Citation of this paper

The effect of using different levels of pomegranate (Punica granatum) peel powder on productive and physiological performance of Japanese quail (Coturnix coturnix japonica)

Rabia J Abbas, Khalid Ch K Al-Salhie and Sabah K M Al-Hummod

Department of Animal Production, College of Agriculture, University of Basra, Basra, Iraq
rj.abbas@yahoo.com

Abstract

The experiment was conducted to evaluate the efficacy of pomegranate peel powder (PPP)(as an unconventional feed stuff) to partially replace yellow maize on productive performance, egg quality, some blood characteristics and jejuna morphology in Japanese quail (Coturnix coturnix japonica) diets. A total of 120 ten weeks of age Japanese quail were randomly and equally assigned to four treatments (n=30). Each treatment was replicated three times (containing 10 birds each). Birds were fed on experimental diets that were formulated to contain the same components as the control diet substituting PPP instead of yellow maize at levels 2.5 or 5.0 and 7.5 % in other three experimental diets respectively.

Results indicated that final body weight was similar among quails fed on replaced diets, whereas, the highest feed intake was recorded in quail that received 7.5 % PPP; however, for 2.5 and 5.0% feed intake was not affected as compared to control. Substitution with PPP improved feed conversion ratio, egg production, egg numbers, egg weight and egg mass. Serum cholesterol, triglyceride, glucose concentration and GPT (5% PPP) were decreased and total protein was increased, whereas the GOT/ GPT ratio was not affected. Quails on experimental diets hadd the highest relative weight in liver and heart, as well as villus height, crypt depth compared to control. Ratio of villi length /villi depth in diets substituted with 5.0 and 7.5% PPP had the highest values as compared to other treatments. Females had greater liver weight, villus length and crypt depth than males. It can be concluded that the substitution of pomegranate peel powder at a level 7.5 %, instead of yellow maize, can improve productive and physiological parameters and jejuna morphology in quails.

Keywords: biochemical parameter, jejuna morphology, yellow maize

Introduction

Pomegranate (Punica granatum L.) peel is a nutritive, antioxidant rich by-product, easily available after production of pomegranate juice and ready to eat arils (Sayed 2014). A large quantity of pomegranate peel waste is produced, and its disposal is an environmental problem (Kanatt et al 2010). Pomegranate peels which constitute up to 40% of the whole fruit remain as a by-product after pomegranate juice production (Panichayupakaranant et al 2010). Pomegranate peel is a good source of tannin's, flavonoids, phenolic and other polyphony's compounds (Li et al 2006), alkaloids, aromatic compounds and enzymes (Dhinesh and Ramasamy 2016). Pomegranate peel was considered to have high content of polyphony compounds, which possess antioxidant properties that can play an important role against cancer cells (Lansky and Newman 2007, Cam and Hisil 2009, Dahham et al 2010).

Many studies have been focused on pomegranate as having antimicrobial activity against a wide range of microorganisms including bacteria (Gram positive, Gram negative), fungi, yeasts and viruses (Naz et al 2007). Several investigators reported that pomegranate peel has antioxidant and antibacterial properties (Reddy et al 2007, Opara et al 2009 , Al-Zoreky 2009) . Pomegranate peel extract (PPE) showed good antimicrobial activity against Staphylococcus aureus and Bacillus cereus having minimum inhibitory concentration of 0.01%, while Pseudonyms could be inhibited at a higher concentration of 0.1% in chicken meat products (Kanatt et al 2010), as well as it has high inhibitory effect against both Gram positive and Gram negative bacterial species (Devatkal et al 2013, Hamady et al 2015).

Moreover, pomegranate peel didn't get much attention as an unusual feed in quails ration. Several investigators reported that using Pomegranate (peel extract or seed pulp) in chicken diets improved egg production, productive, dressed weight percentages and extended meat shelf-life ((Kanatt et al 2010, Saki et al 2014, Hamady et al 2015).

Therefore, we focused our interest in the objective of this study on the pomegranate peel powder to investigate its effect as partial replacement of yellow maize on the productive performance, some physiological parameters and jejuna morphology of Japanese quail.

