components after 48 h of lyophilization.
Quail live body weights (LBW), and feed consump-
tion (per pen) were recorded, and the body weight gain
Identification of Volatile Compounds in (BWG) was calculated by the difference between the
S. platensis Extract by Gas Chromatography final live body weight (35-d of age) and initial live body
−Mass Spectrometry weight (7-d of age). Furthermore, the feed conversion
ratio (FCR) was calculated by dividing feed
The S. platensis supernatant was extracted with n-
consumption by BWG, according to Saad et al. (2022).
hexane (Sigma-Aldrich Chemie GmbH, Taufkirchen,
Germany). For 10 min, the hexane and S. platensis Body weight gainðBWGÞ
supernatant were shaken together in a separating fun- ¼ ðFinal live body weight initial live body weightÞ=Period by days
nel. After that, the liquid was allowed to settle for 5 min ð1Þ
so that 2 layers could form. The upper layer was
removed and evaporated, and the remaining residue was
dried in a rotary vacuum evaporator to produce the Growth rate ðGRÞ
crude extract. Gas chromatography−mass spectrometry
(GC−MS) was used to identify the bioactive chemicals ¼ ðLBW35 LBW1Þ=0:5 ðLBW1 þ LBW35Þ ð2Þ
in S. platensis extract. One mL of S. platensis extract
was inoculated into the GC−MS (Agilent 6890, Foster
City, CA) equipped with a column (HP-5 MS) and an Measurements of Carcass Traits
Agilent mass spectrometer detector (Agilent). At a
1.0 mL/min flow rate, helium was employed as a carrier Three birds per replication were chosen randomly and
gas. The sample size 1 mL was added, and the solvent weighed at the end of the experiments. Following the
was delayed for 3 min. The temperature program went collection of body measurements, the birds were slaugh-
from 40°C to 260°C at a rate of 8°C/min. The detector tered for the purpose of analyzing the features of the
4 ALGHAMDI ET AL.
corpse. These features included the carcass, the dressing Measurement of the Immunological
percentage, and the weight of the visceral organs, which Parameters
included the giblets, heart, liver, and gizzard. The pH of
the intestinal tract was also measured (Zhou et al., Lysozyme activity, an enzyme that aids in the fight
2023). against infection, was evaluated by collecting blood sam-
ples at the end of the study. The lysozyme activity was
determined using the standard activity of each assay,
Determination of the Digestive Enzyme which was calibrated in units of activity per mg under
Activities experimental conditions (37°C) to allow for a direct com-
parison of these 2 assays.
At the end of the investigation, we evaluated the lev-
The turbidimetric assay was performed using a
els of amylase, protease, and lipase activity in the ileum
0.36 mg/mL Micrococcus lysodeikticus suspension and a
(small intestine) of the birds (1/replicate). The quail
microtiter plate reader capable of analyzing enzyme
ileum was dissected from the Meckel’s diverticulum (a
kinetics at 450 nm as recommended by Helal and Melzig
tiny pouch in the ileum) to 2 cm above the ileocecal junc-
(2008).
tion (the ileum-cecum junction). The contents of the
Immunoglobulin isotypes IgM, IgG, and complement
ileum were collected in sterile, screw-capped vials to
3 were assayed using enzyme-linked immunosorbent
avoid contamination.
assay (ELISA) technique (Gao et al., 2023).
The ileal enzyme activity was estimated using the
method developed by Najafi et al. (2005). Amylase assay
was performed at 55°C for 20 min in a 40 mL reaction
mixture, with 35 mL of 1% (w/v) of soluble starch in Measurement of the Antioxidant Activities
50 mM of citrate buffer, pH 6, and 5 mL of suitably
diluted enzyme solution. The reducing sugar released At the time of the slaughter, blood samples were
from starch was measured by dinitro salicylic acid drawn from 9 birds in each group, centrifuged at
(DNSA) (Sigma-Aldrich) at 540 nm using glucose as 4,500 rpm for 20 min, and the plasma that was separated
standard. One unit of enzymatic activity is defined as was stored at -20°C. Malondialdehyde, a lipid oxidation
the amount of enzyme required to produce 1 mM of glu- marker; antioxidant enzyme levels, superoxide dismutase,
cose/min under assay conditions. catalase, glutathione, and total antioxidant capacity
were all measured using Biodiagnostic commercial kits.
Evaluation of Blood Parameters
Blood was collected from the wing veins of quails (3 Histopathological Examination
birds/replicate) using gauge needles in labeled screw-top
tubes to obtain plasma containing 200 mL of EDTA as Intestinal and liver segments were collected, then pre-
an anticoagulant to study various blood parameters (red served in 10% neutral buffered formalin for 48 h, washed
blood cells, hemoglobin, and white blood cells) as recom- with water, dehydrated through ascending grades of
mended by Zhou et al. (2023). alcohol (70, 80, 95, 95, and 100%), cleared with xylene,
paraffin embedded, sectioned at 5 mm with a microtome
(Leica Camera AG, Wetzlar, Germany) and stained
Determination of Liver, Kidney Functions, with hematoxylin and eosin (Suvarna et al., 2018).
and Serum Lipid Profile Sections were examined using light microscope
Blood samples were collected at 35-d old from the (Olympus BH-2, Olympus Optical Co. Ltd., Tokyo,
slaughtered chicks immediately into a tube with an anti- Japan) equipped with a digital camera and software
coagulant to obtain plasma by centrifugation of blood (Jenoptik ProgRes Camera, C12plus, Frankfurt, Ger-
sample at 4,000 rpm for 10 min. many).
The plasma was poured into the clean tube, which was
then sealed completely and stored at -20°C until it was
used. Evaluation of the Meat Quality
The biochemical measurement methods were photo-
metrical, using a spectrophotometer (Apel 310 Spectro- Ten experienced panelists examined meat cubes (3
photometer, Saitama, Japan). The biochemical profiles cm) for sensory evaluation. The breast samples were
alanine transaminase, aspartate transaminase, urea, cre- coded with 3 random digits and presented to the panel-
atinine, total protein, total globulin, albumin/globulin ists. The sensory features (color, flavor, appearance, and
ratio, triglycerides, total cholesterol, high-density lipo- juiciness) were scored on a nine-point hedonic scale,
protein (HDL), low-density lipoprotein (LDL), and the with 1 being a strong dislike and 9 reflecting a strong
very low-density lipoprotein (VLDL) levels were mea- liking.
sured using an automated analyzer and a Biodiagnostic To break up the monotony of the mouthfeel, tap
commercial kit (Biodiagnostic, Giza, Egypt) following water was given to the participants in between sessions
the manufacturer’s instructions (Zhou et al., 2023). (Abd El-Hack et al., 2021).
Estimation of Cecal Microbial Load the plates. After incubation of the LB plates at 37°C in
the dark for 2 d, the inhibition zone diameters were
At 35-d old, 3 birds were slaughtered from each repli- determined in mm (Saad et al., 2021b). The minimum
cation (a total of 9 birds per group) to collect cecal con- inhibitory concentration of S. platensis extract was
tent. The caeca were separated, and the contents were determined according to El-Saadony et al. (2021).
aseptically collected in sterile cups. The inoculums were
serially diluted in a sterile ependymal tube using a 1 mL
suspension with 9 mL of normal saline. Statistical Analysis
Cecal samples were serially diluted 10 times to a dilu-
tion level of 106. Aliquots (0.2 mL) were spread with a Statistical analysis was carried out using 1-way analy-
sterile glass rod over the surface of different general pur- sis of variance (ANOVA). SPSS software (IBM SPSS
poses and selective agar media in sterile plastic Petri 23 Statistics for Mac OS, Armonk, NY) was used for all
dishes (90 mm diameter). Plates were dried in a laminar statistical analyses. All tested means (treatment) were
flow-cabinet for 20 min before incubation at 37°C in the compared by LSD test at a probability of P<0.05, which
dark for 2 d and colony counts were carried out. Six was required for significance. The 2 sample size was evalu-
plates per dilution were made for each sample for each ated from the equation n ¼ ZSD E .
replicate. Population densities were expressed as log10
colony forming units (CFU) g/dry cecal weight. RESULTS
The groups of organisms selected for enumeration and
the media used were as follows: i) total aerobic bacteria Identifications of Volatile Compounds in
on nutrient agar medium (Product Code: LAB008) (Lab S. platensis Extract by GC−MS
M Limited, Lancashire, United Kingdom); ii) total
The composition of volatile compounds in the S. pla-
yeasts and molds count on Sabouraud dextrose agar
tensis extract is displayed in Table 1. The extraction of
(Product Code: MH063) (HiMedia Laboratories Pvt.
volatile compounds is critical for identifying Spirulina
Ltd., Mumbai, India); iii) Escherichia coli on eosin
distinct aroma. It can also be used to analyze the flavor.
methylene blue (EMB agar) (Product Code: LAB061)
Geosmin and 2-methylisoborneol are the main com-
(Lab M Limited); iv) total coliforms on MacConkey
pounds that cause Spirulina to have an unpleasant taste
agar medium (Product Code: LAB045) (Lab M
and odor, even at very low concentrations. Very low lev-
Limited); v), Enterococcus spp. on Pfizer selective
els of b-cyclocitral, and b-ionone, 2-methylisoborneol, 2-
Enterococcus agar (Product code: M787) (HiMedia
pentylfuran, and geosmin were naturally detected in S.
Laboratories); and vi) Salmonella spp. on xylose lysine
platensis in the current study (Table 1).
decarboxylase agar (XLD agar) (Product Code:
LAB032) (Lab M Limited).
Determination of Growth Performance
Antimicrobial Activity of S. platensis Extract Table 2 shows that compared to the negative control
Against Pathogenic Bacteria birds (G1), all groups treated with S. platensis extract
had significantly higher LBW in wk 3 and 5. All groups
S. platensis suspensions were made at various concen- given varying doses of S. platensis extract showed signif-
trations (40, 80, 160, 320, and 640%). Disks (6 mm) icantly greater BWG increase from the first to third
were immersed in each concentration for 30 min. The weeks of life compared to the un-supplemented control
extract of S. platensis was tested against Staphylococcus G1 birds (Table 2). There was a noticeable significant
aureus, Listeria monocytogenes, Campylobacter jejuni, increase in BWG from the third to the fifth week of the
and Salmonella typhi. birds’ age in groups G2, G3, and G5, as compared to
After inoculating Luria-Bertani (LB) agar (Lab M groups G1 and G4 (Table 2).
Limited) plates with the pathogenic bacteria, S. platen- The birds who were given S. platensis extract had a
sis extract-saturated disks, were placed in the middle of significantly higher BWG compared to the birds that
Table 1. Volatile compounds profile in Spirulina platensis extract.
Chemical properties
Number Detected volatile compounds Formula Molecular weight (g/mole) Volatile compounds (%)
1 Pentadecane C15H32 212.24 5.9 c
2 Hexadecane C16H34 226.44 5.2 c
3 Heptadecane C17H36 240.47 62.0 a
4 b-Cyclocitral C10H16O 152.23 0.45 e
5 b-Ionone C13H20O 192.3 5.1 c
6 2-Methylisoborneol C11H20O 168.28 0.3 e
7 2-Pentylfuran C9H14O 138.21 2.1 d
8 Geosmin C12H22O 182.3 21.6 b
Values with same letter in a column are not significantly (P>0.05) different according to protected least significant difference (LSD) test.
6 ALGHAMDI ET AL.
Table 2. Effect of dietary supplementation of Spirulina platensis extract on body measurements, live body weight, body weight gain,
feed intake, and feed conversion ratio of Japanese quails.
Spirulina platensis extract level (mL/kg diet)

