Potential Relevance of Pomegranate (Punica granatum) Peel in the Nutrition, Health, and Quality Products of Poultry

Subject Areas : Camel

E.A. Akuru ¹ , C.I. Chukwuma ² , C.E. Oyeagu ³ , T.C. Mpendulo ⁴ , F.B. Lewu ⁵

1 - Department of Livestock and Pasture Science, University of Fort Hare, Private Bag X1314, Alice 5700, Eastern Cape, South Africa|Department of Animal Science, University of Nigeria Nsukka 410001, Nsukka, Nigeria
2 - Centre for Quality of Health and Living, Faculty of Health and Environmental Science, Central University of Technology, Bloemfontein, South Africa
3 - Department of Agriculture, Faculty of Applied Science, Cape Peninsula University of Technology, Wellington Campus, Private Bag X8, Wellington 7654, Western Cape, South Africa
4 - Department of Livestock and Pasture Science, University of Fort Hare, Private Bag X1314, Alice 5700, Eastern Cape, South Africa
5 - Department of Agriculture, Faculty of Applied Science, Cape Peninsula University of Technology, Wellington Campus, Private Bag X8, Wellington 7654, Western Cape, South Africa

Received: 2023-04-17 Accepted : 2023-08-11 Published : 2023-12-01

Keywords: digestibility, Antioxidant, fatty acid, meat, Gas emission, Eggs,

Abstract :

Poultry farmers constantly source for alternative feed additives for feeding poultry birds to improve the quality and health benefits of their meat and egg. It is common knowledge that synthetic feed additives (antibiotic growth promoters) are accompanied by some limitations. These limitations include amongst others, the detrimental residual effects accompanying the consumption of the meat and egg products of poultry birds fed antibiotic growth promoters. Also, they cause resistance to some bacteria both in poultry and humans. Recently, increased efforts have been put into utilizing plant-based feed additives in the nutrition of poultry birds, due to their minimal toxicity concerns and holistic functional attributes. Pomegranate is an important fruit that cannot be overlooked among the spectrum of natural feed additives. The potential of pomegranate fruit peel to replace in-feed antibiotic growth promoters in poultry nutrition is quite promising. The current review provides an overview of the usefulness and potential utilization of pomegranate peel as a natural and alternative growth promoter in the nutrition of poultry birds. The pomegranate fruit peel promotes growth, stimulates immune responses, enhances the shelf-life of meat, improves egg quality, increases nutrient release. It also improves bone quality, and ensures the release of odorous gases from poultry manure, which may be linked to its rich antioxidant and bioactive phenol and tannin constituents. Tannin is one of the anti-nutrients that limits the performance of poultry when it is included in the diet. Despite huge benefits of pomegranate inclusion in poultry performance, its tannin content may be a source of worry and these concerns needs to be addressed through further research in order to maximize the full potentials of pomegranate. However, pomegranate shows potential to provide nourishment to poultry birds and positively enhance the health indicators of human consumers of the products (meat and egg).

References:

Abbas R.J., Al-Salhie K.C.K. and Al-Hummod S.K. (2017). The effect of using different levels of pomegranate (Punica granatum) peel powder on productive and physiological performance of Japanese quail (Coturnix coturnix japonica). Livest. Res. Rural Dev. 29(12), 1-7.

Abdel-Baset S., Ashour E.A., Abd El-Hack M.E. and El-Mekkawy M.M. (2020). Effect of different levels of pomegranate peel powder and probiotic supplementation on growth, carcass traits, blood serum metabolites, antioxidant status and meat quality of broilers. Anim. Biotechnol. 33(4), 690-700.

Abedi S., Hosseini-Vashan S.J., Farhangfar S.H. and Ghiasi S.E. (2019). Effect of pomegranate peel extract supplementation on performance traits, blood metabolites, small intestine morphology and meat stability in broiler chicks fed diet supplemented with canola oil. Anim. Prod. Res. 8(3), 13-24.

Abid M., Yaich H., Cheikhrouhou S., Khemakhem I., Bouaziz M., Attia H. and Ayadi M.A. (2017). Antioxidant properties and phenolic profile characterization by LC-MS/MS of selected Tunisian pomegranate peels. J. Food Sci. Technol. 54(9), 2890-2901.

Afaq F., Saleem M., Krueger C.G., Reed J.D. and Mukhtar H. (2005). Anthocyanin-and hydrolysable tannin-rich pomegranate fruit extract modulates MAPK and NF-kappaB pathways and inhibits skin tumorigenesis in CD-1 mice. Int. J. Cancer. 113, 423-433.

Ahmadipour B., Pat S. and Khajali F. (2018). The protective effect of pomegranate peel powder on pulmonary hypertension in broiler chickens. JSM Biomarkers 4(1), 1013-1021.

Ahmadipour B., Pat S., Abaszadeh S., Hassanpour H. and Khajali F. (2021). Pomegranate peel as a phytogenic in broiler chickens: Influence upon antioxidant, lipogenesis and hypotensive response. Vet. Med. Sci. 7(5), 1907-1913.

Ahmed S.T., Islam M., Bostami A.B.M.R., Mun H., Kim Y. and Yang C. (2015). Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by products. Food Chem. 188, 481-488.