Material and methods

Animal Husbandry and Treatments

The experiment was carried out in Quail's Field, College of Agriculture, University of Basra from 15/ 3/ 2016 to 9/ 5/ 2016. A total of 120 ten weeks of age Japanese quails (Coturnix coturnix japonica) were weighed. Initial body weight was compared at the beginning of the study. The birds were randomly assigned to four treatments, with three replicates (cages) of ten quails each. All diets were formulated to meet the nutrient requirements of the Japanese quails. A basal control diet was formulated to contain 20.03% CP and 2904 kcal/kg metabolized energy (ME). In the other three experimental diets yellow maize was partially replaced by pomegranate peel powder (PPP) at levels of 2.5 or 5.0 and 7.5%. During the experiment (8 weeks), feed and water were supplied ad libitum. The composition of the basal diet is presented in Table1. Chemical analysis of PPP was carried out according to AOAC (2000) (Table 2) All birds reared in cages (replicates) of (45×70×75 cm), on a 17 h lighting was provided per day.

Table 1. Ingredients and composition of experimental diets
Ingredient, %	Pomegranate peel powder levels, %
Ingredient, %	0	2.5	5	7.5

Yellow Maize	56	53.5	51.0	48.5
Wheat	4.0	2.5	2.5	2.5
Soybean meal, 44%	28	28	28	28
pomegranate peel powder	0.0	2.5	5.0	7.5
Protein concentrate, 43%	5.0	6.0	6.0	6.3
Oil plant	1.0	1.5	1.7	1.8
Limestone	4.4	4.4	4.4	4.4
Dicalcium Phosphate	1.0	1.0	0.8	0.5
Vitamin / mineral premix	0.3	0.3	0.3	0.25
Common Salt	0.3	0.3	0.3	0.25
Total	100	100	100	100
Chemical analysis, %
^# ME, Kcal /Kg diet	2904	2905	2908	2901
Crude protein	20.0	20.2	20.0	20.0
Ether extract	3.93	3.92	3.86	3.82
Crude fiber	3.49	3.71	3.95	4.21
Calorie : protein ratio	145	144	145	145
Calcium	2.31	2.33	2.30	2.30
Phosphorus available	0.46	0.48	0.42	0.40
Methionine	0.38	0.41	0.43	0.46
Lysine	1.06	1.09	1.08	1.09
Methionine + Cystine	0.83	0.88	0.91	0.96
^# ME, Kcal /Kg diet = Metabolized energy

Table 2. Gross chemical composition,% on dry weight basis of pomegranate peel powder
Component, %	Pomegranate peel powder

Moisture	11.9
Crude protein	3.97
Crude fat	2.34
Ash content	4.19
Crude fiber	12.1
Available carbohydrate	77.4
Organic matter	95.8
Metabolized Energy, Kcal/Kg^#	2825
^# ME was calculated according to Lodhi et al (1976)

Data collection

Body weight (BW) was recorded at the beginning and at the end of the study. Egg production was recorded daily and feed consumption, cumulative egg number, egg mass and egg weight were recorded at two weekly intervals. Feed conversion ratio (FCR) was calculated by determining the amount of feed consumed per one kg of egg.

Blood samples and physiological parameters

Four quails per treatment (two males, two females) were randomly selected at the end of the experiment to determine blood serum parameters. Blood samples were collected separately in non-heparin's tubes for biochemical assays, and centrifuged (3000 rpm, 15 min, 25^oC) to obtain serum. Serum samples were stored at –20ºC until analyzed for total protein by a colorimetric method using commercial kits (Bio lab AS, France). Blood serum cholesterol, triglycerides and glucose concentrations were determined according to the methods of Tietz (1999) using commercial kits (Biolabo AS, France). The activities of glutamic-oxaloacetic transaminase (GOT) and glutamic-pyruvic transaminase (GPT) were determined spectrophotometncally by measuring the oxidation rate of NADH (nicotinamide adenine dinucleotide, reduced) in a thermostated cuivette at 340 nm after incubation of samples with L-aspartate and L-alanin, respectively (Bergmeyer and Bernt 1974 a and b).