Body measurements G1 G2 G3 G4 G5 SEM P value
Body weight (g)
1 wk 29.66 a 29.59 a 29.39 a 29.73 a 29.44 a 0.550 0.9900
3 wk 102.45 b 110.92 a 108.18 a 109.09 a 111.41 a 1.700 0.0260
5 wk 205.66 b 223.53 a 220.64 a 214.86 a 222.80 a 2.609 0.0043
Body weight gain (g/d)
1−3 wk 5.20 b 5.81 a 5.63 a 5.67 a 5.86 a 0.082 0.0016
3−5 wk 7.37 b 8.04 a 8.03 a 7.56 b 7.96 a 0.112 0.0093
1−5 wk 6.29 c 6.93 a 6.83 ab 6.61 b 6.91 a 0.080 0.0010
Feed intake (g/d)
1−3 wk 14.92 a 14.65 a 15.63 a 15.32 a 15.25 a 0.460 0.6503
3−5 wk 25.89 a 23.35 b 24.05 b 23.87 b 23.7 b 0.413 0.0131
1−5 wk 20.41 a 19.00 a 19.84 a 19.60 a 19.50 a 0.436 0.3141
Feed conversion ratio (g feed/g gain)
1−3 wk 2.88 a 2.52 a 2.78 a 2.70 a 2.61 a 0.093 0.1915
3−5 wk 3.51 a 2.90 b 3.00 b 3.17 b 2.99 b 0.084 0.0053
1−5 wk 3.25 a 2.74 b 2.91 b 2.97 ab 2.83 b 0.087 0.0235
G1, control birds with basal diet without Spirulina platensis extract; G2, birds supplied with 1 mL S. platensis extract/kg diet; G3 birds supplied with
2 mL S. platensis extract/kg diet; G4, birds supplied with 3 mL S. platensis extract/kg diet; and G5, birds supplied with 4 mL S. platensis extract/kg
diet. Values with same letter in a column are not significantly (P>0.05) different according to protected least significant difference (LSD) test. SEM, stan-
dard error of the mean value.
were given G1 for the entire study period (wk 1−5); Determination of the Digestive Enzyme
more specifically, the birds that were given 4 mL S. pla- Activities
tensis extract/kg food had the highest BWG (6.91 g,
P = 0.0010) (Table 2). In contrast to the birds in G1 Table 4 showed that the levels of digestive enzymes,
that did not receive any S. platensis extract, those birds such as lipase, were significantly higher in G5 (45.57
whose diets were supplemented with it exhibited a sig- U/g) compared to G1 (8.92) with a P value of less than
nificant reduction in feed intake from the third to the 0.0001. Similarly, the levels of protease were signifi-
fifth week only (Table 2). cantly higher in all groups that were given S. platensis
From the third to the fifth week of age, the FCR indicated extract, compared to the birds in G1 that were not sup-
that all birds given S. platensis extract had significantly plemented with S. platensis extract (Table 4). In com-
lower FCR compared to birds in G1 (Table 2). The cumula- parison to birds in groups 1, 2, and 3, the amylase level
tive FCR was highest at (G2) and (G5), with values of 2.74 was significantly higher in groups 4 and 5 (Table 4).
and 2.83, respectively, at a P value of 0.0235 (Table 2).
Evaluation of Blood Parameters

Measurements of Carcass Traits
The blood parameters showed a marked improve-
As shown in Table 3, there were no significant changes ment in the birds given dietary S. platensis extract
in the percentage of carcass, liver, and total giblets. Only compared to the birds in G1, as seen in Table 5. In
gizzard percentage showed a significant increase in G2 contrast to G1, the hemoglobin level in G2, G3, G4,
(1 mL S. platensis extract/kg diet) compared to birds in and G5 showed a significant increase (P
G1 (Table 3). In addition, intestinal pH showed a signifi- value = 0.0246) (Table 5). When birds in G5 were
cant drop in G2 (6.25) and G5 (6.23) compared to birds given 4 mL S. platensis extract/kg of feed, their red
in G1 (6.88) at P = 0.0001 (Table 3). blood cell count was significantly higher than in G1
Table 3. The impact of dietary supplementation of Spirulina platensis extract on carcass traits and intestinal pH of Japanese quails.

Carcass traits G1 G2 G3 G4 G5 SEM P value
Carcass % 70.89 a 72.24 a 73.47 a 71.35 a 74.17 a 1.836 0.6920
Liver % 2.13 a 2.25 a 2.22 a 2.09 a 2.18 a 0.123 0.8816
Gizzard % 1.98 b 2.39 a 2.15 ab 2.07 b 2.25 ab 0.083 0.0474
Heart % 0.89 b 0.94 a 0.93 a 0.84 b 0.95 a 0.104 0.9290
Giblets % 5.01 a 5.59 a 5.30 a 5.00 a 5.38 a 0.135 0.1126
Dressing % 75.89 c 77.82 b 78.77 a 76.35 bc 79.55 a 1.728 0.045536
Intestinal pH 6.88 a 6.25 d 6.50 b 6.37 c 6.23 d 0.037 0.0001
Table 4. The impact of dietary supplementation of Spirulina platensis extract on digestive enzymes, lipase, protease, and amylase of
Japanese quails.

Enzymes (IU/L) G1 G2 G3 G4 G5 SEM P value
Lipase 8.92 d 15.81 c 12.25 cd 23.70 b 45.57 a 1.906 0.000056
Protease 1.02 c 1.44 ab 1.46 ab 1.37 b 1.59 a 0.060 0.0009
Amylase 10.29 c 11.70 c 11.02 c 17.27 b 23.27 a 1.143 0.000016
Table 5. The impact of dietary supplementation of Spirulina platensis extract on hematological properties of Japanese quails.

