M. Alagawany, M. E. Abd El-Hack, M. R. Farag, S. S. Elnesr, M. S. El-Kholy, I. M. Saadeldin, and A. A. Swelum
M. Alagawany, M. E. Abd El-Hack, M. R. Farag, S. S. Elnesr, M. S. El-Kholy, I. M. Saadeldin, and A. A. Swelum
M. Alagawany, M. E. Abd El-Hack, M. R. Farag, S. S. Elnesr, M. S. El-Kholy, I. M. Saadeldin, and A. A. Swelum
ABSTRACT The present study investigated the toxic hatchability percentages comparable to that of control.
impacts of lead (LD) on the productive and repro- Triglycerides, cholesterol, and LDL contents in LD plus
ductive performances of Japanese quails and the role YSE100 or LD plus YSE200 groups were significantly
of Yucca schidigera extract (YSE) in reducing these decreased than LD alone group. LD significantly de-
impacts. A total of 360 mature Japanese quails (at creased superoxide dismutase and catalase activities in
2 months of age) were used and the experiment was the serum with no effect on reduced glutathione con-
lasted for 8 wk. The birds were divided into 6 equal tent. Co-exposure to YSE100 or YSE200 with LD sig-
groups as follows: control (basal diet), basal diet + nificantly increased the catalase activity and numeri-
100 mg LD/kg diet, basal diet + YSE (100 mg/kg cally increased the superoxide dismutase activity than
diet), basal diet + YSE (200 mg/kg diet), basal diet LD alone. YSE100 or YSE200 decreased malondialde-
+ LD (100 mg/kg diet) + YSE (100 mg/kg diet), and hyde contents than LD alone group. LD plus YSE100
basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg or YSE200 groups exhibited significant improvements
diet). LD resulted in a significant decrease in feed in- in the level of immunoglobulins. Co-exposure to YSE
take (FI), feed conversion ratio (FCR), and egg pro- with LD significantly decreased the LD residues in
duction of birds compared with the control group. Sup- egg than the LD group. The obtained results showed
plementation of YSE (100 or 200) to LD containing that YSE exhibited a potential modulatory role against
diet could significantly improve the quail performance the LD-induced inhibitory effects on the productive
parameters to be comparable with the control val- and reproductive performances of Japanese quails
ues. Fertility and hatchability % were decreased by and YSE at 200 mg/kg diet was more effective
LD, whereas YSE at both levels (100 or 200) sepa- than 100 mg/kg diet in reversing the LD-induced
rately or in combination with LD showed fertility and alterations.
Key words: Yucca, lead, performance, blood, quail
2018 Poultry Science 97:3126–3137
http://dx.doi.org/10.3382/ps/pey186
Productive parameters
Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg)
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.
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.
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)
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.
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
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- in the presence of LD. This improvement could be ex-
cium reflecting the inability of intoxicated quails to plained by the suggestions of El Anwer et al. (2009),
mobilize adequate amount of plasma calcium. More- who returned the increased hatchability and fertility to
over, LD exposure decreased the weight and function 2 main assumptions; the first assumption is the ability
of ovary in exposed quails. Therefore, it was suggested of yucca to reduce ammonia concentration in the sur-
that ovary could be involved in the regulation of egg rounding atmosphere of eggs that could help in adjust-
production than calcium. Additionally, LD has been ing the egg pH. The reducing effect of yucca on blood
reported to induce neurotoxicity in quails inducing im- urea has been previously reported in broilers (Balog
pairment of the neurochemical control on reproductive et al., 1994) that could be mainly due to saponin, stil-
hormones regulation (Edens, 1985). benes, and carbohydrates in yucca. These components
In our study, supplementation of YSE to bird’s diet have been reported to have modulatory effects on renal
concurrently with LD resulted in significant improve- functions and could increase the clearance of urea and
ments in the altered productive performance parame- lower blood concentrations of ammonia and urea (Duffy
ters of quails including FI, FCR, egg production, fer- et al., 2001). YES has could inhibit urease enzyme in
tility, and hatchability to levels that are comparable to vivo and in vitro (Asplund 1991; Balog et al., 1994).