Intestinal histology

At the end of the feeding two birds from each replicate were sacrificed after starving them for 12 h to limit intestinal throughput. To ensure clean histology samples, the intestinal samples were removed with sterile surgical tools in a cool environment. Livers and hearts were removed and weighed. The whole length of the small intestine was removed, washed and weighed. A length of 3 cm jejunum from two birds per replicate was cut midway between the end of the duodenum where bile duct and pancreatic ducts meet and the embryonic sac junction, washed with sodium chloride (1%) to remove intestinal contents, then weighed and fixated with 10% neutral buffered formalin over 24 hr. Tissue sections of the preserved small intestine samples were processed for 24 h in a tissue processor with ethanol as dehydrant and samples embedded in paraffin wax. Five µm sections were made from the tissue and were stained with haematoxylin-eosin (Gracia et al 2009). Samples were viewed under a light microscope. Morphometric variables were measured under a light microscope and the height and width of the villi were measured using an eyepiece micrometer. Villus height was obtained from the top of the villus to the crypt–villus junction, while crypt depth was defined as the depth of the invagination between villi (Hu and Guo 2007).

Statistical analysis

The performance data from experiment were executed to a one-way ANOVA, whereas the data (heart and liver weight, villus height, crypt depth and villus height to crypt depth ratio) were subjected to a two-way ANOVA (feeding × gender) by using SPSS program software (2012). Means separated using the Least Significant Difference at p <0.05.

Results and discussion

Productive performance

There were no differences among treatments in body weight (Table 3). Birds fed 7.5% of PPP consumed more feed than on other dietary treatments, while there were no differences in feed intake between 2.5 and 5.0 % PPP and control diets. Data in Table 3 show that there was improvement on feed conversion ratio, egg mass and egg weight in PPP diets compared with the control. Hen day egg production and cumulative egg number were highest in both 5% and 7.5% PPP diets compared with groups fed on 2.5 % PPP diet and the control (Figures 1 and 2).

Table 3. Effect of diets containing different levels of pomegranate peels powder on quail performance at 10-18 weeks of age
Quail performances	Dietary pomegranate peels powder, %				SEM	p
Quail performances	0.0	2.5	5.0	7.5	SEM	p

Initial body weight, g	182	182	183	182	0.61	0.833
Final body weight, g	223	229	228	227	1.74	0.643
Feed intake, g	960^b	943^b	952^b	1013^a	9.48	0.012
Egg mass, g/bird/8wks	347^d	357^c	374^b	390^a	5.04	< 0.001
Feed conversion ratio, g/g	2.77^c	2.64^b	2.55^a	2.60^ab	0.03	0.002
Hen day egg production, %	71.8^c	72.2^c	75.3^b	78.1^a	0.78	< 0.001
Egg weight, g	11.5^c	11.7^b	11.8^ab	11.9^a	0.05	< 0.001
Number of eggs, egg/bird/8wks	30.2^c	30.3^c	31.6^b	32.8^a	0.33	< 0.001
^abc ^d Means without common superscript are different at p < 0.05 ,SEM: Standard error of the mean


Figure 1. Effect different levels of pomegranate peels powder on egg mass (g/bird/8 wks) of quail at 10-18 weeks of age	Figure 2. Effect different levels of pomegranate peels powder on hen egg production (%) of quail at 10-18 weeks of age

Plasma parameters

Serum cholesterol, glucose and triglyceride declined in all dietary groups in comparison with the control (Figure 3). Quails that received diets with 2.5 % PPP had the lowest GPT activity, whereas GOT and GOT/ GPT ratio was not affected as PPP was increased, while serum total protein was superior in dietary treatments compared with the control.

