Dietary supplementation of Yucca schidigera extract enhances productive

and reproductive performances, blood profile, immune function, and

antioxidant status in laying Japanese quails exposed to lead in the diet

M. Alagawany,∗,1 M. E. Abd El-Hack,∗ M. R. Farag,† S. S. Elnesr,‡ M. S. El-Kholy,∗

I. M. Saadeldin,§,# and A. A. Swelum§,,1
∗
Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44519, Egypt; † Forensic Medicine and
Toxicology Department, Veterinary Medicine Faculty, Zagazig University, Zagazig 44519, Egypt; ‡ Department of
Poultry Production, Faculty of Agriculture, Fayoum University, 63514 Fayoum, Egypt; § Department of Animal
Production, College of Food and Agriculture Sciences, King Saud University, P.O. Box 2460, Riyadh 11451,
Saudi Arabia; # Department of Physiology, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44519,
Egypt; and  Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44519,
Egypt

ABSTRACT The present study investigated the toxic
impacts of lead (LD) on the productive and repro-
ductive performances of Japanese quails and the role
of Yucca schidigera extract (YSE) in reducing these
impacts. A total of 360 mature Japanese quails (at
2 months of age) were used and the experiment was
lasted for 8 wk. The birds were divided into 6 equal
groups as follows: control (basal diet), basal diet +
100 mg LD/kg diet, basal diet + YSE (100 mg/kg
diet), basal diet + YSE (200 mg/kg diet), basal diet
+ LD (100 mg/kg diet) + YSE (100 mg/kg diet), and
basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg
diet). LD resulted in a significant decrease in feed in-
take (FI), feed conversion ratio (FCR), and egg pro-
duction of birds compared with the control group. Sup-
plementation of YSE (100 or 200) to LD containing
diet could significantly improve the quail performance
parameters to be comparable with the control val-
ues. Fertility and hatchability % were decreased by
LD, whereas YSE at both levels (100 or 200) sepa-
rately or in combination with LD showed fertility and
Key words: Yucca, lead, performance, blood, quail
hatchability percentages comparable to that of control.
Triglycerides, cholesterol, and LDL contents in LD plus
YSE100 or LD plus YSE200 groups were significantly
decreased than LD alone group. LD significantly de-
creased superoxide dismutase and catalase activities in
the serum with no effect on reduced glutathione con-
tent. Co-exposure to YSE100 or YSE200 with LD sig-
nificantly increased the catalase activity and numeri-
cally increased the superoxide dismutase activity than
LD alone. YSE100 or YSE200 decreased malondialde-
hyde contents than LD alone group. LD plus YSE100
or YSE200 groups exhibited significant improvements
in the level of immunoglobulins. Co-exposure to YSE
with LD significantly decreased the LD residues in
egg than the LD group. The obtained results showed
that YSE exhibited a potential modulatory role against
the LD-induced inhibitory effects on the productive
and reproductive performances of Japanese quails
and YSE at 200 mg/kg diet was more effective
than 100 mg/kg diet in reversing the LD-induced
alterations.
2018 Poultry Science 97:3126–3137
http://dx.doi.org/10.3382/ps/pey186

INTRODUCTION environmental pollutants particularly in industrial ar-

The environmental contamination has been increased
during the last decades resulting in potential hazards
on all biological systems including birds which expe-
rienced a great reduction in their population (Gaston
et al., 2003). Lead (LD) is one of the most widespread