Ahmed S.T. and Yang C.J. (2017). Effects of dietary Punica granatum L. by-products on performance, immunity, intestinal and fecal microbiology and odorous gas emissions from excreta in broilers. J. Poult. Sci. 54(2), 157-166.

Ahmed S., Wang N., Hafeez B.B., Cheruvu V.K. and Haqqi T.M. (2005). Punica granatum L. extract inhibits IL-1beta-induced expression of matrix metalloproteinases by inhibiting the activation of MAP kinases and NF-kappaB in human chondrocytes in vitro. J. Nutr. 135, 2096-2102.

Akhtar S., Ismail T., Fraternale D. and Sestili P. (2015). Pomegranate peel and peel extracts: Chemistry and food features. Food Chem. 174, 417-425.

Akuru E.A., Mpendulo C.T., Oyeagu C.E. and Nantapo C.W.T. (2021a). Pomegranate (Punica granatum L.) peel powder meal supplementation in broilers: effect on growth performance, digestibility, carcase and organ wrights, serum and some meat antioxidant enzyme biomarkers. Italian J. Anim. Sci. 20(1), 119-131.

Akuru E.A., Chukwuma C.I., Oyeagu C.E., Erukainure O.L., Mashile B., Setlhodi R., Mashele S.S., Makhafola T.J., Unuofin J.O., Abifarin T.O. and Mpendulo T.C. (2021b). Nutritional and phytochemical profile of pomegranate (Wonderful variety) peel and its effects on hepatic oxidative stress and metabolic alterations. J. Food Biochem. 46, e13913.

Alexandre E.M.C., Silva S., Santos S.A.O., Silvestre A.J.D., Duarte M.F., Saraiva J.A. and Pintado M. (2019). Antimicrobial activity of pomegranate peel extracts performed by high pressure and enzymatic assisted extraction. Food Res. Int. 115, 167-176.

Al-Ghousein S.S. and Al-Beitawi N. (2009). The effect of feeding crushed thyme (Thymus vulagris L.) on growth, blood constituents, gastrointestinal tract and carcass characteristics of broiler chickens. J. Poult. Sci. 46, 100-104.

Al-Qazzez M.F. (2014). The effect of using pomegranate peel extract on the quality and chemical characteristics for minced frozen spent chicken meat. Diyala Agric. Sci. J. 6(1), 1-10.

Al-Shammari K.I.A., Batkowska J. and Zamil S.J. (2019). Role of pomegranate peels and black pepper powder and their mixture in alleviating the oxidative stress in broiler chickens. Int. J. Poult. Sci. 18(3), 122-128.

Ang E.S., Pavlos N.J., Chai Y., Qi M., Cheng T.S., Steer J.H., Joyce D.A., Zheng M.H. and Qu J. (2009). Caffeic acid phenethyl ester an active component of honeybees propolis attenuates osteoclastogenesis and bone resorption via the suppression of TANKL-induced NF-kB and NFAT activity. J. Cell Physiol. 221, 642-649.

Antongiovanni M., Minieri S., Buccioni A. and Galigani I. (2015). Effect of a tannin from chestnut wood (Castanea sativa Miller) on cholesterol and fatty acids of eggs. European Symp. Qual. Poult. Meat. 22, 52-61.

Azimi H., Fallah-Tafti M., Khakshur A.A. and Abdollahi M. (2012). A review of phytotherapy of acne vulgaris: Perspective of new pharmacological treatments. Fitoterapia. 83(8), 1306-1317.

Bar-Ya’akov I., Tian L., Amir R. and Holland D. (2019). Primary metabolites, anthocyanins and hydrolysable tannins in the pomegranate fruit. Front. Plant Sci. 10, 1-19.

Bassoli B.K., Cassola P., Borba-Murad G.R., Constantin J., Salgueiro-Pagadigorria C.L., Bazotte R.B., dos Santos Ferreira da Silva R.S. and de Souza H.M. (2008). Chlorogenic acid reduces the plasma glucose peak in the oral glucose tolerance test: effects on hepatic glucose release and glycaemia. Cell Biochem. Funct. 26(3), 320-328.

Ben-Simhon Z., Judeinstein S., Trainin T., Harel-Beja R., Bar-Ya’akov I., Borochov-Neori H. and Holland D.A. (2015). White anthocyanin-less pomegranate (Punica granatum L.) caused by an insertion in the coding region of the leucoanthocyanidin dioxygenase (LDOX; ANS) gene. PLoS ONE. 10, e0142777.

Bialonska D., Kasimsetty S.G., Schrader K.K. and Ferreira D. (2009). The effect of pomegranate (Punica granatum L.) byproducts and ellagitannins on the growth of human gut bacteria. J. Agric. Food Chem. 57, 8344-8349.

Bilic-Šobot D., Kubale V., Škrlep M., Candek-Potokar M., Prevolnik Povše M., Fazarinc G. and Škorjanc D. (2016). Effect of hydrolysable tannins on intestinal morphology, proliferation and apoptosis in entire male pigs. Arch. Anim. Nutr. 70, 378-388.

Bostami A., Ahmed S., Islam M., Mun H., Ko S., Kim S. and Yang C. (2015). Growth performance, fecal noxious gas emission and economic efficacy in broilers fed fermented pomegranate byproducts as residue of fruit industry. Int. J. Adv. Res. 3, 102-114.