Table 4. Effect of diets containing different levels of pomegranate peel powder on some blood characteristics of quail at 18 weeks of age
Parameters	Dietary pomegranate peels powder, %				SEM	p
Parameters	0.0	2.5	5.0	7.5	SEM	p

Total Protein, g/dL	5.1^b	5.7^a	5.7^a	5.6^a	0.08	0.043
Glucose, mg/dL	276^a	264^b	262^b	261^c	2.46	0.033
Cholesterol, mg/dL	296.7^a	275.7^bc	258.0^cd	246.7^d	6.28	0.002
Triglycerides, mg/dL	354.7^a	324.7^bc	333.7^b	311.0^c	5.37	0.004
GOT#	221	220	224	218	1.81	0.811
GPT##	18.3^ab	17.4^c	18.7^a	17.8^bc	0.17	0.003
GOT/ GPT ratio	12.1	12.6	12.0	12.3	0.14	0.354
#GOT: Glutamic Oxaloacetic Transaminases enzyme, ##GPT: Glutamic Pyruvic Transaminases enzyme ^abc ^d Means without common superscript are different at p < 0.05 , SEM: Standard error of the mean,

Figure 3. Effect different levels of pomegranate peels powder on serum
cholesterol (mg/dL) of quail at 18 weeks of age

Organ weight and histology measurement

On diets with pomegranate peel at 5% level, heart weight was higher as compared with control, whereas, but there were no differences in heart relative weight between birds fed 2.5 and 7.5% of PPP and control. Liver weights were higher in PPP replaced diets as compared to control. Females were superior to males in these traits. Jejunum villus height, crypt depth and ratio of the villus height to the crypt depth (V/C) were increased with increasing PPP in the diets (Table 5; Figures 4-6) The results also revealed that females were superior compared to males in villus height and crypt depth, while the V/C)ratio was not affected between sexes. The results did not indicate any evidence of treatment × gender interaction for all traits examined (Table 5).

Table 5. Morphometric measurements of the jejunum, heart and liver relative weight of quail fed pomegranate peels powder at 18 weeks of age
Parameter	Sex	Dietary pomegranate peels powder, %				Mean	SEM	p
Parameter	Sex	0.0	2.5	5.0	7.5	Mean	SEM	p

Heart^#	M	0.87	0.91	0.94	0.92	0.91	0.012	0.222
	F	0.89	0.92	0.96	0.93	0.93	0.012	0.222
	mean	0.88^b	0.92^ab	0.95^a	0.93^ab	0.92	0.008	0.048
Liver^#	M	2.21	2.27	2.26	2.31	2.26_B	0.014	< 0.001
	F	2.34	2.42	2.41	2.41	2.40^A	0.014	< 0.001
	mean	2.27^b	2.35^a	2.34^a	2.36^a	2.33	0.017	0.003
Villus length, µm	M	290	343	470	493	400^B	2.672	0.015
	F	307	377	513	517	428^A	2.791	0.015
	mean	298^c	360^b	492^a	505^a	414	1.913	< 0.001
Crypt depth, µm	M	34.7	39.3	48.7	50.3	43.3^B	0.201	0.007
	F	36.7	42.3	52.3	51.7	45.8^A	0.205	0.007
	mean	35.7^c	40.8^b	50.5^a	51.0^a	44.5	0.143	< 0.001
Villus/ crypt ratio	M	8.39	8.74	9.64	9.88	9.17	0.219	0.672
	F	8.27	8.89	9.80	10.0	9.25	0.239	0.672
	mean	8.33^b	8.81^b	9.72^a	9.94^a	9.21	0.159	< 0.001
^# as percent to body weight ^abc Means in the same row with no common superscript are different at p < 0.05, ^AB Means in the same column with no common superscript are different at p <0.05. SEM : Standard error of the mean,


Figure 4. Effect different levels of pomegranate peel powder on villus length (µm) of quail at 18 weeks of age	Figure 5. Effect different level of pomegranate peels powder on crypt depth (µm) of quail at 18 weeks of age

Figure 6. Effect different level of pomegranate peels powder on
villus/crypt ratio of quail at 18 weeks of age