C2018 Poultry Science Association Inc.
Received February 27, 2018.
Accepted April 13, 2018.
1
Corresponding authors: mmalagwany@zu.edu.eg; aswelum@ksu.
edu.sa
3126
eas (Klaminder et al., 2006). Birds are exposed to LD
from various sources such as the general environment,
industrial pollution and contamination of water, soil
and food by agricultural processing (Berglund et al.,
2010). Oral administration of LD results in its absorp-
tion at a small extent but its elimination rate is slow; as
a result, exposure to small quantities for long periods
could lead to accumulation of harmful levels (Madhavi
et al., 2007). When LD enters in to the blood stream,
it is absorbed and some of it is bound to erythrocytes
and some is conjugated in the liver then pass to kidney.
After that, a small amount is excreted in urine and the
 YUCCA MODULATES LEAD TOXICITY IN QUAILS
remaining stay in plasma to be distributed in the body
and accumulates in various organs and impaired their
function. Ingestion of LD has been reported to induce
poor performance, weight loss, decreased production,
and even death of animals (Hoshiari and Pourkhabbaz,
2012). Lead has been reported to induce some clinical
manifestations in birds such as atrophy of breast mus-
cle and loss of visceral and subcutaneous fat (Beyer et
al., 1998). It also resulted in weight loss, poor body
conditions, and even starvation of birds as subsequent
conditions following muscular paralysis of digestive sys-
tem including esophagus, proventriculus, gizzard, and
the intestines (Pattee and Pain, 2003).
Lead has been accounted for mortality and morbidity
in birds from different species in some previous reports
(Mateo et al., 2003; Pain et al., 2015). Lead also ex-
hibited some immunotoxic effects as described by Oh-
sawa (2009). Additionally, birds can maintain metals in
high levels in different tissues like kidney, liver, meat,
and eggs (Farahani, et al., 2015; Humayun et al., 2015).
Such residues can be transmitted to human and other
organisms through food chain resulting in a wide range
of biochemical and physiological abnormalities in car-
diovascular system, nervous system, reproductive or-
gans, kidneys, and red blood cells (Elayat and Bakheetf,
2010).
Lead poisoning has been also reported to induce
oxidative stress and enhance the production of reac-
tive oxygen species (ROS) as major mechanisms of its
toxic action and thereby can cause cell structure dam-
age, lipid peroxidation, and DNA and protein oxida-
tion (Kasperczyk et al., 2012). The potential effect of
LD in induction of oxidative stress suggests that some
medicinal plants and herbs with antioxidant and pos-
sible chelating activities may be helpful in modulating
the LD-induced toxicity (Patrick, 2006).
Yucca schidigera is a plant belongs to the family
“Agavaceae,” native to Mexico and the South-Western
United States. Yucca is a widespread medicinal plant
and is considered as natural (100%) additive (Bal-
azi et al., 2013). It has many beneficial effects like
growth promoter, hypocholesterolemic, hypoglycemic,
anti-inflammatory, antioxidant, anticarcinogenic, and
immunostimulatory (Alagawany et al., 2016a). Yucca
is a commercial source of saponins, resveratrol, vari-
ous enzymes, and antioxidants (Chrenková et al., 2012;
Alagawany et al., 2016b; Farag et al., 2016). Steroid
saponins of yucca products are approved by GRAS
(Generally Recognized as Safe) given by FDA (Food
and drug administration) that allows their human di-
etary use (Tenon et al., 2017). It is also used in the
manufacture of cosmetics, beverages, and as dietary
supplement for poultry and animal. In addition, yucca
can conserve ammonia and decrease its content in the
poultry houses and air and decrease blood urea concen-
tration (Piacente et al., 2005) and has a great absorp-
tion capacity for harmful volatile compounds, such as
ammonia and hydrogen sulfide (Vlckova et al., 2017).
Therefore, the main objective of the present study was
3127
to investigate the toxic effects of LD on productive and
reproductive performances, blood biochemical parame-
ters, and the oxidative status of laying Japanese quails
and to determine the egg quality criteria and residual
concentrations of LD in the produced eggs. Addition-
ally, this study would clarify the potential modulatory
role of Yucca schidigera extract (YSE) against these ef-
fects.
MATERIALS AND METHODS
Birds and Diets
The present study was carried out at Poultry Re-
search Farm, Faculty of Agriculture, Zagazig Univer-
sity, Egypt. All experimental procedures were carried
out according to the Local Experimental Animal Care
Committee and approved by the ethics of the institu-
tional committee of Zagazig University, Zagazig, Egypt.
A total number of 360 mature Japanese quails
(Coturnix coturnix japonica) at 2 mo of age with initial
body weight 240.50 ± 2.00 g were used in a complete
randomized design experiment with 6 treatments of 60
birds each. Each group was subdivided into 4 replicates
with 15 birds. The experiment lasted for 8 wk. Birds
were fed the basal diet with or without supplemental
LD or YSE that formulated to meet laying quail re-
quirements according to NRC (1994). The treatments
were as follows: 1) control basal diet, 2) basal diet +
100 mg LD/kg diet, 3) basal diet + YSE (100 mg/kg
diet), 4) basal diet + YSE (200 mg/kg diet), 5) basal
diet + LD (100 mg/kg diet) + YSE (100 mg/kg
diet), and 6) basal diet + LD (100 mg/kg diet) +
YSE (200 mg/kg diet). The ingredients and chemical
composition of the basal diet are presented in Table 1.
Birds were housed in conventional type cage (50 × 30
× 50 cm3 ; 1,500 cm2 of floor space) with feed and fresh