those of control. Dietary supplementation of Y. schidi- Biochemical findings of the present study revealed
gera has been reported to induce significant impacts that total protein level was found to be decreased
on layer performance by increasing the egg production in serum of LD-exposed group compared to control.
and final body weight (Gurbuz et al., 2016). Similarly, These results are in accordance with those of Humayun
Cheek (1998) reported that feeding poultry on yucca et al. (2015) who studied hematobiochemical changes
could improve their growth and productivity. These induced by LD poisoning in quails. The decreased pro-
positive effects of yucca could be returned to the pres- tein level could be returned to increasing protein utiliza-
ence of steroidal saponins as a main component and tion to obtain the energy required by quails exposed to
other surface active components that could promote toxic stresses. Furthermore, Hamidipoor et al. (2016a)
the utilization and absorption of nutrients from gas- related the decrease in total protein of quails exposed to
trointestinal tract by improving its epithelial lining of LD acetate and deltamethrin to the reduced utilization
the cell membrane and decreasing the surface tension of dietary protein, malnutrition, or decreased protein
(Goetsch and Owens, 1985). synthesis in liver.
Fertility and hatchability are important parameters Globulin and albumin are the major components of
in studying the reproductive performance; they are af- total protein and the changes in their levels can be
fected by environment, insufficient nutrients, and ge- used to monitor the health status of liver, kidney, and
netic involvement (Ayasan, 2013). Therefore, to ob- the immune system (Patra et al., 2011). When protein
tain the highest fertility and hatchability percentages synthesis in the liver is reduced, it directly affects the
of quails, optimum conditions should be provided be- globulin level. In agreement with this, the results of the
fore and after hatching (Ggüçlü, 2011). In the present present study showed that LD significantly decreased
study, yucca at high level (200 mg/kg body weight) was the albumin and globulin level than control a long with
found to improve fertility and hatchability percentages decreasing total protein level in LD-exposed quails.
YUCCA MODULATES LEAD TOXICITY IN QUAILS 3133
In the present study, the extent of LD-induced cellu- and facilitate the discharge of neutral sterols including
lar injury was assessed by monitoring the serum level plant sterols, cholesterol, coprostanol, and bile acids
of ALT and AST. These enzymes were released into in fecal matter (Jenkins and Atwal, 1994). Saponins
serum or plasma in case of liver damage, necrosis, or can also destruct the cell membrane and cause loss of
inflammation. In addition, ALT enzyme has been re- cholesterol (Morehouse, Bangerter, DeNinno, Inskeep,
ported to increase in muscular dystrophy heart fail- McCarthy, Pettini, Savoy, Sugarman, Wilkins, Wilson,
ure, anemia, and obstruction of bile duct (Philip et al., Woody, Zaccaro and Chandler, 1999). Moreover, the
1995). Herein, LD significantly elevated ALT and AST presence of saponins can enhance bile acid absorp-
activities in the serum of LD-treated quails. These re- tion and form high molecular weight micelles (cellulose
sults agreed with previous works reported an elevation saponin–bile acid complexes) thus prevent bile acids
in ALT and AST activities in serum after exposure to reabsorption and lead to the increase in the choles-
LD in quails (Humayun et al., 2015; Hamidipoor et al., terol conversion into bile acids in the hepatic tissue
2016a). Lead significantly reduced the total protein, al- (Sidhu and Oakenfull, 1986). The decrease in choles-
bumin, and globulin levels and significantly increased terol absorption decreased its hepatic content and this
the AST and ALT activities in quails (Hamidipoor et enhanced the activity of HMG-CoA reductase and in-
al., 2016b). This elevation may be attributed to increas- creased the LDL receptors in the liver (Harwood et al.,
ing the permeability of cellular membrane, fluidity of 1993).
the microsomal membrane, or the damage of hypato- Exposure to LD can impair the antioxidant defense
cytes cell membranes (Abdou et al., 2007). Production system and increase the cell vulnerability to the free
of free radicals increased cellular basal metabolic rate, radicles attack leading to oxidative damage (Liu et al.,
irritability, and destructive alteration of liver under the 2010). This could explain the observed decrease in SOD
influence of LD (Ibrahim et al., 2012). and CAT activities of LD-exposed quails in the present
Considering the effect of LD on lipid profile, the study. However, LD did not significantly alter the GSH
present study showed that exposure of quails to LD in content in serum of quails. The altered antioxidant
their diet significantly increased triglycerides, choles- status after LD exposure has been reported in some
terol, and LDL while significantly decreased HDL val- previous works on animals and workers (Baranowska-
ues compared to control and other treatment groups. Bosiacka et al., 2012; Dai et al., 2013).