Discussion

Similar results to ours were reported by Rajani et al (2011) and Bostami et al (2015) on body weight gain, for pomegranate peels powder (PPP) inclusion in broiler diets. Differently from the present study, Yassein et al (2015), recorded decrease in FI and FCR in Japanese quails fed diet supplemented with 10 and 15 g PPP/kg diet. Improvements in feed intake, feed conversion ratio and egg production traits in birds fed pomegranate peel powder may be related to the palatability and digestion stimulating effects of these additives. Positive effects that plant feed additives exert on gastro-intestinal enzymatic activity and enhanced nutrient absorption and digestibility were reported by Banerjee et al (2013). The presence of active substances in PPP that improve digestion and metabolism have been attributed to antioxidant and antibacterial properties. These help to decrease combat pathogens in the intestine and as a consequence more nutrients are available in the intestinal lumen for absorption to convert to body mass (Jamroz et al 2006, Reddy et al 2007, Opara et al 2009, Al-Zoreky 2009). Health benefits of pomegranate peel are thought to be due to its biological activities such as antioxidant, antimicrobial, anti-inflammatory, and anticancer effects (Prakash and Prakash 2011), as well as tannins (Hassanpour et al 2011) , could be the main reasons for its bioactive functions.

The findings related to serum cholesterol, glucose and triglyceride levels, obtained in this study agree with Yassein et al (2015) who found a decrease in lipid profile and glucose in Japanese quails fed with PPP. In contrar to our results, Saki et al (2014) reported an increase in serum cholesterol levels, when using up to 15% of PPP in diets of laying hen. Depending on the presence of phenolic compounds (punicalagin, punicalin, gallic acid and particularly elegiac acid), PPP may affect serum lipid concentrations and other blood indices (Rajabian et al 2007). Moreover, some investigations showed that pomegranate peels contain high ratios of antioxidants material in addition to phenolic materials and metals (Ibrahium 2010, Ullah et al 2012, Taher-Maddah et al 2012). Furthermore, polyphony's of pomegranate may accelerate and promote cholesterol metabolism by reversing cholesterol transport via HDL (Aviram et al 2002, Esmaillzadeh et al 2004).

In respect to sex effects on liver weight, our results are in line with those of Selim et al (2006), who reported higher weight of liver in females than in males. As for the improvement in jejunum measurements recorded in the present study, Svihus (2014) indicated that the jejunum is largely responsible for digestion and absorption of all the major nutrients, thus, increased villi height may be a consequence of greater need for digestive capacity. Accordingly, the change in villus lengths of jejunum may influence health and may increase nutrient uptake, which is positively reflected in egg production. In intestinal parameters, females showed the highest values in micro metric criteria in all ages compared to males (Rahmat et al 2016).

Conclusions

Data from the present study indicate that up to 7.5 % level of pomegranate peel powder could be utilized effectively by Japanese quails for egg production with improvements in productivity, and in some physiological parameters and jejuna morphology in both males and females.

Acknoledgment

The authors would like to acknowledge the Department of Animal Production College of Agriculture University of Basra for logistic support.

References

Al-Zoreky N S 2009 Antimicrobial Activity of Pomegranate (Punica granatum L.) Fruit Peels. International Journal of Food Microbiology134:244-248.

AOAC 2000 Association of Official Analytical Chemists. Official Methods of Analysis of the AOAC International, 17th ed. Gaithersburg, Marylad, USA.

Aviram M, Dornfield L and Coleman R 2002 Pomegranate Juice Polyphenols Inhibit L-density Lipoprotein Oxidation in Cardiovascular Diseases: Studies in Atherosclerotic Mice and in Humans. Drugs Under Experimental and Clinical Research 28:49 - 62.

Banerjee S, Mukhopadhayay S K, Haldar S, Ganguly S, Pradhan S, Patra N C, Niyogi D and Isore D P 2013 Effect of Phytogenic Growth Promoter on Broiler Birds. Journal of Pharmacognosy and Phytochemistry 1:183–188.

Bergmeyer H U and Bernt E 1974a Glutamate-Oxaloacetate Transaminase, UV-Assay, Manual Method. In: Bergmeyer, H U (ed.) Methods of Enzymatic Analysis Vol. 2. Academic Press, New York p:727-733.

Bergmeyer H U and Bernt E 1974b Glutamate-pyruvate transaminase, UV-assay, manual method. In: Bergmeyer H. U. (ed.) Methods of enzymatic enzymatic analysis, Vol.2. Academic Press, New York, p:752-758.

Bostami A B M R, Ahmed S T, Islam M M, Mun H S, KoS Y, Kim S S and Yang C J 2015 Growth Performance, Fecal Noxious Gas Emission and Economic Efficacy in Broilers Fed Fermented Pomegranate Byproducts as Residue of Fruit Industry. International Journal of Advanced Research 3(3):102-114.