Hematological parameters G1 G2 G3 G4 G5 SEM P value
Hemoglobin (g/dL) 9.93 b 11.95 a 12.62 a 13.08 a 12.40 a 0.563 0.0246
Red blood cells count £ 106/mL 2.36 d 3.12 cd 3.42 bc 4.12 ab 4.39 a 0.236 0.0018
White blood cells count £ 102/mL 13.32 b 13.95 b 13.72 b 15.45 ab 17.24 a 0.637 0.0095
dard error of the mean value. g/dL, grams per deciliter.
(Table 5). In G5 birds, the white blood cell count was functions, urea and creatinine levels were significantly
significantly higher than in G1 birds (Table 5). lower in birds fed different S. platensis extract from G2
to G5 compared to unfed birds in G1 (Table 6).
Total cholesterol levels were significantly lower in
Determination of Liver, Kidney Functions birds supplied with varying S. platensis extract levels in
and Serum Lipid Profile G2, G3, G4, and G5 as compared to unsupplied birds in
G1 (Table 7). Birds (G2) had a significant drop in total
Table 6 shows that compared to birds in G1, birds cholesterol levels (141.01) when compared to other
given a 4 mL S. platensis extract/kg meal had a signifi- groups (P value <0.0001) (Table 7). Triglyceride levels
cantly higher total protein. Albumin levels appear to be were significantly lower in all experimental groups given
significantly higher in G3 birds compared to G1, G2, S. platensis extract compared to birds in G1, at
and G4 birds (Table 6). Furthermore, globulin levels in P<0.0001 (Table 7). The HDL levels were significantly
birds increased significantly in G5 compared to G1, G2, higher in birds in G5, indicating that the highest level of
G3, and G4 (Table 6). The albumin/globulin ratio S. platensis extract improved the lipid profile (53.16) at
showed a significant reduction in G5 in contrast with G1 P = 0.0002 (Table 7).
(Table 6). LDL levels decreased significantly in birds fed differ-
In terms of liver function, alanine transaminase, ent S. platensis extract, with birds fed G2 showing a sig-
aspartate transaminase levels in G5 birds were signifi- nificant reduction in LDL levels (62.46) compared to G1
cantly lower than in G1 birds. In terms of kidney (187.91 mg/dL) at P value <0.0001 (Table 7). VLDL
Table 6. The impact of dietary supplementation of Spirulina platensis extract on liver and kidney functions of Japanese quails.

Liver and kidney functions G1 G2 G3 G4 G5 SEM P value
Total protein (g/dL) 2.90 c 3.25 bc 3.65 ab 2.82 c 4.02 a 0.182 0.0061
Albumin (g/dL) 1.71 bc 1.71 bc 2.24 a 1.46 c 2.13 ab 0.132 0.0103
Globulin (g/dL) 1.19 c 1.55 b 1.41 bc 1.36 bc 1.89 a 0.085 0.0022
Albumin/globulin ratio (%) 1.44 a 1.12 b 1.59 a 1.07 b 1.12 b 0.057 0.0026
Alanine transaminase (IU/L) 11.49 a 4.72 c 8.58 b 8.13 b 6.26 bc 0.768 0.0012
Aspartate transaminase (IU/L) 145.60 a 137.70 a 151.00 a 103.64 b 118.75 b 5.371 0.0005
Urea (mg/dL) 5.82 a 2.46 d 2.67 cd 4.10 bc 4.48 ab 0.471 0.0040
Creatinine (mg/dL) 0.71 a 0.56 bc 0.50 c 0.60 b 0.58 bc 0.024 0.0034
dard error of the mean value. g/dL, grams per deciliter.
8 ALGHAMDI ET AL.
Table 7. The impact of dietary supplementation of Spirulina platensis extract on lipid profile of Japanese quails.

Lipid profile G1 G2 G3 G4 G5 SEM P value
Total cholesterol (mg/dL) 264.82 a 141.01 c 150.45 bc 170.45 b 162.40 bc 7.812 <0.0001
Triglycerides (mg/dL) 233.78 a 192.75 b 136.35 c 134.75 c 152.37 c 5.358 <0.0001
High-density lipoprotein (mg/dL) 30.15 c 40.00 b 51.06 a 43.57 b 53.16 a 2.164 0.0002
Low-density lipoprotein (mg/dL) 187.91 a 62.46 c 72.12 c 99.94 b 78.77 c 4.912 <0.0001
Very low-density lipoprotein (mg/dL) 46.76 a 38.55 b 27.27 c 26.95 c 30.47 c 1.072 <0.0001
dard error of the mean value. mg/dL, milligrams per deciliter.
levels were found to be significantly lower in G4 birds sections. In Figure 1A the upper panel showed that the
(26.95 mg/dL) as compared to G1 birds at P value denuded villi tips have desquamation of enterocytes into
<0.0001 (Table 7). The data showed that food supple- their lumina with limitation of their goblet cells, while
mentation with S. platensis extract improved the bird’s the birds supplied with S. platensis extract showed
lipid profile when compared to un-supplemented control enhancement of villi structure with marked thin villi
birds (Table 7). with little goblet cells metaplasia in a dose-dependent
pattern (Figure 1B−E lower panel). While, in Figure 1A
−E in the lower panels, the liver of control quail (birds
Measurement of the Immunological not supplied with S. platensis extract), showed no signif-
Parameters and Antioxidant Activities icant differences between control untreated birds and
birds supplied with different concentrations of S. platen-
As shown in Table 8, the immune profile revealed that sis extract as all the 5 groups revealed normal cell archi-
the birds in G2 had significantly higher levels of IgG, tecture without any structural abnormalities (Figure 1).
and G3 had higher levels of IgM and complement 3. G5 They showed normal hepatocytes and sinusoids without
on the other hand, had signfcantly higher lysozyme than eosinophilia, centrilobular necrosis, vacuolation, or
the control birds in G1 (Table 8). In addition, as com- inflammatory cell, centrilobular necrosis, vacuolation or
pared to birds in G1, birds fed 4 mL S. platensis extract/ inflammatory cell infiltration (Figure 1).
kg food (G5) showed a significant improvement in
malondialdehyde, superoxide dismutase, catalase, gluta-
thione, and total antioxidants levels as 0.30, 1.01, 0.67, Evaluation of the Meat Quality
0.59, and 0.85, respectively (Table 8). When compared
Table 9 illustrates the effect of adding S. platensis
to unsupplied chicks in G1, the birds given varying
extract at 4 doses on quail meat quality. After cooking
amounts of S. platensis extract significantly improved
the quail flesh, sensory characteristics (juiciness, tender-
their immune and antioxidant status (Table 8).
ness, scent, and taste) were assessed. The addition of S.
platensis extract significantly increased the juiciness and
Histopathological Examination tenderness properties compared to the control, whereas
the aroma and taste properties were marginally
Figure 1 shows the histological examination of hema- decreased at higher concentrations of S. platensis extract
toxylin and eosin-stained quail liver and intestine (Table 9). This may be because of the presence of
Table 8. The impact of dietary supplementation of Spirulina platensis extract on immunity and antioxidant levels of Japanese quails.