Contradicting results were obtained by Hamidipoor Oxidative stress of LD exposure was also evidenced
et al. (2016b), where LD exposure had no significant by increased MDA (lipid peroxidation marker) com-
changes in cholesterol, whereas it significantly reduced pared to control. The elevated MDA indicated the
the concentration of triglycerides. The disturbances in inability of antioxidant defense system to counteract
lipid profile could be possibly returned to enhanced the ROS-induced damage. These results agreed with
biosynthesis of cholesterol and its accumulation in liver some earlier reports in which LD induced oxidative
and/or impairment of biliary functions (Ashour et al., damage in birds and significantly enhanced lipid
2014) and this came on line with the obtained results peroxidation in liver of chick embryos (Somashekaraiah
of liver functions. et al., 1992), in brain, and liver of mallards exposed
From the present study, it was obvious that dietary to LD in the diet and in geese and mallards exposed
supplementation of YSE improved the blood biochem- to sediments contaminated by LD (Mateo et al.,
ical parameters (total protein, albumin, globulin) and 2003). MDA levels increased in liver following LD
the activities of liver function enzymes (ALT and AST) exposure (Sandhir and Gill, 1995). These results could
and showed positive effects on the lipid profile of quails be returned to the destructive effects of LD on cell
in the co-exposed groups (LD+YSE) especially at high membrane components including proteins and lipids
level. This indicates the potential modulatory role of resulting in altered membrane function and structure
YSE on liver function mainly due to yucca saponins (Donaldson and Knowles, 1993).
and phenolics that showed hypocholesterolemic, antiox- In the present study, supplementation of YSE to
idant, hypoglycemic, anti-inflammatory, immunostim- bird’s diet contained LD significantly improved the an-
ulatory, antiviral, anticarcinogenic, and anti-mutagenic tioxidant enzymes activities, whereas it significantly
activities (Gupta, 2014; Alagawany et al., 2016a). It is decreased the serum level of MDA in birds com-
well known that powder and extracts of plants rich in pared to the LD group. These results indicate that
saponins can alter the lipid metabolism of birds and dif- YSE could counteract the undesirable impact of ox-
ferent animal as reported by Rao and Kendall (1986). idation reaction and could decrease the lipid perox-
Saponins reduced the serum cholesterol level in laying idation in birds exposed to environmental contami-
hens (Aslan et al., 2004) and rabbits (Morehouse et al., nation. Gümüş and İmik (2016) demonstrated that
1999). Saponins can form complexes with cholesterol yucca can act as a good antioxidant for poultry
leading to its precipitation and can reduce hypercholes- and its supplementation to broiler diets increased
terolemia by altering the stability and size of choles- the total antioxidant capacity by improving the an-
terol micelle and decreasing its penetration into mucous tioxidants activities. These positive impacts could
membrane cells (Milgate and Roberts, 1995). Addition- be attributed to the phytochemicals of yucca such
ally, saponins can reduce the absorption of cholesterol as polyphenolic compounds (resveratrol (RES) and
3134 ALAGAWANY ET AL.
yuccaols A, B, C, D, and E) and steroidal saponins yucca saponins could enhance cellular and antibody hu-
(Alagawany et al., 2015). RES exhibited a powerful moral immune responses, stimulate the cytokines secre-
scavenging activity against free radicals generated by tions, and activate the innate immunity (Palatnik de
heavy metals as hydroxyl and superoxide radicals and Sousa et al., 2004). Saponins in chicken diets increased
could make activation of the major transcription factors the level of IgA (Zhai et al., 2011). Supplementation
that regulate the response to antioxidants (erythroid- of yucca powder to broiler chicks stimulated the im-
derived nuclear factor) (Rubiolo and Vega, 2008) and mune responses (cellular and humoral) (Su et al., 2016).