Cam M, Hısıl Y and Durmaz G 2009 Classification of Eight Pomegranate Juices Based on Antioxidant Capacity measured by Four Methods. Food chemistry 112:721 –72 6.

Dahham, S S, Ali M N, Tabassum H and Khan M 2010 Studies on Antibacterial and Antifungal Activity of Pomegranate ( Punica granatum L.). American-Eurasian Journal of Agricultural & Environmental Sciences 9(3):273-281.

Devatkal S K, Jaiswal P, Jha S N, Bharadwaj R and Viswas K N 2013 Antibacterial Activity of Aqueous Extract of Pomegranate Peel Against Pseudomonas stutzeri Isolated from Poultry Meat. Journal of Food Science and Technology 50(3):555-560.

Dhinesh K V and Ramasamy D 2016 Pomegranate Processing and Value Addition: Review. Journal of Food Processing & Technology 7(3):565-566.

Esmaillzadeh A, Tahbaz F and Gaini I 2004 Concentrated Pomegranate Juice Improves Lipid Profiles in Diabetic Patients with Hyperlipidemia. Journal of Medicinal Food 7:305 -308.

Gracia M I, Lazaro R, Latorre M A, Medel P, Aranibar M J, Jimenez-Moreno E and Mateos G G 2009 Influence of Enzyme Supplementation of Diets and Cooking–Flaking of Maize on Digestive Traits and Growth Performance of Broilers from 1 to 21Days of Age. Animal Feed Science and Technology 150:303-315.

Hamady G A A, Abdel-Moneim M A, El-Chaghaby G A, Abd-El-Ghany Z M and Hassanin M S 2015 Effect of Pomegranate Peel Extract as Natural Growth Promoter on the Productive Performance and Intestinal Microbiota of Broiler Chickens. African Journal of Agricultural Science and Technology3(12) :514-519.

Hassanpour S, Maheri-Sis N, Eshratkhah B and Mehmandar F B 2011 Plants and Secondary Metabolites (Tannins):A Review. International Journal of Forest, Soil and Erosion1(1):47-53.

Hu Z and Guo Y 2007 Effects of Dietary Sodium Butyrate Supplementation on the Intestinal Morphological Structure, Absorptive Function and Gut ﬂora in Chickens. Animal Feed Science and Technology 132: 240–249.

Ibrahium M I 2010 Efficiency of Pomegranate Peel Extract as Antimicrobial, Antioxidant and Protective Agents. World Journal of Agricultural Sciences 6(4):338-344.

Jamroz D, Wertelecki T, Houszka M and Kamel C 2006 Influence of Diet Type on the Inclusion of Plant Origin Active Substances on Morphological and Histochemical Characteristics of the Stomach and Jejunum Walls in Chicken. Journal of Animal Physiology and Animal Nutrition, (Berl) 90:255–268.

Kanatt S R, Chander R and Sharma A 2010 Antioxidant and Antimicrobial Activity of Pomegranate Peel Extract Improves the Shelf life of Chicken Products. International Journal of Food Science & Technology45:216–222.

Lansky E P and Newman R A 2007 Punica granatum (Pomegranate) and its Potential for Prevention and Treatment of Inflammation and Cancer. Journal of Ethnopharmacology 109:177-206.

Li Y, Guo C, Yang J, Wei J, Xu J and Cheng S 2006 Evaluation of Antioxidant Properties of Pomegranate Peel Extract in Comparison with Pomegranate Pulp Extract. Food Chemistry 96:245-260.

Lodhi G N, Singh D and Ichhponani J S 1976 Variation in Nutrient Content of Feeding Stuffs Rich in Protein and Reassessment of the Chemical Method for Metabolizable Energy Estimation for Poultry. Journal of Agricultural Science and Technology86 (02):293-303.

Naz S, Siddiqi R S, Ahmed R, Rasool S A and Sayeed S A 2007 Antibacterial Activity Directed Isolation of Compounds from Punica granatum. Journal of Food Science9(72):341-345.