water provided ad libitum. Birds also were maintained
on a 17 h light: 7 h dark cycle throughout the trial. All
birds were kept under the same managerial, hygienic,
and environmental conditions.
Tested Chemicals
Lead in the form of LD acetate (99.6% purity) was
purchased from El-Gomhoria Chemical Co., Egypt.
Yucca schidigera extract was purchased from Free Trade
Egypt Company (El-Behera, Egypt). All other chemi-
cals were purchased from Sigma (St. Louis, MO). All
other reagents used were of analytical grade.
Data Collection and Calculation
Feed intake (FI) (g) was recorded daily, whereas feed
conversion ratio (FCR) was calculated as the egg mass
value divided by the amount of consumed feed. Egg
numbers and weights were recorded daily to compute
the egg mass.
3128
Table 1. Composition and calculated analysis of the basal diets.
Item Basal diet (%)
Ingredients
Corn
Soybean meal (44%)
Corn gluten meal (60%)
Di-calcium phosphate
Limestone
Vit. & Min. premix1
NaCl
Dl- Methionine
L-Lysine Hcl
Cotton seed oil
Total 100
Calculated analysis (%)2
Crude protein
ME (kcal/kg) 2922
Calcium
Non-phytate phosphorus
Lysine
Methionine + Cystine
1
Layer Vit. & Min. premix: Each 2.5 kg of vitamins and minerals
premix (commercial source pfiezer Co.): consist of Vit. A 12 MIU, VIT
E 15 KIU, Vit. D3 4 MIU, Vit. B1 1 g, Vit B2 8 g, Vit B6 2 g, Vit B12
10 mg, pantothenic acid 10.87 g, niacin30 g, folic acid 1 g, biotin 150 mg,
copper 5 g, iron 15 g, manganese 70 g, iodine 0.5 g, selenium 0.15 g, zinc
60 g, and antioxidant 10 g.
2
Calculated according to NRC (1994).
Fertility and Hatchability Percentages
Twenty eggs from each replicate were collected and
incubated at the end of each month. After hatching,
chicks were counted and non-hatched eggs were exam-
ined to calculate the fertility and hatchability percent-
ages. Fertility and hatchability percentages were calcu-
lated as follows: fertility percentage = (number of fertile
eggs/total eggs set) × 100; hatchability percentage from
fertile eggs = (number of hatched chicks/total number
of fertile eggs) × 100; hatchability percentage from the
total egg set = (number of hatched chicks/total eggs
set) × 100.
Egg Quality Criteria
Egg quality criteria were measured monthly using 3
eggs from each replicate. Interior and exterior parame-
ters of egg quality (percentages of yolk, albumen, shell,
and egg shape index, yolk index Haugh units, and shell
thickness) were determined according to Romanoff and
Romanoff (1949).
Blood Sampling and Laboratory Analyses
Blood samples were randomly collected from 6 birds
per treatment from the wing vein into sterilized tubes.
The samples were allowed to coagulate for 30 min at
room temperature and then centrifuged for 15 min
at 3,500 rpm for serum separation; the serum sam-
ples were stored at –20◦ C until analysis. Total pro-
tein, albumin, globulin, total cholesterol, triglycerides,
low-density lipoprotein (LDL) cholesterol, high-density
lipoprotein (HDL) cholesterol, alanine amino trans-
ALAGAWANY ET AL.
ferase (ALT), and aspartate aminotransferase (AST)
were determined spectrophotometrically using commer-
cial diagnostic kits provided from Biodiagnostic Co.
(Giza, Egypt). Immunoglobulins (IgG and IgM) were
60.05
25.00
determined according to Akiba et al. (1982).
5.70
3.30
3.80 Antioxidant Assays
0.25
0.20 Superoxide dismutase (SOD) and catalase (CAT)
0.05 activities as well as reduced glutathione (GSH) and
0.15
1.50
malondialdehyde (MDA) concentrations were deter-
mined in serum by spectrophotometric methods (Hi-
tachi spectrophotometer, Japan) using commercial
20.03
biodiagnostic kits provided from BioMérieux (Marcy
2.51 l’etoile, France) according to the manufacturer’s in-
0.55 structions.
1.08
0.77
Determination of LD Residues
Eggs were transferred to the laboratory in plastic
bags and stored at cool and dark place. Then, each
egg was washed by distilled water and soap and cut at
the air cell end by dissecting scissors and pointed for-
ceps. The content of each sample was placed in a clean
glass jar. The samples then were dried at 75◦ C to get
constant weight (Zaki, 1998).
Then, the egg samples were digested by acid diges-
tion method of Mahaffey et al. (1981),where 1 g of each
sample was putted into a clean screw capped glass bot-
tle and digested with a 4 mL of (nitric/perchloric acid,
1:1) as a digestion solution. Initial digestion was per-
formed at room temperature for 24 h, and then heated
for 2 h at110◦ C. Then the samples were left to cool and
then followed by addition of deionized water and the
solution was left for 1 h in water bath to expel nitrous
gases. The digests were filtered and diluted to 25 mL
deionized water (Julshman, 1983). The obtained solu-
tion was then analyzed using flame atomic absorption
spectrophotometer.
Statistical Analysis
The data were statistically analyzed using general lin-
ear models procedure adapted by SPSS for user’s guide
with one-way ANOVA. The differences among treat-
ments were determined using the post hoc Newman–
Keuls test (P < 0.05).
RESULTS
Productive Performance of Japanese Quails
Table 2 depicts the effects of LD along with the
role of YSE on productive performance of quails dur-
ing the experimental period. Supplementation of LD
to quails diet showed a significant decrease in the FI,
FCR, and egg production of birds compared with the
control group. On the other hand, there were no sig-
nificant changes in the egg weight or egg mass among
 YUCCA MODULATES LEAD TOXICITY IN QUAILS 3129
Table 2. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or
200 mg/kg diet) on productive parameters of Japanese quail.