Brus M., Dolin J., CenCi C.A. and Skorjanc D. (2013). Effect of chestnut (Castanea sativa) wood tannins and organic acids on growth performance and faecal microbiota of pigs from 23 to 127 days of age. Belgian J. Agric. Sci. 19, 841-847.

Çetingül İ.S., Iqbal A., Bayram İ., Gültepe E.E., Uyarlar C. and Özçınar Ü. (2019). Effect of pomegranate molasses on egg quality traits during different storage time in laying hens. Kocatepe Vet. J. 12(2), 193-199

Chamorro S., Viveros A., Rebole A., Rica B.D., Arija I. and Brenes A. (2015). Influence of dietary enzyme addition on polyphenol utilization and meat lipid oxidation of chicks fed grape pomace. Food Res. Int. 73, 197-203.

Changxing L., Chenling M., Alagawany M., Jianhua L., Dongfang D., Gaichao W., Wenyin Z., Syed F.S., Arain M.A., Saeed M., Hassan F.U. and Chao S. (2018). Health benefits and potential applications of anthocyanins in poultry feed industry. World’s Poult. Sci. J. 74(02), 251-264.

Choct M. (2009). Managing gut health through nutrition. British Poult. Sci. 50(1), 9-15.

Chukwuebuka E. and Chinenye I.J. (2015). Biological functions and anti-nutritional effects of phytochemicals in living system. IOSR J. Pharm. Biol. Sci. 10(2), 10-19.

Chukwuma C.I., Mashele S.S. and Akuru E.A. (2020). Evaluation of the in vitro α-amylase inhibitory, antiglycation, and antioxidant properties of Punica granatum L. (pomegranate) fruit peel acetone extract and its effect on glucose uptake and oxidative stress in hepatocytes. J. Food Biochem. 44(5), 13-24.

Collins F.L., Irwin R., Bierhalter H., Schepper J. and Britton R.A. (2016). Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS One. 11(4), e0153180.

Delimont N.M., Haub M.D. and Lindshield B.L. (2017). The impact of tannin consumption on iron bioavailability and status: A narrative review. Curr. Dev. Nutr. 1(2), 1-12.

Destefanis G., Brugiapaglia G., Barge M.T. and Dal Molin E. (2007). Relationship between beef consumer tenderness perception and Warner–Bratzler shear force. Meat Sci. 78(3), 153-156.

Ebrahim R., Liang J.B., Jahromi M.F., Shokryazdan P., Ebrahimi M., Li C.W. and Goh Y.M. (2015). Effects of tannic acid on performance and fatty acid composition of breast muscle in broiler chickens under heat stress. Italian J. Anim. Sci. 14, 39-56.

Eid Y., Kirrella A.A., Tolba A., El-Deeb M., Sayed S., El-Sawy H.B., Shukry M. and Dawood M.A.O. (2021). Dietary pomegranate by-product alleviated the oxidative stress induced by dexamethasone in laying hens in the pre-peak period. Animals. 11(4), 1022-1032.

El-Hadary A.E. and Taha M. (2020). Pomegranate peel methanolic-extract improves the shelf-life of edible-oils under accelerated oxidation conditions. Food Sci. Nutr. 8(3), 1798-1811.

El-Nashi H.B., Abdel-Fattah A.A., Abdel Rahman N.R. and Abd El-Razik M.M. (2015). Quality characteristics of beef sausage containing pomegranate peels during refrigerated storage. Ann. Agric. Sci. 60(2), 403-412.

Estevez M. (2015). Oxidative damage to poultry: From farm to fork. Poult. Sci. 94(6), 1368-1378.

Farahat M.H., Abdallah F.M., Ali H.A. and Hernandez Santana A. (2017). Effect of dietary supplementation of grape seed extract on the growth performance, lipid profile, antioxidant status and immune response of broiler chickens. Animal. 11(5), 771-777.

Fawole O.A. and Opara U.L. (2013). Effects of maturity status on biochemical content, polyphenol composition and antioxidant capacity of pomegranate fruit arils (cv. ‘Bhagwa’). South African J. Botany. 85, 23-31.

Fawole O.A., Makunga N.P. and Opara U.L. (2012). Antibacterial, antioxidant and tyrosinase-inhibition activities of pomegranate fruit peel methanolic extract. BMC Complement. Altern. Med. 12, 200-211.

Ferket P.R., van Heugten E., van Kempen T.A.T.G. and Angel R. (2002). Nutritional strategies to reduce environmental emissions from nonruminants. J. Anim. Sci. 80(2), 168-182.

Franczyk-Zarow M., Kostogrys R.B., Szymczyk B., Jawien J., Gajda M., Cichocki T., Wojnar L., Chlopicki S. and Pisulewski P.M. (2008). Functional effects of eggs, naturally enriched with conjugated linoleic acid, on the blood lipid profile, development of atherosclerosis and composition of atherosclerotic plaque in apolipoprotein E and low-density lipoprotein receptor double-knockout mice (apoE/LDLR/). British J. Nutr. 99, 49-58.

Gambacorta L., Pinton P., Avantaggiato G., Oswald I.P. and Solfrizzo M. (2016). Grape pomace, an agricultural byproduct reducing mycotoxin absorption: In vivo assessment in pig using urinary biomarkers. J. Agric. Food Chem. 64(35), 6762-6771.