Opara L U, Majeed R, Al-Ani M R and Al-Shuaibi Y S 2009 Physico-Chemical Properties, Vitamin C Content and Antimicrobial Properties of Pomegranate Fruit (Punica granatum L).Food and Bioprocess Technology 2(3):315 – 321.

Panichayupakaranant P, Tewtrakul S and Yuenyongsawad S 2010 Antibacterial, Anti-inflammatory and Anti-allergic Activities of Standardised Pomegranate Rind Extract. Food Chemistry 123:400-403.

Prakash C V S and Prakash I 2011 Bioactive Chemical Constituents from Pomegranate (Punica granatum) Juice, Seed and Peel- A Review. International Journal of Research in Chemistry and Environment 1:1-18.

Rahmat A F D, Baghaib R and Rahimib R 2016 Morphometric Properties and Distribution of Alpha-Actin in the Smooth Muscle Cells (ASMA) of the Small Intestine During Development in Chicken. Journal of Applied Animal Research 44(1):492-497. http://dx.doi.org/10.1080/09712119.2015.1091325.pdf

Rajabian T, Fallah Hoseini H, Karami M, Rasuli A and Faghihzadeh S 2007 Effects of Pomegranate Juice and Seed Oil on Blood Lipid Levels and Atherosclerosis in Rabbits Hypercholestrolemic. Plan Journal and Medicare 25:93-105.

Rajani, Karimi Torshizi M A and Rahimi S 2011 Control of Ascites Mortality and Improved Performance and Meat Shelf life in Broilers Using Feed Adjuncts with Presumed Antioxidant Activity. Animal Feed Science and Technology 170:239-245.

Reddy M K, Gupta S K, Jacob M R, Khan S I and Ferreira D 2007 Antioxidant, Antimalarial and Antimicrobial Activities of Tannin-rich Fractions Ellagitannins and Phenolic Acids from Punica granatum L. Planta Medica 73:461-467.

Saki A A, Rabet M, Zamani P and Yousefi A 2014 The Effects of Different Levels of Pomegranate Seed Pulp with Multi-enzyme on Performance, Egg Quality and Serum Antioxidant in Laying Hens. Iranian Journal of Applied Animal Science 4(4):803-808.

Sayed-Ahmed E F 2014 Evaluation of Pomegranate Peel Fortified Pan Bread on Body Weight Loss. International Journal of Food Sciences and Nutrition3(5):411-420.

Selim K, Ibarhim S and Ozge Y 2006 Effect of Separate and Mixed Rearing According to Sex on Fattening Performance and Carcass Characteristics in Japanese quails (Cotunix cotunix Japonica). Archiv fur Tierzucht 49(6): 607-614.

SPSS 2012 SPSS User’s Guide Statistics Version 19. Copyright IBM, SPSS Inc., USA.

Svihus B 2014 Function of the Digestive System. The Journal of Applied Poultry Research 23:306-314.

Taher-Maddah M, Maheri-Sis N, Salamatdoustnobar R and Ahmadzadeh A 2012 Comparing Nutritive Value of Ensiled and Dried Pomegranate Peels for Ruminants Using in Vitro gas Production Technique. Annals of Biological Research 3(4):1942-1946. (http://scholarsresearchlibrary.com/archive.html).pdf

Tietz N W 1999 Textbook of Clinical Chemistry.3rd ed. Burtis, E R Ash Wood, W.B. Saunders Company, Philadelphia pp: 616.

Ullah N, Ali J, Ali Khan F, Khurram M, Hussain A, Inayat-Ur-Rahman, Zia-Ur- Rahman and Shafqatullah 2012 Proximate Composition, Minerals Content, Antibacterial and Antifungal Activity Evaluation of Pomegranate (Punica granatum L.) Peels Powder. Middle-East Journal of Scientific Research 11(3):396-401.

Yassein D M M, Abdallah E A, Ismail I I and Faddle A A 2015 Effect of Dietary Supplementation of Pomegranate Peel Powder and Butylated hydroxy Toluene on some Productive, Physiological and Immunological Parameters of Japanese Quail. Egyptian Journal of Animal Production 52 (Suppl. Issue):105-113.

Received 6 June 2017; Accepted 6 October 2017; Published 1 December 2017

Go to top