Immunity and antioxidants G1 G2 G3 G4 G5 SEM P value
Immunity
Immunoglobulin G (mg/dL) 0.75 c 1.26 a 1.03 b 1.12 ab 1.07 ab 0.066 0.0047
Immunoglobulin M (mg/dL) 0.58 b 0.89 a 1.06 a 0.87 a 1.04 a 0.065 0.0033
Complement 3 (mg/dL) 52.66 c 51.74 c 169.25 a 50.57 c 97.15 b 5.579 <0.0001
Lysozyme (U/mg) 0.25 b 0.52 a 0.50 a 0.47 a 0.56 a 0.033 0.0006
Antioxidants
Malondialdehyde (nmol/mL) 0.46 a 0.29 b 0.25 b 0.21 b 0.30 b 0.041 0.0153
Superoxide dismutase (U/mL) 0.49 b 0.98 a 0.90 a 0.83 a 1.01 a 0.055 0.0004
Catalase (ng/mL) 0.32 b 0.60 a 0.62 a 0.58 a 0.67 a 0.042 0.0013
Reduced glutathione (ng/mL) 0.34 c 0.49 b 0.39 c 0.47 b 0.59 a 0.040 0.0123
Total antioxidant (ng/mL) 0.32 c 0.38 c 0.68 b 0.55 bc 0.85 a 0.042 <0.0001
dard error of the mean value. mg/dL, milligrams per deciliter.
Figure 1. Photomicrograph of sections of quail intestine (upper panel) and liver (lower panel) stained with hematoxylin and eosin at 100£. (A
upper panel), in the intestine of control quail (birds not supplied with S. platensis extract), showing the denuded villi tips (arrow) due to desquama-
tions enterocytes into their lumina (star) with limitation of their goblet cells (100£), (B upper panel) G2 (birds fed with 1 mL S. platensis extract/
kg diet) showing a few desquamated parts in lumen (arrow) with mild goblet cells metaplasia (100£), (C upper panel) G3 (birds fed with 2 mL S.
platensis extract/kg diet) showing more healthy arranged tall separated villi (arrow) with increase intestinal crypts activation (star) (100£), (D
upper panel) G4 (birds fed with 3 mL S. platensis extract/kg diet) showing more healthy arranged tall separated villi (arrow) with increase intestinal
crypts activation (star) (100£), (E upper panel) (birds fed with 4 mL S. platensis extract/kg diet) showing marked thin villi (star) with still presence
of mild goblet cells metaplasia (arrow) (100£). (A lower panel), in the liver of control quail (birds not supplied with S. platensis extract/kg diet),
liver cell showing normal cell architecture (arrow) without any structural abnormality (star), (B lower panel) G2 (birds fed with 1 mL S. platensis
extract/kg diet) liver cell showing normal cell architecture (arrow) without any structural abnormality (star), (C lower panel) G3 (birds fed with
2 mL S. platensis extract/kg diet) showing showed normal hepatocytes and sinusoids of control quails, no eosinophilia, centrilobular necrosis, vacuo-
lation or inflammatory cell infiltration (arrow) (100£), (D lower panel) G4 (birds fed with 3 mL S. platensis extract/kg diet) showing showed normal
hepatocytes and sinusoids of control quails, no eosinophilia, centrilobular necrosis, vacuolation or inflammatory cell infiltration (arrow) (100£), (E
lower panel) (birds fed with 4 mL S. platensis extract/kg diet) showing showed normal hepatocytes and sinusoids of control quails, no eosinophilia,
centrilobular necrosis, vacuolation or inflammatory cell infiltration (arrow) (100£).
geosmin and 2-methylisoborneol (Juttner and Wasten, fed S. platensis extract in G2, G3, G4, and G5 compared
2007). On the other hand, the green color of S. platensis to G1. Additionally, in contrast to G1, the total yeast
extract decreased lightness parameters, where redness and molds count decreased significantly in G2, G3, G4,
and yellowness increased (Table 9). and G5 (Table 10). In comparison to the control group
in G1, the birds given the highest dose of S. platensis
extract showed a significant decrease in the number of
Estimation of Cecal Microbial Load E. coli and total coliform bacteria (Table 10). Further-
more, compared to birds in G1 that were not given any
As indicated in Table 10, at P<0.0001, the overall
S. platensis extract, birds given any amount of the die-
microbial count appeared to drop significantly in birds
tary supplement had significantly lower counts of
Enterococcus spp. and Salmonella spp. (Table 10).
Table 9. The impact of dietary supplementation of Spirulina pla-
tensis extract on sensory evaluation and color properties of Japa-
nese quails’ meat. Antimicrobial Activity of S. platensis Extract
Against Pathogenic Bacteria
G1 G2 G3 G4 G5 P value The antibacterial activity of different concentrations
Meat quality Sensory evaluation of S. platensis extract against pathogenic bacteria, S.
Juiciness 8.8 a 8.8 a 8.9 a 8.7 b 8.7 b 0.022 aureus, L. monocytogenes, C. jejuni, and S. typhi is
Tenderness 8.4 c 8.5 bc 8.6 b 8.8 a 8.9 a 0.032 depicted in Figure 2A.
Aroma 8.7 a 8.3 b 8.4 b 8.3 b 8.3 b 0.029
Taste 8.6 a 8.5 b 8.4 b 8.2 c 8.1 c 0.012 The inhibitory zones increased with concentration
Meat quality Color properties (P<0.05). S. aureus was the most susceptible bacterium
Lightness (L) 60.1 a 59.5 ab 59.0 b 58.9 b 58.6 c 0.022 to S. platensis extract at 640 g/mL concentration (inhi-
Redness (a) 5.1 b 5.2 b 5.3 a 5.3 a 5.2 b 0.045
Yellowness (b) 14.6 c 15.0 b 15.2 b 15.3 a 15.6 a 0.041 bition zone = 42 mm), followed by L. monocytogenes
with inhibition zone = 37 mm, while S. typhi was the
G1, control birds with basal diet without Spirulina platensis extract;
G2, birds supplied with 1 mL S. platensis extract/kg diet; G3 birds sup- most resistant bacteria with an inhibition
plied with 2 mL S. platensis extract/kg diet; G4, birds supplied with 3 mL zone = 26 mm, followed by C. jejuni with inhibition
S. platensis extract/kg diet; and G5, birds supplied with 4 mL S. platensis zone = 29 mm (Figure 2A). The minimum inhibitory
extract/kg diet. Values with same letter in a column are not significantly
(P>0.05) different according to protected least significant difference concentration that inhibits the tested bacteria, ranged
(LSD) test. from 20 to 40 mg/mL (Figure 2B).
10 ALGHAMDI ET AL.
Table 10. The impact of dietary supplementation of Spirulina platensis extract on cecal microbial community in Japanese quails.

Cecal microbial community (Log10 colony forming units/g) G1 G2 G3 G4 G5 SEM P value
Total bacterial count 7.01 a 5.40 d 6.21 b 5.74 c 6.04 b 0.079 <0.0001
Total yeasts and molds count 4.69 a 4.13 b 4.28 b 3.88 c 3.74 c 0.068 <0.0001
Escherichia coli 5.82 a 4.38 d 5.23 b 4.74 c 4.32 d 0.085 <0.0001
Total coliform 6.26 a 5.10 c 6.01 a 5.56 b 5.14 c 0.100 <0.0001
Enterococcus spp. 6.14 a 5.11 b 5.06 b 4.66 c 4.45 c 0.081 <0.0001
Salmonella spp. 4.11 a 2.20 c 2.92 b 2.19 c 2.12 c 0.091 <0.0001
Overall, the results of the birds fed different levels of DISCUSSION