Garcês A., Afonso S.M.S., Chilundo A. and Jairoce C.T.S. (2013). Evaluation of different litter materials for broiler production in a hot and humid environment: 1. Litter characteristics and quality. J. Appl. Poult. Res. 22, 168-176.

Ghasemi-Sadabadi M., Ebrahimnezhad Y., Maheri-Sis N., Ghalehkandi G.J. and Shaddel-Teli A. (2021). Immune response and antioxidant status of broilers as influenced by oxidized vegetable oil and pomegranate peel. J. Anim. Sci. Technol. 63(5), 1034-1063.

Ghosh S., Chatterjee J.K., Chalkroborty B. and Kundu P. (2019). Estimation of beta carotene from fruit peel wastes by high performance thin layer chromatography. J. Pharmacog. Phytochem. 8(1), 2598-2600.

Ghosh S., Chatterjee P.N. and Chatterjee J. (2021). Supplementing pomegranate peel infusion in drinking water enhances antioxidant quality of broiler meat. Exp. Anim. Med. Res. 11(1), 131-134.

Ghosh S., Chatterjee P.N., Maity A., Mukherjee J., Batabyal S. and Chatterjee J.K. (2020). Effect of supplementing pomegranate peel infusion on body growth, feed efficiency, biochemical metabolites and antioxidant status of broiler chicken. Trop. Anim. Health Prod. 52(6), 3899-3905.

Goni I., Brenes A., Centeno C., Viveros A., Saura-Calixto F., Rebol E.A., Arija I. and Estevez R. (2007). Effect of dietary grape pomace and vitamin E on growth performance, nutrient digestibility, and susceptibility to meat lipid oxidation in chickens. Poult. Sci. 86(3), 508-516.

Gopi M., Dutta N., Puttanaik A.K, Jadhav S.E., Madhupriya V., Tyagi P.K. and Mohan J. (2020). Effect of polyphenol extract on performance, serum biochemistry, skin pigmentation and carcass characteristics in broiler chickens fed with different cereal sources under hot-humid conditions. Saudi J. Biol. Sci. 27(10), 2719-2726.

Graham S.A., Hall J., Sytsma K. and Shi S. (2005). Phylogenetic analysis of the Lythraceae based on four gene regions and morphology. Int. J. Plant Sci. 166(16), 995-1017.

Guerrero-Solano J.A., Osmar Antonio J.M., Tania Jiménez-C., Thania Alejandra U.H., Alejandro C.R., Elena G.O.H. and Mirandeli B. (2020). Punica protopunica Balf., the forgotten sister of the common pomegranate (Punica granatum L.): Features and medicinal properties-A review. Plants. 9, 1214-1224.

Gullon P., Astray G., Gullon B., Tomasevic I. and Lorenzo J.M. (2020). Pomegranate peel as suitable source of high-added value bioactives: Tailored functionalized meat products. Molecules. 25, 2859-2868.

Gungor E., Altop A., Erener G. and Coskun I. (2021). Effect of raw and fermented pomegranate pomace on performance, antioxidant activity, intestinal microbiota and morphology on broiler chickens. Arch. Anim. Nutr. 75(2), 355-375.

Halliwell B. and Gutteridge J.M.C. (2007). Free Radicals in Biology and Medicine. Clarendon Press, New York.

Hamad K.M. and Kareem K.Y. (2019). Growth performance, carcass quality and economics of production of Japanese quails fed with pomegranate peel powder. Int. Trans. J. Eng. Manage. Appl. Sci. Technol. 10(14), 1-7.

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 J. Agric. Sci. Technol. 312, 514-519.

Hassan I.A., Elzuber E.A. and Tinay H.A. (2003). Growth and apparent absorption of minerals in broiler chicks fed diets with low or high tannin content. Trop. Anim. Health Prod. 35, 189-196.

Hassan N.A., El-Halwagi A.A. and Sayed H.A. (2012). Phytochemicals, antioxidant and chemical properties of 32 pomegranate accessions growing in Egypt. World Appl. Sci. J. 16(8), 1065-1073.

Heckert R., Estevez I., Russek-Cohen E. and Pettit-Riley R. (2002). Effects of density and perch availability on the immune status of broilers. Poult. Sci. 81(4), 451-457.

Hidayat C., Irawan A., Jayanegara A., Sholikin M.M., Prihambodo T.R., Yanza Y.R., Wina E., Sadarman S., Krisnan R. and Isbandi I. (2021). Effect of dietary tannins on the performance, lymphoid organ weight, and amino acid ileal digestibility of broiler chickens: A meta-analysis. Vet. World. 14(6), 1405-1411.

Holland D., Hatib K. and Bar-Ya’akov I. (2009). Pomegranate: Botany, horticulture, breeding. Pp. 127-191 in Horticultural Reviews. J. Janick, Ed., John Wiley and Sons Inc., New York.

Honikel K.O. (2004). Conversion of muscle to meat/glycolysis. Pp. 314-318 in Encyclopedia of meat sciences. W.K. Jensen, C. Devine and M. Dikeman, Eds., Elsevier Academic Press, Oxford, United Kingdom.

Hosseini-Vashan S.J., Sharifian M., Piray A.H. and Fathi-Nasri M.H. (2020). Growth performance, carcass and blood traits, immunity, jejunal morphology and meat quality of heat stressed broiler chickens fed urea-treated pomegranate (Punica granatum L.) peel. Anim. Feed Sci. Technol. 267, 1-12.