Productive parameters
Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg)

Control 13.78 ± 0.79 83.52 ± 8.49

a,b
692.09 ± 102.17 31.54 ± 1.30
a,b
2.98b ± 0.31
Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11
YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30
YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39
LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25
LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15
P-value1 0.060 0.010 0.200 0.031 0.057

Different superscripts within 1 column are significantly different (P < 0.05).

1
Overall treatment P-value.

Table 3. Effects of separate and concurrent exposure to lead Hatchability (%) from the fertile eggs was found
(LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 to be significantly decreased in the LD group com-
or 200 mg/kg diet) on reproductive parameters of Japanese quail.
pared to control, whereas the YSE100 group showed
Reproductive parameters the highest percentage among all other experimental
groups. On the other hand, supplementation of YSE
Hatchability
(%) (from the Hatchability (%)
(100 or 200 mg/kg diet) to LD diet could restore
total set of (from the fertile the hatchability (%) from the fertile eggs to that of
Items Fertility (%) eggs) eggs) control.
Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93
Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92
YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 Egg Quality Criteria
YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89
LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 Supplementation of quail’s diet by LD, YSE (100 or
LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 200) separately or in combination did not alter the egg
P-value1 0.030 0.003 0.005
composition (shell, yolk, and albumen), exterior or in-
Different superscripts within 1 column are significantly different terior egg quality parameters than the control group as
(P < 0.05).
1
Overall treatment P-value.
shown in Table 4.

the different experimental groups. Supplementation of Liver Function Markers

YSE (100 or 200) to LD containing diet could signifi-
cantly improve the quail performance parameters (FI,
FCR, and egg production) and restored them to the
control values. YSE200 groups showed the highest FI
level and egg production percentage compared to all
other groups.
Reproductive Performance of Japanese
Quails
Results in Table 3 indicate that supplementation of
diets with LD resulted in a significant decrease in the
fertility percentage compared to the control group. On
the other hand, YSE at both levels (100 or 200) sepa-
rately or in combination with LD showed fertility per-
centages comparable to that of control.
Results of hatchability (%) from the total set of eggs
revealed no significant changes between control, YSE
100, or YSE200 groups. Whereas, this percentage was
significantly decreased in the LD group compared to
the control group. On the other hand, supplementation
of YSE (100 mg/kg diet) to LD containing diet could
not improve the reduced hatchability of quails, whereas
addition of YSE (200 mg) to LD diet could restore the
hatchability percentage of birds to control values.
Liver function markers are given in Table 5. Total
protein, albumin, and globulin levels were found to be
decreased in serum of LD-exposed group only compared
to control. The higher levels of total protein and albu-
min were obtained for birds of YSE200 group followed
by the YSE100 group compared to the control group.
Co-exposure to YSE 100 or 200 with LD was found to
significantly increase the levels of total protein, albu-
min, and globulin.
In response to LD exposure, the values of AST and
ALT were increased significantly compared to the con-
trol group. On the other hand, lower levels of AST
and ALT were observed for YSE100 and YSE200.
AST and ALT levels in LD plus YSE100 or LD plus
YSE200 groups were significantly decreased than LD
alone group and a better reduction was observed in
LD plus YSE 200 group; however, both the levels did
not return the AST and ALT levels to the control
values.
Effects on Lipid Profile
Exposure of quails to LD in their diet significantly in-
creased the triglycerides, cholesterol, and LDL whereas
3130 ALAGAWANY ET AL.

Table 4. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or
200 mg/kg diet) on egg quality criteria in Japanese quail.

Egg quality criteria

Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score

Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10
Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97
YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14
YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46
LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88
LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30
P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392
1
Overall treatment P-value.

Table 5. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or
200 mg/kg diet) on liver functions in serum of Japanese quail.

Liver functions1
Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL)

Control 4.75 ± 0.05

b,c
1.81 ± 0.01
c
2.94 ± 0.05
b
56.31 ± 1.26
d
26.59d ± 0.40
Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37
YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03
YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76
LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01
LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26
P-value2 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001

Different superscripts within 1 column are significantly different (P < 0.05).

1
AST: aspartate aminotransferase, ALT: alanine aminotransferase
2
Overall treatment P-value.

Table 6. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera
extract (YSE, 100 or 200 mg/kg diet) on lipid profile in serum of Japanese quail.

Lipid profile (mg/dL)

Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL)

Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04

Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56
YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07
YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40
LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36
LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68
P-value1 < 0.001 < 0.001 < 0.001 < 0.001

Different superscripts within 1 column are significantly different (P < 0.05).