dietary S. platensis extract revealed a significant
improvement in LBG, BWG, FCR, carcass traits, blood Overuse or improper administration of antimicrobial
parameters, digestive enzymes, liver and kidney func- drugs can lead to the development of drug-resistant
tions, immunological parameters, lipid profile, antioxi- microorganisms (Marouf et al., 2023). The most com-
dant profile, and gut microbial count compared to the mon cause of antimicrobial resistance is the overuse and
control birds in G1. misuse of antibiotics in humans and animals (Osei
Figure 2. Antibacterial activity of Spirulina platensis extract (SPE) against pathogenic bacteria. SA, Staphylococcus aureus; LM, Listeria
monocytogenes; CJ, Campylobacter jejuni; and ST, Salmonella typhi. Values with same letter are not significantly (P>0.05) different according to
protected least significant difference (LSD) test. IZD, inhibition zone diameter in mm; MIC, minimum inhibitory concentration.
Sekyere and Mensah, 2020). Antibiotic resistance and enhanced carcass characteristics and belly fat in hens
the spreading of related genes among populations of fed S. platensis.
aggressive pathogens are the most important issue in The total giblet (liver, heart, and gizzard) data in
combating infectious diseases (Alenazy, 2022). Gene Table 3 revealed a numerical increase when compared to
mutations were the target of antibiotics and the primary control groups; these data are consistent with that
cause of antibiotic resistance in the early days of antibi- obtained by Zahir et al. (2019). In contrast, Fathi
otic use (Saleh et al., 2023). Horizontal gene transfer, or (2018) reported that total giblet weight reduced consid-
the ability of bacteria to share genes, is an essential fac- erably when chicks were fed Spirulina supplementation.
tor of antibiotic resistance development and transmis- Furthermore, the previous data agree with Abou-Zeid et
sion in pathogenic bacteria (Alenazy, 2022). al. (2015), who found that birds fed 2 g S. platensis
Veterinarians and other veterinary professionals play extract/kg feed achieved superior means of BW, a signif-
an important role in the fight against antimicrobial resis- icant difference in carcass percentage and abdominal fat
tance by regulating and supervising the use of antimicro- percentage, and no significant difference in liver, heart,
bials in animals, providing expert advice to farmers and and gizzard weight.
animal owners on how to use antimicrobials responsibly. According to our findings, the S. platensis extract
They are also collaborating with the human healthcare increased the activity of digestive enzymes such as
sector to share information and develop antimicrobial lipase, protease, and amylase (Table 4). These findings
resistance strategies (Cheong et al., 2016). Understand- may explain why birds’ performance and production
ing the mechanisms of resistance is critical for finding have improved, as these enzymes improved feed digest-
novel methods to this challenge; thus, microalgae as a ibility and nutrient absorption. Furthermore, groups
supplement improves poultry by boosting survival feed, given S. platensis extract had reduced cecal microbial
utilization, growth rate, and carcass quality (Cheong et load than control birds in G1 (Table 10). These findings
al., 2016). are consistent with those of Alwaleed et al. (2021), who
Spirulina are blue-green algae that grow naturally in observed that adding Spirulina powder to the diet
warm freshwater lakes (Alaqil et al., 2023). Spirulina improved gut morphology, with longer villi and more
has been consumed by humans since ancient times; sci- goblet cells.
entists have recently discovered that it includes signifi- Moreover, the primary mechanisms that contribute to
cant levels of protein, vitamins, minerals, vital fatty the positive impact that phyto-additives have on the
acids, antioxidants, enzymes, amino acids, chlorophyll, digestibility of nutrients are as follows: the enhancement
carotenoids, and polysaccharides (Alaqil et al., 2023). of digestive secretion (Puvaca et al., 2013), the enhance-
The primary goal of the current study was to find out ment of intestinal lipase, trypsin, and amylase activities
if S. platensis extract could be fed to Japanese broiler (Lee et al., 2004), and the enhancement of gut morpho-
quails and how it affected their productivity, lipid pro- logical characteristics (Jamroz et al., 2003). The
file, antioxidant status, immunological response, blood increased protein digestibility seen in Spirulina-supple-
indicators, digestive enzymes, and gut microorganisms. mented feed may be due to enhanced absorption, which
Table 2 shows the effects of adding S. platensis extract improves broiler chicken development (Park et al.,
as a feed supplementation on the growth age of Japanese 2018).
quails from d 7 to to d 35. Quails were supplemented Red blood cell, hemoglobin level, and white blood cell
with S. platensis extract for 35 d; at the end of the trial, count improvements were observed in the present study
birds fed 4 mL SE/kg meal had significantly greater in groups that were given S. platensis extract (Table 5).
BW, BWG, and lower FCR than those fed a basal diet In addition, the current study examined clinical serum
in control group G1. biochemicals, the concentrations of circulating total pro-
This could be because Spirulina helps birds maintain tein, globulins, albumin/globulin ratio, and liver and
natural microbiota health, which helps them digest food kidney functions (Table 6). S. platensis extract supple-
and perform correct metabolism through vitamin and mentation generated a direct change in blood hemoglo-
mineral absorption. These findings are consistent with bin levels (Table 5) due to its high mineral content and
those of Hanafy (2022), who observed comparable propensity to affect intestinal integrity and permeability
results in broiler chickens treated with Spirulina and as suggested by Yu et al. (2020). In addition, increasing
referred to an increase in live BWG in chicks due to the amount of Spirulina powder in broiler feed at either
improved mineral and vitamin intake. Furthermore, 5 or 10 g/kg of feed resulted in an increase in the amount
Zahir et al. (2019) proposed that S. platensis might be of hemoglobin (Alwaleed et al., 2021).
used in place of antibiotics as a growth stimulant. In the present study, compared to the control group,
Table 3 shows the impact of S. platensis extract die- birds given S. platensis extract had a significantly
tary levels (1, 2, 3, and 4 mL/kg feed) on a few slaughter enhanced lipid profile (Table 7). Similarly, Abd El-Hady
parameters expressed as a proportion of carcass body and El-Ghalid (2018) found that broiler meals supple-
weight and internal organ weight (giblet, liver, heart, mented with 3 to 6% Spirulina considerably reduced
gizzard) at 35 d. Results showed that S. platensis extract total cholesterol, triglycerides, and low-density lipopro-
supplementation significantly improved some slaughter tein levels when compared to the control group. The
parameters at 35 d of age (Table 3). These findings were reduction in the serum lipid profile of broiler chickens
consistent with those of Hanafy (2022), who reported fed dietary Spirulina may be due to Spirulina
12 ALGHAMDI ET AL.
supplementation, which increases the Lactobacillus pop- fats with numerous health benefits, including lowering
ulation (Mariey et al., 2012). inflammation, improving heart health, and boosting
In the current investigation, the supplementation brain function (Park et al., 2018).
with S. platensis extract reduced total cholesterol and Upon cooking, the juiciness and tenderness of the
total triglycerides in Japanese quail (Table 7). It is well quail meat were enhanced by increasing concentrations
known that Spirulina decreases cholesterol levels in the of S. platensis extract, while its aroma and taste were
blood and liver by increasing the activity of lipoprotein significantly reduced (Table 9). Furthermore, using a
lipase and liver triglyceride lipase (Hassanein et al., high concentration of S. platensis extract reduced the
2014). Lipoprotein lipase and hepatic triglyceride lipase lightness of the meat while increasing its redness and yel-
are enzymes that breakdown cholesterol and triglycer- lowness (Table 9). Geosmin and 2-methylisoborneol are
ides, respectively. Spirulina can help lower cholesterol the main compounds that cause Spirulina to have an
levels and improve overall heart health by increasing the unpleasant taste and odor, that is, 15 and 35 ng/L,
activity of these enzymes (Hassanein et al., 2014). respectively (Juttner and Wasten, 2007). In addition, 2-
When compared to control birds in G1, our findings pentylfuran is produced by cyanobacteria (Milovanovic
demonstrated that quails given S. platensis extract had a et al., 2015), which is formed during the auto-oxidation
better antioxidant and immunological performance of linoleic acid, and its content dependes on the content
(Table 8). Biomolecules, such as nucleic acids, proteins, of linolenic acid in algal cells (Xu et al., 2017).
and enzymes, undergo denaturation when oxidative stress Additionally, when 9-hydroxy linoleate breaks down,
heightens the production of reactive oxygen species it produces conjugated diene radicals. These radicals
(ROS), as stated by Ghasemian et al. (2022). The can react with oxygen to form vinyl hydroperoxide,
decrease in serum protein may be related to the increased which then cyclizes to form 2-pentylfuran (Xu et al.,
oxidative stress caused by heat stress, which may be 2017). Furthermore, Toyomizu et al. (2001) reported
exacerbated in part by lower protein consumption and a that feeding Spirulina to birds resulted in a variable
lack of essential amino acids (Laudadio et al., 2012). (P<0.01) meat color in broiler muscles when Spirulina
The histopathological examination of the intestine was given to chicks’ diets.
and liver revealed that the intestine showed a marked The cecum is necessary for avoiding infection coloni-
improvement in the intestinal structure in the birds zation, detoxifying harmful chemicals, recycling nitro-
treated with S. platensis extract in a dose-dependent gen, and microbiological vitamin production, cleavage of
manner compared to untreated control birds. That specific carbohydrates, and absorption of additional
result explains the improvement of birds’ productivity nutrients. Our findings revealed that S. platensis extract
as the improvement of the histopathology of the intesti- significantly reduced total bacterial count, total yeasts
nal villi enhances the absorption of the different and molds count, E. coli, total coliform, Enterococcus
nutrients and is also reflected in birds’ final LBW and spp., and Salmonella spp. counts (Table 10). Our find-
FCR. In the current study, there was no significant dif- ings are consistent with those of Park et al. (2018), who
ferences among birds in the control untreated group and investigated the influence of Spirulina fortification in
the birds supplied with different concentrations of S. broiler chickens on cecal microbial communities and
platensis extract, and all groups showed normal hepato- found that supplementing broiler feed with Spirulina
cyte structures that confirm that different doses of S. extract resulted in a higher concentration of cecal Lacto-
platensis extract have no negative impact on the liver bacillus.
structure. Our results concurred with Abdulla et al. The growth of Candida albicans was inhibited by
(2023), who found that the Spirulina powder alleviates 17.6% when Spirulina was extracted in either methanol
histopathological alterations in case of induced hepatic or water. Alternatively, the extract increased Lactococ-
damage in rats. Furthermore, Morsy et al. (2019) found cus lactis development by 50% (De Mule et al., 1996).
that S. platensis extract has a safeguarding impact on The results of this study (Table 10 and Figure 2) are in
the intestines of rats against induced ulcerative colitis. agreement with those obtained by Alwaleed et al.
According to Bondar et al. (2023), polyphenols pos- (2021), who found that the addition of Spirulina powder
sess both antioxidant and antibacterial properties. Anti- to the diet resulted in an improvement in the healthy
oxidants can help prevent lipid oxidation by scavenging intestinal microbial community. Specifically, they
free radicals, neutralizing free radicals before they can noticed an increase in Lactobacillus species and a
cause lipid oxidation, and disrupting chain reactions. decrease in E. coli.
Furthermore, antioxidants can disrupt the chain events Spirulina extract has been shown by Kaushik and
that occur during lipid oxidation by decomposing perox- Chauhan (2008) to destroy or inhibit the growth of dan-