Houshmand M., Hojati F. and Parsaie S. (2015). Dietary nutrient manipulation to improve the performance and tibia characteristics of broilers fed oak acorn (Quercus brantii L.). Brazilian J. Poult. Sci. 17, 17-24.

Hu Y., Wang Y., Li A., Wang Z., Zhang X., Yun T. and Yin Y. (2016). Effects of fermented rapeseed meal on antioxidant functions, serum biochemical parameters and intestinal morphology in broilers. Food Agric. Immunol. 27(2), 182-193.

Huang Q., Liu X., Zhao G., Hu T. and Wang Y. (2018). Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim. Nutr. 4(2), 137-150.

Hughes J.M., Oiseth S.K., Purslow P.P. and Warner R.D. (2014). A structural approach to understanding the interactions between colour, water-holding capacity and tenderness. Meat Sci. 98(3), 520-532.

International Plant Genetic Resources Institute (IPGRI) (2001). IPGRI Annual Report 2000. Rome, Italy

Jabber S.S., Khalil A.H. and Al-Gharawi J.K. (2021). Effect of adding different levels of pomegranate peel powder to feed on some biochemical blood traits of laying hens. Earth Environ. Sci. 923, 1-10.

Joseph M.M., Aravind S.R., Varghese S., Mini S. and Sreelekha T.T. (2012). Evaluation of antioxidant, antitumor and immunomodulatory properties of polysaccharide isolated from fruit rind of Punica granatum. Mol. Med. Rep. 5(2), 489-496.

Kamel E.M., Shafik B.M., Mamdouh M., Elraffay S. and Abdelfattah F.A.I. (2021). Effect of dietary pomegranate peel powder on productive traits, blood chemistry, economic efficiency and the expression of FSHR and LH-β genes in two strains of laying Japanese quails. Trop. Anim. Health Prod. 53(3), 358-369.

Kandylis P. and Kokkinomagoulos E. (2020). Food applications and potential health benefits of pomegranate and its derivatives. Foods. 9, 122-131.

Khalil A.A., Khan M.R., Shabbir M.A. and Rahman K.U. (2017). Comparison of antioxidative potential and punicalagin content of pomegranate peels. J. Anim. Plant Sci. 27(2), 522-527.

Khan R.U., Nikousefat Z., Tufarelli V. and Naz S. (2012). Garlic (Allium sativum) supplementation in poultry diets: Effect on production and physiology. Worlds Poultr. Sci. J. 68(3), 417-424.

Khorrami P., Gholami-Ahangaran M. and Moghtadaei-Khorasgani E. (2022). The efficacy of pomegranate peel extract on Eimeria shedding and growth indices in experimental coccidiosis in broiler chickens. Vet. Med. Sci. 12, 1-7.

Kim J.H., Hwangbo J., Choi N.J., Park H.G., Yoon D.H., Park E.W., Lee S.H., Park B.K. and Kim Y.J. (2007). Effect of dietary supplementation with conjugated linoleic acid, with oleic, linoleic, or linolenic acid, on egg quality characteristics and fat accumulation in the egg yolk. Poult. Sci. 86, 1180-1186.

Kishawy A.T., Amer Y.S.A., Abd El-Hack M.E., Saadeldin I.M. and Swelum A.A. (2019). The impact of dietary linseed oil and pomegranate peel extract on broiler growth, carcass traits, serum lipid profile, and meat fatty acid, phenol, and flavonoid contents. Asian Australasian J. Anim. Sci. 32(8), 1161-1171.

Kostogrys R.B., Filipiak-Florkiewicz A., Deren K., Drahun A., Czyzy˙nska-Cicho N.I., Cieslik E., Szymczyk B. and Franczyk-Zarów M. (2017). Effect of dietary pomegranate seed oil on laying hen performance and physicochemical properties of eggs, Food Chem. 221, 1096-1103.

Krauss R.M., Eckel R.H., Howard B., Appel L.J., Daniels S.R. and Deckelbaum R.J. (2001). AHA dietary guidelines. Revision 2000: a statement for healthcare professionals from the nutrition committee of the American heart association. Circulation. 102(18), 2284-2299.

Kroliczewska B., Mista D., Kroliczewski J., Zawadzki W., Kubaszewski R., Wincewicz E. and Szopa J. (2017). A new genotype of flax (Linum usitassiumum L.) with decreased susceptibility to fat oxidation: Consequences to haematological and biochemical profiles of blood indices. J. Sci. Food Agric. 97(1), 165-171.

Kumar N. and Neeraj S.K. (2018). Functional properties of pomegranate (Punica granatum L.). Pharma Innov. J. 7(10), 71-81.

Labsi M., Khelifi L., Mezioug L.D., Soufli I. and Touli-Boukoffa C. (2016). Antihydatic and immunomodulatory effects of Punica granatum peel aqueous extract in a murine model of echinococcosis. Asian Pac. J. Trop. Med. 9(3), 211-220.

Larrosa M., Gonzalez-Sarrias A., Yanez-Gascon M.J., Selma M.V., Azorin-Ortuno M., Toti S., Tomas-Barberan F., Dolara P. and Espin J.C. (2009). Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J. Nutr. Biochem. 21(8), 717-25.