1
Overall treatment P-value.

significantly decreased HDL values compared to control Effects on Antioxidant Status

and other treatment groups. On the other hand, con-
tradicting results were obtained for the YSE200 group.
Triglycerides, cholesterol, and LDL contents in LD plus
YSE100 or LD plus YSE200 groups were significantly
decreased than LD alone group and a better effect was
observed in LD plus YSE 200 group where it could
restore the triglyceride level to normal and decreased
the cholesterol level than the LD+YSE100 group how-
ever still higher than control. Co-exposure to YSE 100
or 200 with LD was found to significantly increase
the levels of HDL than control and YSE200 was more
effective than YSE100. On the other hand, YSE100
alone did not alter the HDL value compared to control
(Table 6).
Table 7 shows the effects of LD and YSE on antiox-
idant system of quails. The LD treatment significantly
decreased both the SOD and CAT enzyme activities
in the serum of treated quails compared to the control
group. YSE100 did not significantly change the antiox-
idant activities than those of control, whereas YSE200
significantly enhanced the SOD and CAT activities to
be better than the control itself.
GSH content was not significantly changed in all
groups compared to control except YSE200 that was
higher than control.
Co-exposure to YSE100 or YSE200 with LD was
found to significantly increase the CAT activity than
 YUCCA MODULATES LEAD TOXICITY IN QUAILS 3131
Table 7. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or
200 mg/kg diet) on antioxidant and immunity in serum of Japanese quail.

Antioxidant and immunity1

Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μ mol/mL) IgG(mg/dL) IgM(mg/dL)

Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43
Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43
YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52
YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25
LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72
LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40
P-value2 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001

Different superscripts within 1 column are significantly different (P < 0.05).

1
SOD: superoxide dismutase, CAT: catalase, GSH: reduced glutathione, MDA: malondialdehyde, IgG: immunoglobulin G, IgM:
immunoglobulin M.
2
Overall treatment P-value.