ides, which are intermediate products of lipid oxidation. gerous bacteria such as S. typhi, S. aureus, Klebsiella
Antioxidants can also decrease the amount of oxygen pneumonia, E. coli, and Pseudomonas aeruginosa. This
available for lipid oxidation by binding to metal ions is in agreement with our results as shown in Figure 2.
and other catalysts that activate lipid oxidation (Bon- According to Bhowmik et al. (2009), the addition of
dar et al., 2023). According to Park et al. (2018), adding 10 mg/mL dry Spirulina to lactic acid bacteria growth
omega-3 fatty acid-enriched additives to broiler diets media resulted in a 186% increase in the growth of Lac-
can make their thigh meat healthier and more nutri- tobacillus acidophilus, which is indicative of the microal-
tious; this is because omega-3 fatty acids are essential gae’s potential utilization as a prebiotic product.
Furthermore, Abedin and Taha (2008) found that Production, Application, Regulation, and Sustainability. E.
alkaloids and lipopolysaccharides in S. platensis extract Jacob-Lopes, M. I. Queiroz, M. M. Maroneze and L. Q. Zepka, eds.
Academic Press, London, United Kingdom.
had antibacterial action against E. coli. An in vivo Abd El-Hack, M. E., B. A. Alaidaroos, R. M. Farsi,
experiment conducted by Janczyk et al. (2009) and D. E. Abou-Kassem, M. T. El-Saadony, A. M. Saad, M. E. Shafi,
Kang et al. (2013) found that giving Chlorella to laying N. M. Albaqami, A. E. Taha, and E. A. Ashour. 2021. Impacts of
chickens increased the number of lactic acid bacteria supplementing broiler diets with biological curcumin, zinc nano-
particles and Bacillus licheniformis on growth, carcass traits,
found in the chickens’ cecums. blood indices, meat quality and cecal microbial load. Animals
Few research has been conducted in birds to investi- 11:1878.
gate the antibacterial activities of microalgae, specifi- Abd El-Hady, A. M., and O. A. H. El-Ghalid. 2018. Spirulina platen-
cally S. platensis extract. Spirulina supplementation sis algae (SPA): a novel poultry feed additive. Effect of SPA sup-
plementation in broiler chicken diets on productive performance,
would sustain the lactic acid bacteria community, lipid profile and calcium-phosphorus metabolism. VI Mediterra-
accounting for the enhanced digestibility and growth nean Poultry Summit 18−20 June 2018, Torino − Italy.
observed in the present study. Abd El-Hack, M. E., M. T. El-Saadony, A. R. Elbestawy,
N. A. El-Shall, A. M. Saad, H. M. Salem, A. M. El-Tahan,
A. F. Khafaga, A. E. Taha, S. F. AbuQamar, and
CONCLUSIONS K. A. El-Tarabily. 2022b. Necrotic enteritis in broiler chickens: dis-
ease characteristics and prevention using organic antibiotic alter-
The high concentration of volatile components in S. natives − a comprehensive review. Poult. Sci. 101:101590.
Abd El-Hack, M. E., M. T. El-Saadony, H. M. Salem,
platensis extract gave it antibacterial capabilities. A. M. El-Tahan, M. M. Soliman, G. B. Youssef, A. E. Taha,
Therefore, the dietary inclusion of a 4 mL SE/kg diet is S. M. Soliman, A. E. Ahmed, A. F. El-Kott, and
preferable to improve the productivity of Japanese K. M. Al Syaad. 2022a. Alternatives to antibiotics for organic
poultry production: types, modes of action and impacts on bird’s
quails, including LBW, BWG, FCR, carcass traits, gen- health and production. Poult. Sci. 101:101696.
eral health conditions, including lipid profile, blood pro- Abd El-Hack, M. E., H. M. Salem, A. F. Khafaga, S. M. Soliman, and
file, digestive enzymes activities, liver and kidney M. T. El-Saadony. 2022c. Impacts of polyphenols on laying hens’
functions, and disease resistance, including immunologi- productivity and egg quality: A review. J. Anim. Physiol. Anim.
Nutr. 107:928–947.
cal, antioxidant status, and meat quality. Abdulla, I. T., B. S. Al Sulivany, G. S. Ali, and
T. T. Mohammed. 2023. Amelioration of sodium arsenate-induced
stimulation of enzyme activities in the plasma and liver, and liver
ACKNOWLEDGMENTS histopathology in rat models by Spirulina (Arthrospora platensis).
Egypt. Acad. J. Biol Sci. D Histol. Histochem. 15:15–25.
This research work was funded by Institutional Fund Abedin, R. M., and H. M. Taha. 2008. Antibacterial and antifungal
Projects under grant number (IFPIP: 1233-247-1443). activity of cyanobacteria and green microalgae. Evaluation of
The authors gratefully acknowledge technical and finan- medium components by Plackett-Burman design for antimicrobial
activity of Spirulina platensis. Glob. J. Biotechnol. Biochem. 3:22–
cial support provided by the Ministry of Education and 31.
King Abdelaziz University, DSR, Jeddah, Saudi Arabia. Abou-Zeid, A. E., S. Z. El-Damarawy, Y. A. Mariey, and
Author Contributions: Conceptualization, M. A. A., M. M. El-Mansy. 2015. Effect of using Spirulina platensis and/or
F. M. R., H. K. M., S. M. A. B., H. M. S., W. A. A., K. Chlorella vulgaris algae as feed additives on productive perfor-
mance of broiler chicks. J. Anim. Poult. Prod. 6:623–634.
A. E.-T., and A. S. A., formal analysis, A.-F. S. S., N. G. Alaqil, A. A., and A. O. Abbas. 2023. The effects of dietary Spirulina
M., S. M. A., M. D. A. M., A. M. S., K. A. E.-T., and A. platensis is on physiological responses of broiler chickens exposed
S. A., investigation, M. A. A., M. D. A. M., A. M. S., K. to endotoxin stress. Animals 13:363.
A. E.-T., and A. S. A., data curation, M. A. A., F. M. Alenazy, R. 2022. Antibiotic resistance in Salmonella: targeting mul-
tidrug resistance by understanding efflux pumps, regulators and
R., H. K. M., S. M. A. B., K. A. E.-T., and A. S. A., writ- the inhibitors. J. King Saud Univ. Sci. 34:102275.
ing original draft preparation, N. G. M., S. M. A., M. D. Alwaleed, E. A., M. El-Sheekh, M. M. Abdel-Daim, and
A. M., A. M. S., K. A. E.-T., and A. S. A., writing final H. Saber. 2021. Effects of Spirulina platensis and Amphora cof-
feaeformis as dietary supplements on blood biochemical parame-
manuscript and editing, M. A. A., F. M. R., H. K. M., S. ters, intestinal microbial population, and productive performance
M. A. B., H. M. S., W. A. A., A.-F. S. S., K. A. E.-T., in broiler chickens. Environ. Sci. Pollut. Res. 28:1801–1811.
and A. S. A., visualization and methodology, M. A. A., Bhowmik, D., J. Dubey, and S. Mehra. 2009. Probiotic efficiency of
F. M. R., H. K. M., S. M. A. B., H. M. S., W. A. A., A.- Spirulina platensis-stimulating growth of lactic acid bacteria.
World J. Dairy Food. Sci. 4:160–163.
F. S. S., N. G. M., S. M. A., M. D. A. M., A. M. S., and Bondar, A., L. Horodincu, G. Solcan, and C. Solcan. 2023. Use of Spi-
A. S. A. All authors have read and agreed to the pub- rulina platensis and Curcuma longa as nutraceuticals in Poultry.
lished version of the manuscript. Agriculture 13:1553.
Bonos, E., E. Kasapidou, A. Kargopoulos, A. Karampampas,
I. Nikolakakis, E. Christaki, and P. Florou-Paneri. 2016. Spirulina
DISCLOSURES as a functional ingredient in broiler chicken diets. S. Afr. J. Anim.
Sci. 46:94–102.
Authors declare no conflict of interests. Castanon, J. I. R. 2007. History of the use of antibiotic as growth pro-
moters in European poultry feeds. Poult. Sci. 86:2466–2471.
Chaves, A. A., C. F. Martins, D. F. Carvalho, D. M. Ribeiro,
M. Lordelo, J. P. Freire, and A. M. de Almeida. 2021. A viewpoint
REFERENCES on the use of microalgae as an alternative feedstuff in the context
Abd El-Hack, M. E., A. M. E. Abdel-Moneim, A. M. Shehata, of pig and poultry feeding—a special emphasis on tropical regions.
N. M. Mesalam, H. M. Salem, M. T. El-Saadony, and Trop. Anim. Health Prod. 53:396.
K. A. El-Tarabily. 2023. Microalgae applications in poultry feed. Cheong, D. S. W., A. Kasim, A. Q. Sazili, O. M. A. R. Hishamuddin,
Pages 435−450 in Handbook of Food and Feed From Microalgae. and J. Y. Teoh. 2016. Effect of supplementing Spirulina on live
14 ALGHAMDI ET AL.
performance, carcass composition and meat quality of Japanese Kanagaraju, P., and A. V. Omprakash. 2016. Effect of Spirulina pla-
quail. Walailak J. Sci. Technol. 13:77–84. tensis algae powder supplementation as a feed additive on the
Cheong, S. H., M. Y. Kim, D. E. Sok, S. Y. Hwang, J. H. Kim, growth performance of Japanese quails. Indian Vet. J. 93:31–33.
H. R. Kim, J. H. Lee, Y. B Kim, and M. R. Kim. 2010. Spiru- Kang, H. K., H. M. Salim, N. Akter, D. W. Kim, J. H. Kim,
lina prevents atherosclerosis by reducing hypercholesterolemia H. T. Bang, M. J. Kim, J. C. Na, J. Hwangbo, H. C. Choi, and
in rabbits fed a high-cholesterol diet. J. Nutr. Sci. Vitaminol. O. S. Suh. 2013. Effect of various forms of dietary Chlorella supple-
56:34–40. mentation on growth performance, immune characteristics, and
De Mule, M. C. Z., G. Z. De Caire, and M. S. De Cano. 1996. Bioac- intestinal microflora population of broiler chickens. J. Appl. Poult.
tive substances from Spirulina platensis (Cyanobacteria). Phyton Res. 22:100–108.
58:93–96. Kaoud, H. A. 2012. Effect of Spirulina platensis as a dietary supple-
El-Saadony, M. T., A. M. Saad, T. F. Taha, A. A. Najjar, ment on broiler performance in comparison with prebiotics. Sci. J.
N. M. Zabermawi, M. M. Nader, S. F. AbuQamar, Appl. Res. 1:44–48.
K. A. El-Tarabily, and A. Salama. 2021. Selenium nanoparticles Kaushik, P., and A. Chauhan. 2008. In vitro antibacterial activity of
from Lactobacillus paracasei HM1 capable of antagonizing animal laboratory grown culture of Spirulina platensis. Indian J. Micro-
pathogenic fungi as a new source from human breast milk. Saudi J. biol. 48:348–352.
Biol. Sci. 28:6782–6794. Khan, M., J. C. Shobha, I. K. Mohan, M. U. R. Naidu, C. Sundaram,
El-Saadony, M. T., H. M. Salem, A. M. El-Tahan, S. Singh, P. Kuppusamy, and V. K. Kutala. 2005. Protective effect
T. A. Abd El-Mageed, S. M. Soliman, A. F. Khafaga, of Spirulina against doxorubicin-induced cardiotoxicity. Phyt-
A. A. Swelum, A. E. Ahmed, F. A. Alshammari, and other. Res. 19:1030–1037.
M. E. Abd El-Hack. 2022. The control of poultry salmonellosis Kharde, S. D., R. N. Shirbhate, K. B. Bahiram, and
using organic agents: an updated overview. Poult. Sci. 101:101716. S. F. Nipane. 2012. Effect of Spirulina supplementation on growth
El-Shall, N. A., S. Jiang, M. R. Farag, M. Azzam, A. A. Al-Abdullatif, performance of broilers. Indian J. Vet. Res. 21:66–69.
R. Alhotan, K. Dhama, F. U. Hassan, and M. Alagawany. 2023. Laudadio, V., L. Passantino, A. Perillo, G. Lopresti, A. Passantino,
Potential of Spirulina platensis as a feed supplement for poultry to R. U. Khan, and V. Tufarelli. 2012. Productive performance and
enhance growth performance and immune modulation. Front. histological features of intestinal mucosa of broiler chickens fed dif-
Immunol. 14:1072787. ferent dietary protein levels. Poult. Sci. 91:265–270.
El-Sheekh, M. M., S. S. AlKafaas, H. A. Rady, B. E. Abdelmoaty, Lee, K. W., H. Everts, H. J. Kappert, J. Van Der Kuilen,
H. M. Bedair, A. A. Ahmed, M. T. El-Saadony, S. F. AbuQamar, A. G. Lemmens, M. Frehner, and A. C. Beynen. 2004. Growth per-
and K. A. El-Tarabily. 2023. How synthesis of algal nanoparticles formance, intestinal viscosity, fat digestibility and plasma choles-
affects cancer therapy? − A complete review of the literature. Int. terol in broiler chickens fed a rye-containing diet without or with
J. Nanomed. 18:6601–6638. essential oil components. Int. J. Poult. Sci. 3:613–618.
Fathi, M. A. 2018. Effect of dietary supplementation of algae meal Majumder, S., A. Sigamani, T. Rahman, and
(Spirulina platensis) as growth promoter on performance of broiler M. Rahmatullah. 2020. Exploring phytochemicals as alterna-
chickens. Egypt. Poult. Sci. J. 38:375–389. tives to antimicrobials - prospects and potentials. World J.
Gao, D., J. Yu, X. Dai, Y. Tian, J. Sun, X. Xu, and X. Cai. 2023. Pharm. Pharm. Sci. 9:1802–1813.
Development and evaluation of an indirect enzyme-linked immu- Mancuso, G., S. De Gaetano, A. Midiri, S. Zummo, and
nosorbent assay based on a recombinant SifA protein to detect Sal- C. Biondo. 2023. The challenge of overcoming antibiotic resistance
monella infection in poultry. Poult. Sci. 102:102513. in carbapenem-resistant gram-negative bacteria: “Attack on
Ghasemian, S. O., M. Gholami-ahangaran, O. Pourmahdi, and Titan”. Microorganisms 11:1912.
A. Ahmadi-Dastgerdi. 2022. Dietary supplementation of protexin Mariey, Y. A., H. R. Samak, and M. A. Ibrahem. 2012. Effect of using
and artichoke extract for modulating growth performance and oxi- Spirulina platensis algae as a feed additive for poultry diets: 1-pro-
€
dative stress in broilers. Ankara Univ. Vet. Fak€ult. Dergisi 69:281– ductive and reproductive performances of local laying hens. Egypt.
288. Poult. Sci. 32:201–215.
syt_e,
Gruzauskas, R., R. Lekavicius, A. Raceviciut_e-Stupelien_e, V. Sa Marouf, S., X. Li, H. M. Salem, Z. S. Ahmed, S. M. Nader,