Lawrie R. and Ledward D. (2006). Lawrie's Meat Science. Woodhead Publishing Limited. Cambridge England, United Kingdom.

Le P.D., Aarnink A.J.A., Ogink N.W.N., Becker P.M. and Verstegen M.W.A. (2005). Odour from animal production facilities: its relationship to diet. Nutr. Res. Rev. 18, 3-30.

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 Chem. 2(96), 254-260.

Lioliopoulou S., Papadopoulos G.A., Giannenas I., Vasilopoulou K., Squires C., Fortomaris P. and Mantzouridou F.T. (2023). Effects of dietary supplementation of pomegranate peel with xylanase on egg quality and antioxidant parameters in laying hens. Antioxidants. 12, 208-217.

Liu H.W., Zhou D., Tong J. and Vaddella V. (2012). Influence of chestnut tannins on welfare, carcass characteristics, meat quality, and lipid oxidation in rabbits under high ambient temperature. Meat Sci. 90, 164-169.

Lye C. (2008). Pomegranate: Preliminary Assessment of the Potential for an Australian Industry. Rural Industries Research and Development Corporation of Australian Government Publication No. 08/153, P17.

Maertens L. and Štruklec M. (2006). Technical note: Preliminary results with a tannin extract on the performance and mortality of growing rabbits in an enteropathy infected environment. World Rabbit Sci. 14, 189-192.

Mahmoud M., Abo G., Mohamed F.E., Ayman E.T., Mohamed E.A., Mahmoud A., Badreldin M.A., Mona M.E. and Karim E. (2020). Effect of housing system and Rosemary and Cinnamon essential oils on layers performance, egg quality, haematological traits, blood chemistry, immunity, and antioxidant. Animals. 10(12), 245-256.

Manterys A., Franczyk Z.M. and Czyzynska C.I. (2016). Haematological parameters, serum lipid profile, liver function and fatty acid profile of broiler chickens fed on diets supplemented with pomegranate seed oil and linseed oil. British Poult. Sci. 57(6), 771-779.

Marzoni M., Castillo A., Franzoni A., Nery J., Fortina R., Romboli I. and Schiavone A. (2020). Effects of dietary quebracho tannin on performance traits and parasite load in an Italian slow-growing chicken (White Livorno breed). Animals. 10(4), 1-11.

Mbikay M. (2012). Therapeutic potential of Moringa oleifera leaves in chronic hyperglycemia and dyslipidemia-A review. Front. Pharmacol. 3, 24-36.

McRae J.M. and Kennedy J.A. (2011). Wine and grape tannin interactions with salivary proteins and their impact on astringency: A review of current research. Molecules. 16(3), 2348-2364.

Melgarejo P., Nunez-Gomez D., Legua P. and Martinez-Nicolas J.J. (2020). Pomegranate (Punica granatum L.) a dry pericarp fruit with fleshy seeds. Trends Food Sci. Technol. 102, 232-236.

Middha S.K., Usha T. and Pande V. (2013). HPLC evaluation of phenolic profile, nutritive content, and antioxidant capacity of extracts obtained from Punica granatum fruit peel. Adv. Pharmacol. Sci. 2013, 1-6.

Mir N.A., Rafiq A., Kumar F., Singh V. and Shukla V. (2017). Determinants of broiler chicken meat quality and factors affecting them: a review. J. Food Sci. Technol. 54(10), 2997-3009.

Moyle J.R., Burke J.M., Fanatico A., Mosjidis J.A., Spencer T., Arsi K., Reyes-Herrera I., Woo-Ming A., Donoghue D.J. and Donoghue A.M. (2012). Palatability of tannin-rich sericea lespedeza fed to broilers. J. Appl. Poult. Res. 21(4), 891-896.

Murugesan G.R., Syed B., Haldar S. and Pender C. (2015). Corrigendum: Pytogenic feed additives as an alternative to antibiotic growth promoters in broiler chickens. Front. Vet. Sci. 2, 37-45.

Mutlu S.I. and Güler T. (2021). The effect of ellagic acid on performance, digestibility, egg quality, cecal bacterial flora, antioxidant activity, and some blood parameters in laying quails reared at different temperatures. Turkish J. Vet. Anim. Sci. 45, 101-112.

Okuda T. and Ito H. (2011). Tannins of constant structure in medicinal and food plants-hydrolyzable tannins and polyphenols related to tannins. Molecules. 16(3), 2191-2217.

Oloruntola O.D., Ayodele S.O., Agbede J.O. and Oloruntola D.A. (2016). Effect of feeding broiler chickens with diets containing Alchornea cordifolia leaf meal and enzyme supplementation. Arch. Zootec. 65(252), 489-498.

Omer H.A.A., Abdel-Magid S.S. and Awadalla I.M. (2019). Nutritional and chemical evaluation of dried pomegranate (Punica granatum L.) peels and studying the impact of level of inclusion in ration formulation on productive performance of growing ossimi lambs. Bullet. Natl. Res.Centre. 43, 182-193.

Owens C.M., Alvarado C.Z. and Sams A.R. (2010). Poultry Meat Processing. CRC Press, Danvers, USA.

Oyeagu C.E., Mlambo V. and Lewu F.B. (2023). Histomorphometric traits, microbiota, nutrient digestibility, growth performance, carcass traits and meat quality parameters of chickens fed diets supplemented with different levels of Bacillus protease. J. Appl. Anim. Res. 51(1), 137-155.