LD alone to be comparable with control and numeri- DISCUSSION

cally increase the SOD activity however still under con-
trol values.
The lipid peroxidation, as evidenced by the forma-
tion of MDA, was significantly increased in LD-treated
group compared to the control group. MDA contents in
LD plus YSE100 or YSE200 groups were significantly
decreased than LD alone group, and a better effect was
observed in LD plus YSE 200 group. Meanwhile, MDA
level in the YSE200 group was significantly lower than
control however YES100 was comparable to both con-
trol and YSE200 groups.
Effects on Immunoglobulins
Results in Table 7 showed that the highest values
of immunoglobulins (IgG and IgM) were obtained by
birds fed diet supplemented with 200 mg YSE/kg fol-
lowed by those received 100 mg YSE/kg diet, whereas
the lowest values of IgG and IgM were obtained in re-
sponse to LD exposure. On the other hand, LD plus
YSE100 or LD plusYSE200 groups exhibited signif-
icant improvements in the level of immunoglobulins
compared to the LD group and YSE200 showed better
effects.
LD Residues
Analysis of eggs for detection of LD residues at the
end of the experiment is represented in Figure 1, which
revealed that the highest concentrations of accumu-
lated LD were detected in eggs of LD-exposed group
(0.932 ± 0.04). On the other hand, there were no sig-
nificant changes in the residue level of LD among con-
trol, YSE100, and YSE200 groups (0.13 ± 0.04, 0.09 ±
0.03, 0.04 ± 0.02), respectively. Co-exposure to YSE100
or YSE200 with LD was found to significantly de-
crease the LD residues in egg 0.797 ± 0.04, 0.700 ±
0.02 respectively than the LD group. The YSE200 was
better than YSE100 however still higher than control
level.
The aim of the current poultry production is to
achieve the highest growth rates, FCRs, and produc-
tion percentages to cover the widely increasing de-
mand of animal proteins particularly in developing
countries. The intensive breeding and farming increased
the sensitivity of birds to external stressors from their
surrounding environment resulting in acute stress re-
sponses, reduced productive and reproductive perfor-
mances, health problems, increased susceptibility to
infectious diseases, and low-quality poultry products
(Shahid ul Islam et al., 2014). Therefore, it is of impor-
tance to explore the stress responses to environmental
contaminants on the productive and reproductive per-
formance of birds and try to find effective methods to
decrease these responses. Japanese quail could be used
as a model to study the effects of environmental con-
tamination as they are similar to wild birds, ready avail-
able, and information concerning their normal physiol-
ogy is solid (Franson and Pain, 2011).
The present study indicated that LD supplementa-
tion to diets of quails showed a significant decrease in
FI, FCR, and egg production; however, it did not influ-
ence the other performance parameters including egg
weight and egg mass compared to control. Exposure of
quails to LD in their diet decreased the hatchability of
total eggs set, hatchability of fertile eggs set, and the
percentage of fertile eggs compared to control. On the
other hand, LD did not alter the egg quality criteria
of exposed quails. High dietary LD has been reported
to inhibit the growth performance parameters in quails
(Humayun et al., 2015; Farag et al., 2018). Similarly,
LD decreased the body weight and egg production in
adult quail hens (Stone and Soares, 1976). On the same
context, Butkauskas and Sruoga (2004) stated that LD
could increase the number of unfertile eggs of quail up
to 30% relative to control. Salisbury, et al. (1958) re-
ported a cessation of egg production in adult chicken
hens intoxicated with LD.
The inhibitory effect of dietary LD exposure on re-
productive performance of female quails was reported
by Edens and Garlich (1983), who demonstrated that
3132
Figure 1. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca schidigera extract (YSE, 100 or 200 mg/kg
diet) on accumulation of lead residues (μ g/g wet weight) in eggs of treated Japanese quails compared to the control group.
dietary LD significantly depressed the total plasma cal-
cium reflecting the inability of intoxicated quails to
mobilize adequate amount of plasma calcium. More-
over, LD exposure decreased the weight and function
of ovary in exposed quails. Therefore, it was suggested
that ovary could be involved in the regulation of egg
production than calcium. Additionally, LD has been
reported to induce neurotoxicity in quails inducing im-
pairment of the neurochemical control on reproductive
hormones regulation (Edens, 1985).
In our study, supplementation of YSE to bird’s diet
concurrently with LD resulted in significant improve-
ments in the altered productive performance parame-
ters of quails including FI, FCR, egg production, fer-
tility, and hatchability to levels that are comparable to
those of control. Dietary supplementation of Y. schidi-
gera has been reported to induce significant impacts
on layer performance by increasing the egg production
and final body weight (Gurbuz et al., 2016). Similarly,
Cheek (1998) reported that feeding poultry on yucca
could improve their growth and productivity. These
positive effects of yucca could be returned to the pres-
ence of steroidal saponins as a main component and
other surface active components that could promote
the utilization and absorption of nutrients from gas-
trointestinal tract by improving its epithelial lining of
the cell membrane and decreasing the surface tension
(Goetsch and Owens, 1985).
Fertility and hatchability are important parameters
in studying the reproductive performance; they are af-
fected by environment, insufficient nutrients, and ge-
netic involvement (Ayasan, 2013). Therefore, to ob-
tain the highest fertility and hatchability percentages
of quails, optimum conditions should be provided be-
fore and after hatching (Ggüçlü, 2011). In the present
study, yucca at high level (200 mg/kg body weight) was
found to improve fertility and hatchability percentages
ALAGAWANY ET AL.
in the presence of LD. This improvement could be ex-
plained by the suggestions of El Anwer et al. (2009),
who returned the increased hatchability and fertility to
2 main assumptions; the first assumption is the ability
of yucca to reduce ammonia concentration in the sur-
rounding atmosphere of eggs that could help in adjust-
ing the egg pH. The reducing effect of yucca on blood
urea has been previously reported in broilers (Balog
et al., 1994) that could be mainly due to saponin, stil-
benes, and carbohydrates in yucca. These components
have been reported to have modulatory effects on renal