V. T_evelis, and G. J. Svirmickas. 2004. Visciuku˛ broileriu˛ M. Shaalan, F. H. Awad, H. Zhou, and T. Cheang. 2023. Molecular
virskinimo procesu˛ optimizavimas simbiotiniais preparatais. Vet. detection of multidrug resistant Pseudomonas aeruginosa of differ-
Irzoote. 28:51–56. ent avian sources with pathogenicity testing and in vitro evalua-
Hanafy, A. 2022. Spirulina platensis a promising growth promoter for tion of antibacterial efficacy of silver nanoparticles against
poultry industry. Asian J. Anim. Vet. Sci. 10:27–33. multidrug resistant P. aeruginosa. Poult. Sci. 102:102995.
Hassanein, H., M. M. Arafa, M. A. Abo Warda, and Milovanovic, I., A. Misan, J. Simeunovic, D. Kovac, D. Jambrec, and
A. Abd−Elall. 2014. Effect of using Spirulina platensis and Chlo- A. Mandic. 2015. Determination of volatile organic compounds in
rella vulgaris as feed additives on growing rabbit performance. selected strains of cyanobacteria. J. Chem. 2015:1–6.
Egypt. J. Rabbit Sci. 24:413–431. Morsy, M. A., S. Gupta, A. B. Nair, K. N. Venugopala, K. Greish, and
Helal, R., and M. F. Melzig. 2008. Determination of lysozyme activity M. El-Daly. 2019. Protective effect of Spirulina platensis extract
by a fluorescence technique in comparison with the classical tur- against dextran-sulfate-sodium-induced ulcerative colitis in rats.
bidity assay. Pharmazie 63:415–419. Nutrients 11:2309.
Iatrou, A. M., G. A. Papadopoulos, I. Giannenas, A. Lymberopoulos, Najafi, M. F., D. Deobagkar, and D. Deobagkar. 2005. Potential
and P. Fortomaris. 2022. Effects of dietary inclusion of Spirulina application of protease isolated from Pseudomonas aeruginosa
platensis on the reproductive performance of female Mink. Vet Sci PD100. Electronic J. Biotechnol. 8:197–203.
9:428. Osei Sekyere, J., and E. Mensah. 2020. Molecular epidemiology and
Jafari, S. M. A., M. Rabbani, M. Emtyazjoo, and F. Piryaei. 2014. mechanisms of antibiotic resistance in Enterococcus spp., Staphy-
Effect of dietary Spirulina platensis on fatty acid composition of lococcus spp., and Streptococcus spp. in Africa: a systematic
rainbow trout (Oncorhynchus mykiss) fillet. Aquacult. Int. review from a one health perspective. Ann. N. Y. Acad. Sci.
22:1307–1315. 1465:29–58.
Jamroz, D., J. Orda, C. Kamel, A. Wiliczkiewicz, T. Wertelecki, Park, J. H., S. I. Lee, and I. H. Kim. 2018. Effect of dietary Spirulina
and J. Skorupi nska. 2003. The influence of phytogenic extracts (Arthrospira) platensis on the growth performance, antioxidant
on performance, nutrient digestibility, carcass characteristics, enzyme activity, nutrient digestibility, cecal microflora, excreta
and gut microbial status in broiler chickens. J. Anim. Feed. noxious gas emission, and breast meat quality of broiler chickens.
Sci. 12:583–596. Poult. Sci. 97:2451–2459.
Janczyk, P., B. Halle, and W. B. Souffrant. 2009. Microbial community Puvaca, N., V. Stanacev, D. Glamocic, J. Levic, L. Peric, and
composition of the crop and ceca contents of laying hens fed diets D. Milic. 2013. Beneficial effects of phytoadditives in broiler nutri-
supplemented with Chlorella vulgaris. Poult. Sci. 88:2324–2332. tion. Worlds Poult. Sci. J. 69:27–34.
Juttner, F., and S. B. Watson. 2007. Biochemical and ecological con- Qureshi, M. A., J. D. Garlich, and M. T. Kidd. 1996. Dietary Spirulina
trol of geosmin and 2-methylisoborneol in source waters. Appl. platensis enhances humoral and cell-mediated immune functions in
Environ. Microbiol. 73:4395–4406. chickens. Immunopharmacol. Immunotoxicol. 18(3):465–476.
Saad, A. M., A. S. Mohamed, and M. F. Ramadan. 2021a. Storage Shi, Z., M. J. Rothrock Jr., and S. C. Ricke. 2019. Applications of
and heat processing affect flavors of cucumber juice enriched with microbiome analyses in alternative poultry broiler production sys-
plant extracts. Int. J. Veg. Sci. 27:277–287. tems. Front. Vet. Sci. 6:157.
Saad, A. M., M. Z. Sitohy, A. I. Ahmed, N. A. Rabie, S. A. Amin, Suvarna, S. K., C. Layton, and J. D. Bancroft. 2018. Pages 584 in
S. M. Aboelenin, M. M. Soliman, and M. T. El-Saadony. 2021b. Bancroft’s Theory and Practice of Histological Techniques. 8th ed.
Biochemical and functional characterization of kidney bean pro- Elsevier, Amsterdam, the Netherlands.
tein alcalase-hydrolysates and their preservative action on stored atkiewicz,
Swi ˛ S., A. Arczewska-W»osek, and D. J ozefiak. 2015. Appli-
chicken meat. Molecules 26:4690. cation of microalgae biomass in poultry nutrition. Worlds Poult.
Saad, A. M., M. Z. Sitohy, M. I. Sultan-Alolama, K. A. El-Tarabily, Sci. J. 71:663–672.
and M. T. El-Saadony. 2022. Green nanotechnology for controlling Toyomizu, M., K. Sato, H. Taroda, T. Kato, and Y. Akiba. 2001.
bacterial load and heavy metal accumulation in Nile tilapia fish Effects of dietary Spirulina on meat color in muscle of broiler chick-
using biological selenium nanoparticles biosynthesized by Bacillus ens. Br. Poult. Sci. 42:197–202.
subtilis AS12. Front. Microbiol. 13:1015613. Xu, L., X. Yu, M. Li, J. Chen, and X. Wang. 2017. Monitoring oxida-
Saadaoui, I., R. Rasheed, A. Aguilar, M. Cherif, H. Al Jabri, tive stability and changes in key volatile compounds in edible oils
S. Sayadi, and S. R. Manning. 2021. Microalgal-based feed: promis- during ambient storage through HS-SPME/GC−MS. Int. J. Food
ing alternative feedstocks for livestock and poultry production. J. Prop. 20:S2926–S2938.
Anim. Sci. Biotechnol. 12:76. Yu, T., Y. Wang, X. Chen, W. Xiong, Y. Tang, and L. Lin. 2020. Spi-
Saleh, A. A., A. Hafez, K. Amber, A. Y. Abdelhady, H. M. Salem, rulina platensis alleviates chronic inflammation with modulation
M. Fathy, M. A. Kamal, M. Alagawany, and of gut microbiota and intestinal permeability in rats fed a high-fat
M. H. Alzawqari. 2023. Drug-independent control strategy of clos- diet. J. Cell. Mol. Med. 24:8603–8613.
tridial infection in broiler chickens using anti-toxin environmen- Zahir, U., B. AnwarulHaque, B. Maksuda, and U. M. Mahfuj. 2019.
tally friendly multienzymes. Sci. Rep. 13:5614. Effect of dietary supplement of algae (Spirulina platensis) as an
Salem, H. M., A. M. Saad, S. M. Soliman, S. Selim, W. F. Mosa, alternative to antibiotics on growth performance and health status
A. E. Ahmed, S. K. Al Jaouni, M. S. Almuhayawi, of broiler chickens. J. Poult. Sci. 18:576–584.
M. E. Abd El-Hack, K. A. El-Tarabily, and Zarrouk, C. 1966. Contribution a l’etuded’unecyanobacterie: influ-
M. T. El-Saadony. 2023. Ameliorative avian gut environment ence de divers facteurs physiques et chimiques sur la croissance et
and bird productivity through the application of safe antibiot- la photosynthese de Spirulina maxima (Setchell et Gardner) Gei-
ics alternatives: a comprehensive review. Poult. Sci. tler. University of Paris, Paris, France PhD Thesis.
102:102840. Zhou, L., K. Abouelezz, M. A. Momenah, M. A. Bajaber, N. Baazaoui,
Samad, A. 2022. Antibiotics resistance in poultry and its solution. T. F. Taha, A. E. Awad, S. A. Alamoudi, E. A. Beyari,
Devot. J. Commun. Serv. 3:999–1020. Y. F. Alanazi, and A. Allohibi. 2023. Dietary Paenibacillus poly-
Samarth, V. R., D. G. Jagtap, N. P. Dakshinkar, M. V. Nimbulkar, myxa AM20 as a new probiotic: improving effects on IR broiler
and M. D. Kothekar. 2002. Effect of ashwagandha root powder growth performance, hepatosomatic index, thyroid hormones, lipid
(Withania somnifera) on performance of broilers. Indian Vet. J. profile, immune response, antioxidant parameters, and caecal
79:733–734. microorganisms. Poult. Sci. 103,:103239.