Pagliarulo C., De Vito V., Picariello G., Colicchio R., Gabiria P., Salvatore P. and Volpe M.G. (2016). Inhibitory Effect of pomegranate (Punica granatum L.) polyphenol extracts on the bacterial growth and survival of clinical isolates of pathogenic Staphylococcus aureus and Escherichia coli. Food Chem. 190, 824-831.

Park S.H., Jung-Lye K., Eun-Sook L., Seon-Young H., Ju-Hyun G., Min-Kyung K. and Young-Hee K. (2011). Dietary ellagic acid attenuates oxidized LDL uptake and stimulates cholesterol efflux in murine macrophages. J. Nutr. 141(11), 1931-1937.

Penido M.G. and Alon U.S. (2012). Phosphate homeostasis and its role in bone health. Paediatr. Nephrol. 27(11), 2039-2048.

Pérez-Vicente A., Gil-Izquierdo A. and Cristina G.V. (2002). In vitro gastrointestinal digestion study of pomegranate juice phenolic compounds, anthocyanins, and vitamin C. J. Agric. Food Chem. 50(8), 2308-2312.

Perricone V., Comi M., Rebucci R., Agazzi A., Savoin G. and Bontempo V. (2020). Green tea and pomegranate extract administered during critical moments of the production cycle improves blood antiradical activity and alters cecal microbial ecology of broiler chicken. Animals. 10, 75-83.

Pirzadeh M., Caporaso N., Rauf A., Shariati M.A., Yessimbekov Z., Khan M.U., Imran M. and Mubarak M.S. (2020). Pomegranate as a source of bioactive constituents: A review on their characterization, properties and applications. Crit. Rev. Food Sci. Nutr. 61(6), 982-999.

Pomegranate Association of South Africa (POMASA). (2018). Pomegranate Industry Overview. WebMD. http://www.hortgro.co.za/portfolio/pomegranates Accessed Mar. 2018.

Powell J.M., Aguerre M.J. and Wattiaux M.A. (2011). Tannin extracts abate ammonia emissions from simulated dairy barn floors. J. Environ. Qual. 40(3), 907-914.

Prihambodo T.R., Sholikin M.M., Qomariyah N., Jayanegara A., Batubara I., Utomo D.B. and Nahrowi N. (2021). Effects of dietary flavonoids on performance, blood constituents, carcass composition and small intestinal morphology of broilers: A meta-analysis. Anim. Biosci. 34(3), 434-442.

Raes K., De Smet S. and Demeyer D. (2004). Effect of dietary fatty acids on incorporation of long chain polyunsaturated fatty acids and conjugated linoleic acid in lamb, beef, and pork meat: A review. Anim. Feed Sci. Technol. 113(1), 199-221.

Rahman A., Eren G.E., Uyarlar C., Cetıngul S., Iqbal A. and Bayram I. (2017). Effect of mentha piperita (Peppermint) extract and its juice on egg quality traits during different storage time in laying hens. Kocatepe Vet. J. 10(101), 14-20.

Rajani J., Karimi Torshizi M.A. and Rahimi S.H. (2011). Control of ascites mortality and improved performance and meat shelf-life in broilers using feed adjuncts with presumed antioxidant activity. Anim. Feed Sci. Technol. 170(3), 239-245.

Rama Rao S.V., Raju M.V.L.N., Prakash B., Ullengala R. and Reddy E.P.K. (2019). Effect of supplementing Moringa (Moringa oleifera) leaf meal and pomegranate (Punica granatum L.) peel meal on performance, carcass attributes, immune and antioxidant responses in broiler chickens. Anim. Prod. Sci. 59(2), 288-294.

Ravindran G., Ravindran V. and Bryden W.L. (2006). Total and ileal digestible tryptophan contents of feedstuffs for broiler chickens. J. Sci. Food Agric. 86, 1132-1137.

Reddy B.U., Mullick R., Kumar A., Sudha G., Srinivasan N. and Saumitra D. (2014). Small molecule inhibitors of HCV replication from pomegranate. Sci. Rep. 4, 5411-5413.

Redondo L.M., Chacana P.A., Dominguez J.E. and Fernandez M.E. (2014). Perspectives in the use of tannins as alternative to antimicrobial growth promoter factors in poultry. Front. Microbiol. 5, 118-128.

Rezvani M.R. and Rahimi S. (2017). Effects of adding pomegranate peel extract and commercial antioxidant to diets on performance, nutrient digestibility, gastrointestinal microflora and antibody titer of broilers. J. Vet. Res. 72(2), 147-156.

Romeo F.V., Ballistreri G., Fabroni S., Pangallo S., Li Destri N.M.G., Schena L. and Rapisarda P. (2015). Chemical characterization of different sumac and pomegranate extracts effective against Botrytis cinerea rots. Molecules. 20, 11941-11958.

Saki A.A., Rabet M., Zamani P. and Yousefi A. (2014). The effects of different levels of pomegranate seed pulp with multienzyme on performance, egg quality and serum antioxidant in laying hens. Iranian J. Appl. Anim. Sci. 4, 803-808.

Saki A.A., Shamsollah T. and Ashoori A. (2019). Egg iron enrichment in response to various levels of pomegranate by-product in laying hen diet. Iranian J. Appl. Anim. Sci. 9, 747-754.