functions and could increase the clearance of urea and
lower blood concentrations of ammonia and urea (Duffy
et al., 2001). YES has could inhibit urease enzyme in
vivo and in vitro (Asplund 1991; Balog et al., 1994).
Biochemical findings of the present study revealed
that total protein level was found to be decreased
in serum of LD-exposed group compared to control.
These results are in accordance with those of Humayun
et al. (2015) who studied hematobiochemical changes
induced by LD poisoning in quails. The decreased pro-
tein level could be returned to increasing protein utiliza-
tion to obtain the energy required by quails exposed to
toxic stresses. Furthermore, Hamidipoor et al. (2016a)
related the decrease in total protein of quails exposed to
LD acetate and deltamethrin to the reduced utilization
of dietary protein, malnutrition, or decreased protein
synthesis in liver.
Globulin and albumin are the major components of
total protein and the changes in their levels can be
used to monitor the health status of liver, kidney, and
the immune system (Patra et al., 2011). When protein
synthesis in the liver is reduced, it directly affects the
globulin level. In agreement with this, the results of the
present study showed that LD significantly decreased
the albumin and globulin level than control a long with
decreasing total protein level in LD-exposed quails.
 YUCCA MODULATES LEAD TOXICITY IN QUAILS
In the present study, the extent of LD-induced cellu-
lar injury was assessed by monitoring the serum level
of ALT and AST. These enzymes were released into
serum or plasma in case of liver damage, necrosis, or
inflammation. In addition, ALT enzyme has been re-
ported to increase in muscular dystrophy heart fail-
ure, anemia, and obstruction of bile duct (Philip et al.,
1995). Herein, LD significantly elevated ALT and AST
activities in the serum of LD-treated quails. These re-
sults agreed with previous works reported an elevation
in ALT and AST activities in serum after exposure to
LD in quails (Humayun et al., 2015; Hamidipoor et al.,
2016a). Lead significantly reduced the total protein, al-
bumin, and globulin levels and significantly increased
the AST and ALT activities in quails (Hamidipoor et
al., 2016b). This elevation may be attributed to increas-
ing the permeability of cellular membrane, fluidity of
the microsomal membrane, or the damage of hypato-
cytes cell membranes (Abdou et al., 2007). Production
of free radicals increased cellular basal metabolic rate,
irritability, and destructive alteration of liver under the
influence of LD (Ibrahim et al., 2012).
Considering the effect of LD on lipid profile, the
present study showed that exposure of quails to LD in
their diet significantly increased triglycerides, choles-
terol, and LDL while significantly decreased HDL val-
ues compared to control and other treatment groups.
Contradicting results were obtained by Hamidipoor
et al. (2016b), where LD exposure had no significant
changes in cholesterol, whereas it significantly reduced
the concentration of triglycerides. The disturbances in
lipid profile could be possibly returned to enhanced
biosynthesis of cholesterol and its accumulation in liver
and/or impairment of biliary functions (Ashour et al.,
2014) and this came on line with the obtained results
of liver functions.
From the present study, it was obvious that dietary
supplementation of YSE improved the blood biochem-
ical parameters (total protein, albumin, globulin) and
the activities of liver function enzymes (ALT and AST)
and showed positive effects on the lipid profile of quails
in the co-exposed groups (LD+YSE) especially at high
level. This indicates the potential modulatory role of
YSE on liver function mainly due to yucca saponins
and phenolics that showed hypocholesterolemic, antiox-
idant, hypoglycemic, anti-inflammatory, immunostim-
ulatory, antiviral, anticarcinogenic, and anti-mutagenic
activities (Gupta, 2014; Alagawany et al., 2016a). It is
well known that powder and extracts of plants rich in
saponins can alter the lipid metabolism of birds and dif-
ferent animal as reported by Rao and Kendall (1986).
Saponins reduced the serum cholesterol level in laying
hens (Aslan et al., 2004) and rabbits (Morehouse et al.,
1999). Saponins can form complexes with cholesterol
leading to its precipitation and can reduce hypercholes-
terolemia by altering the stability and size of choles-
terol micelle and decreasing its penetration into mucous
membrane cells (Milgate and Roberts, 1995). Addition-
ally, saponins can reduce the absorption of cholesterol
3133
and facilitate the discharge of neutral sterols including
plant sterols, cholesterol, coprostanol, and bile acids
in fecal matter (Jenkins and Atwal, 1994). Saponins
can also destruct the cell membrane and cause loss of
cholesterol (Morehouse, Bangerter, DeNinno, Inskeep,
McCarthy, Pettini, Savoy, Sugarman, Wilkins, Wilson,
Woody, Zaccaro and Chandler, 1999). Moreover, the
presence of saponins can enhance bile acid absorp-
tion and form high molecular weight micelles (cellulose
saponin–bile acid complexes) thus prevent bile acids
reabsorption and lead to the increase in the choles-
terol conversion into bile acids in the hepatic tissue
(Sidhu and Oakenfull, 1986). The decrease in choles-
terol absorption decreased its hepatic content and this
enhanced the activity of HMG-CoA reductase and in-
creased the LDL receptors in the liver (Harwood et al.,
1993).
Exposure to LD can impair the antioxidant defense
system and increase the cell vulnerability to the free
radicles attack leading to oxidative damage (Liu et al.,
2010). This could explain the observed decrease in SOD
and CAT activities of LD-exposed quails in the present
study. However, LD did not significantly alter the GSH
content in serum of quails. The altered antioxidant
status after LD exposure has been reported in some
previous works on animals and workers (Baranowska-
Bosiacka et al., 2012; Dai et al., 2013).
Oxidative stress of LD exposure was also evidenced
by increased MDA (lipid peroxidation marker) com-
pared to control. The elevated MDA indicated the
inability of antioxidant defense system to counteract
the ROS-induced damage. These results agreed with
some earlier reports in which LD induced oxidative
damage in birds and significantly enhanced lipid
peroxidation in liver of chick embryos (Somashekaraiah
et al., 1992), in brain, and liver of mallards exposed
to LD in the diet and in geese and mallards exposed
to sediments contaminated by LD (Mateo et al.,
2003). MDA levels increased in liver following LD
exposure (Sandhir and Gill, 1995). These results could