The Potential of Spirulina Platensis To Substitute Antibiotics in Japanese Quail Diets - Impacts On Growth, Carcass Traits, Antioxidant Status, Blood Biochemical Parameters, and Cecal Microorganisms

Uploaded by

Document Informationclick to expand document information

Copyright:

Available Formats

The Potential of Spirulina Platensis To Substitute Antibiotics in Japanese Quail Diets - Impacts On Growth, Carcass Traits, Antioxidant Status, Blood Biochemical Parameters, and Cecal Microorganisms

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

The Potential of Spirulina Platensis To Substitute Antibiotics in Japanese Quail Diets - Impacts On Growth, Carcass Traits, Antioxidant Status, Blood Biochemical Parameters, and Cecal Microorganisms

Uploaded by

Copyright:

Available Formats

The potential of Spirulina platensis to substitute antibiotics in Japanese quail

diets: impacts on growth, carcass traits, antioxidant status, blood biochemical

INTRODUCTION microalgae to boost nutritional value, especially that of

Table 1. Volatile compounds proﬁle in Spirulina platensis extract.

Spirulina platensis extract level (mL/kg diet)

Evaluation of Blood Parameters

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Spirulina platensis extract level (mL/kg diet)

Overall, the results of the birds fed different levels of DISCUSSION

You might also like