could improve the activities of CAT, GSH-Px, SOD, Similarly, yucca powder improved IgG content in layer
glutathione S-transferase (GST), and nicotinamide chicken (Alagawany et al., 2016a).
adenine dinucleotide phosphate (NADPH) quinoneox- Fresh egg and egg products are among the most im-
idoreductase (Young et al., 2000). It could also main- portant nutritional sources in the daily diet so inves-
tain the reduced state of glutathione by inhibiting the tigating the residual level of heavy metals is impor-
formation of glutathione disulfide; thereby it can pro- tant as they could induce negative impacts on bird per-
tect cells from the attack of free radicales (FR), pre- formance, productivity, and the consumers as well (Li
vent the oxidative damage of macromolecules, and in- et al., 2005). The present study revealed that eggs from
hibit apolipoprotein B protein peroxidation (Yan et al., LD-exposed quails showed the highest residual level
2012). Similarly, RES as a dietary supplement has been than other experimental groups. Birds can reduce the
reported to diminish oxidative stress and improve the deposition of metals into their eggs through decreas-
antioxidant status in birds (Liu et al., 2014). Moreover, ing the deposition of minerals. This type of protection
RES and other phenolic compounds from yucca could could be sufficient to prevent deposition of some metals
inhibit the generation of FR and reduced lipid peroxi- like Cr and Mn but insufficient for LD (Hui, 2002). This
dation (LPO) in blood platelets (Olas et al., 2003). is in consistence with our results and may explain the
The impact of environmental pollutants on the bird’s obtained decreased hatchability percentage that could
immune system is of great importance as birds are be returned to the ability of LD to induce some embryo
highly required to compensate the shortage in animal toxic impacts. On the other hand, YSE supplementa-
protein sources and the presence of these pollutants tion significantly reduced the LD residues suggesting
could increase the susceptibility of birds to parasites that in addition to its antioxidant activity, it could also
and infectious diseases (Galloway and Depledge, 2001). act as chelator and this makes YSE a powerful candi-
The present study showed that LD significantly de- date for treating LD toxicity.
creased the levels of immunoglobulin (IgG and IgM) in
exposed birds. These findings came on line with the ob- CONCLUSIONS
served decrease in the levels of plasma globulin of the
same group that indicated a reduced immunity as the From the obtained results, we concluded that expo-
liver cannot synthesis enough globulin for immunologic sure of quails to LD in their diets resulted in apparent
actions. On the same context, exposure to LD signif- adverse effects on the performance parameters (produc-
icantly reduced IgG, IgA, and IgM in serum accom- tive and reproductive) and altered the biochemical pa-
panied with increased MDA as a marker of oxidative rameters of liver function and lipid profile in addition to
damage in some organs of rats (Gurer and Ercal, 2000). its inhibitory effect on immune response of birds. These
The significant decrease in IgG and IgM can indi- adverse effects were accompanied with oxidative dam-
cate the deleterious effect of LD on the functions of B age evidenced by decreased antioxidant enzymes and
cells that could be resulted from oxidative damage (de- increased lipid peroxidation. On the other hand, using
creased antioxidant activities and increased MDA) of of YSE as a natural feed additive in quail diets could
LD on these cells and this is totally agreed with Nu- alleviate the deleterious effects of LD and enhanced the
ran Ercal et al. (2001). Lead has been reported to de- immune function via improving levels of immunoglob-
crease the activation of lymphocytes and inhibit their ulin. However, YSE at high level (200 mg/kg diet) was
proliferation, decrease the migration and motility of more effective than low one (100 mg/kg diet).
macrophage (Kiremidjian-Schumacher et al., 1981), and
reduce the cytotoxicity and natural killer (Talcott et al.,
ACKNOWLEDGMENTS
1985).
From the present study, it was obvious that di- The authors extend their appreciation to the Dean-
etary supplementation of YSE improved the immune ship of Scientific Research at King Saud University for
response, which was evidenced by the significant im- funding this work through a research group project
provements in immunoglobulins. This could be proba- (# RG-1438–066).
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- CONFLICT OF INTEREST
fects are consistent with some previous reports on the The authors declare that they have no competing in-
positive effects of YSE on immune functions, where terests.
YUCCA MODULATES LEAD TOXICITY IN QUAILS 3135
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