be returned to the destructive effects of LD on cell
membrane components including proteins and lipids
resulting in altered membrane function and structure
(Donaldson and Knowles, 1993).
In the present study, supplementation of YSE to
bird’s diet contained LD significantly improved the an-
tioxidant enzymes activities, whereas it significantly
decreased the serum level of MDA in birds com-
pared to the LD group. These results indicate that
YSE could counteract the undesirable impact of ox-
idation reaction and could decrease the lipid perox-
idation in birds exposed to environmental contami-
nation. Gümüş and İmik (2016) demonstrated that
yucca can act as a good antioxidant for poultry
and its supplementation to broiler diets increased
the total antioxidant capacity by improving the an-
tioxidants activities. These positive impacts could
be attributed to the phytochemicals of yucca such
as polyphenolic compounds (resveratrol (RES) and
3134 ALAGAWANY ET AL.
yuccaols A, B, C, D, and E) and steroidal saponins
(Alagawany et al., 2015). RES exhibited a powerful
scavenging activity against free radicals generated by
heavy metals as hydroxyl and superoxide radicals and
could make activation of the major transcription factors
that regulate the response to antioxidants (erythroid-
derived nuclear factor) (Rubiolo and Vega, 2008) and
could improve the activities of CAT, GSH-Px, SOD,
glutathione S-transferase (GST), and nicotinamide
adenine dinucleotide phosphate (NADPH) quinoneox-
idoreductase (Young et al., 2000). It could also main-
tain the reduced state of glutathione by inhibiting the
formation of glutathione disulfide; thereby it can pro-
tect cells from the attack of free radicales (FR), pre-
vent the oxidative damage of macromolecules, and in-
hibit apolipoprotein B protein peroxidation (Yan et al.,
2012). Similarly, RES as a dietary supplement has been
reported to diminish oxidative stress and improve the
antioxidant status in birds (Liu et al., 2014). Moreover,
RES and other phenolic compounds from yucca could
inhibit the generation of FR and reduced lipid peroxi-
dation (LPO) in blood platelets (Olas et al., 2003).
The impact of environmental pollutants on the bird’s
immune system is of great importance as birds are
highly required to compensate the shortage in animal
protein sources and the presence of these pollutants
could increase the susceptibility of birds to parasites
and infectious diseases (Galloway and Depledge, 2001).
The present study showed that LD significantly de-
creased the levels of immunoglobulin (IgG and IgM) in
exposed birds. These findings came on line with the ob-
served decrease in the levels of plasma globulin of the
same group that indicated a reduced immunity as the
liver cannot synthesis enough globulin for immunologic
actions. On the same context, exposure to LD signif-
icantly reduced IgG, IgA, and IgM in serum accom-
panied with increased MDA as a marker of oxidative
damage in some organs of rats (Gurer and Ercal, 2000).
The significant decrease in IgG and IgM can indi-
cate the deleterious effect of LD on the functions of B
cells that could be resulted from oxidative damage (de-
creased antioxidant activities and increased MDA) of
LD on these cells and this is totally agreed with Nu-
ran Ercal et al. (2001). Lead has been reported to de-
crease the activation of lymphocytes and inhibit their
proliferation, decrease the migration and motility of
macrophage (Kiremidjian-Schumacher et al., 1981), and
reduce the cytotoxicity and natural killer (Talcott et al.,
1985).
From the present study, it was obvious that di-
etary supplementation of YSE improved the immune
response, which was evidenced by the significant im-
provements in immunoglobulins. This could be proba-
bly due to the modulating effect of yucca in liver func-
tions including the level of globulin and the antioxidant
power of YSE observed in the present study. These ef-
fects are consistent with some previous reports on the
positive effects of YSE on immune functions, where
yucca saponins could enhance cellular and antibody hu-
moral immune responses, stimulate the cytokines secre-
tions, and activate the innate immunity (Palatnik de
Sousa et al., 2004). Saponins in chicken diets increased
the level of IgA (Zhai et al., 2011). Supplementation
of yucca powder to broiler chicks stimulated the im-
mune responses (cellular and humoral) (Su et al., 2016).
Similarly, yucca powder improved IgG content in layer
chicken (Alagawany et al., 2016a).
Fresh egg and egg products are among the most im-
portant nutritional sources in the daily diet so inves-
tigating the residual level of heavy metals is impor-
tant as they could induce negative impacts on bird per-
formance, productivity, and the consumers as well (Li
et al., 2005). The present study revealed that eggs from
LD-exposed quails showed the highest residual level
than other experimental groups. Birds can reduce the
deposition of metals into their eggs through decreas-
ing the deposition of minerals. This type of protection
could be sufficient to prevent deposition of some metals
like Cr and Mn but insufficient for LD (Hui, 2002). This
is in consistence with our results and may explain the
obtained decreased hatchability percentage that could
be returned to the ability of LD to induce some embryo
toxic impacts. On the other hand, YSE supplementa-
tion significantly reduced the LD residues suggesting
that in addition to its antioxidant activity, it could also
act as chelator and this makes YSE a powerful candi-
date for treating LD toxicity.
CONCLUSIONS
From the obtained results, we concluded that expo-
sure of quails to LD in their diets resulted in apparent
adverse effects on the performance parameters (produc-
tive and reproductive) and altered the biochemical pa-
rameters of liver function and lipid profile in addition to
its inhibitory effect on immune response of birds. These
adverse effects were accompanied with oxidative dam-
age evidenced by decreased antioxidant enzymes and
increased lipid peroxidation. On the other hand, using
of YSE as a natural feed additive in quail diets could
alleviate the deleterious effects of LD and enhanced the
immune function via improving levels of immunoglob-
ulin. However, YSE at high level (200 mg/kg diet) was
more effective than low one (100 mg/kg diet).
ACKNOWLEDGMENTS
The authors extend their appreciation to the Dean-
ship of Scientific Research at King Saud University for
funding this work through a research group project
(# RG-1438–066).
CONFLICT OF INTEREST
The authors declare that they have no competing in-
terests.
 YUCCA MODULATES LEAD TOXICITY IN QUAILS
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