Saleh H., Golian A., Kermanshahi H. and Mirakzchi M.T. (2017). Effects of dietary a-tocopherol acetate, pomegranate peel and pomegranate peel extract on phenolic content, fatty aid composition and meat quality of broiler chickens. J. Appl. Anim. Res. 45, 629-636.

Saleh H., Golian A., Kermanshahi H. and Mirakzehi M.T. (2018). Antioxidant status and thigh meat quality of broiler chickens fed diet supplemented with α-tocopherolacetate, pomegranate pomace and pomegranate pomace extract. Italian J. Anim. Sci. 17, 386-395.

Sarica S. and Urkmez D. (2016). The use of grape seed olive leaf and pomegranate peel extracts as alternative natural antimicrobial feed additive in broiler diets. European Poult. Sci. 80, 1-13.

Schwarz M., Rodrıguez M., Martınez C., Bosquet V., Guilen D.A. and Barroso C.C. (2009). Antioxidant activity of Brandy de Jerez and other aged distillates and correlation with their polyphenolic content. Food Chem. 116(1), 29-33.

Seeram N.P., Zhang Y., McKeever R., Henning S.M., Lee R.P., Suchard M.A., Li Z., Chen S., Thames G. and Zerlin A. (2008). Pomegranate juice and extracts provide similar levels of plasma and urinary ellagitannin metabolites in human subjects. J. Med. Food. 11, 390-394.

Senay S., Islim P. and Tugay A. (2019). Supplementation of natural antioxidants to reduced crude protein diets for Japanese quails exposed to heat stress. Brazilian J. Poult. Sci. 21(1), 1-14.

Shang H., Song H., Jiang Y., Ding G., Xing Y., Niu S., Wu B. and Wang L. (2014). Influence of fermentation concentrate of Hericium caput-medusae (Bull: Fr.) Pers on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Technol. 198, 166-175.

Sharifian M., Hosseini-Vashan S.J., Fathi Nasri M.H. and Perai A.H. (2019). Pomegranate peel extract for broiler chickens under heat stress: Its influence on growth performance, carcass traits, blood metabolites, immunity, jejunal morphology, and meat quality. Livest. Sci. 227, 22-28.

Shaw A.L., Blake J.P. and Moran E.T. (2010). Effects of flesh attachment on bone breaking and of phosphorus concentration on performance of broilers hatched from young and old flocks. Poult. Sci. 89(2), 295-302.

Singh B., Singh J.P., Kaur A. and Singh N. (2018). Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: A review. Food Chem. 261, 75-86.

Siri‐Tarino P.W., Qi S., Hu F.B. and Krauss R.M. (2010). Meta‐analysis of prospective cohort studies evaluating the association of saturated fat with cardiovascular disease. American J. Clin. Nutr. 91(3), 535-546.

Somparn N., Saenthaweeuk S., Naowaboot J., Thaeomor A. and Kukongviriyapan V. (2018). Effect of lemongrass water extract supplementation on atherogenic index and antioxidant status in rats. Acta Pharaceut. 68(2), 185-197.

Sorrenti V., Randazzo C.L., Caggia C., Ballistreri G., Romeo F.V., Fabroni S., Timpanaro N., Raffaele M. and Vanella L. (2019). Beneficial effects of pomegranate peel extract and probiotics on pre-adipocyte differentiation. Front. Microbiol. 10, 660-669.

Spilmont M., Leotoing L., Davicco M.J., Lebecque P., Miot-Noirault E., Pilet P., Wittrant Y. and Coxam V. (2015). Pomegranate peel extract prevents bone loss in a preclinical model of osteoporosis and stimulates osteoblastic differentiation in vitro. Nutrients. 7(11), 9265-9284.

Such N., Mezőlaki Á., Rawash M.A., Tewelde K.G., Pál L., Wágner L., Schermann K., Poór J. and Dublecz K. (2023). Diet composition and using probiotics or symbiotics can modify the urinary and faecal nitrogen ratio of broiler chicken's excreta and also the dynamics of in vitro ammonia emission. Animals. 13(3), 332-341.

Sultana M., Verma P.K., Raina R., Prawez S. and Dar M.A. (2012). Quantitative analysis of total phenolic, flavonoids and tannin contents in acetone and n-hexane extracts of Ageratum conyzoides. Int. J. Chem. Res. 4(3), 996-999.

Swiatkiewicz S., Arczewska-Wlosek A., Krawczyk J., Szczurek W., Puchala M. and Jozefiak K. (2018). Effect of selected feed additives on egg performance and eggshell quality in laying hens fed a diet with standard or decreased calcium content. Ann. Anim. Sci. 18(1), 167-183.

Talaty P.N., Katanbaf M.N. and Hester P.Y. (2009). Variability in bone mineralization among purebred lines of meat-type chickens. Poult. Sci. 88(9), 1963-1974.

Talkhonche M.Z. and Moghtadaiee E. (2019). Effect of pomegranate peel extract on oocyte shedding and intestinal pathology in experimental coccidiosis of broiler chickens. J. Med. Herbs. 10(2), 7-13.

Tandiang D.M., Diop M.T., Dieng A., Yoda G.M.L., Cisse N. and Nassim M. (2014). Effect of corn substitution by sorghum grain with low tannin content on broilers production: Animal performance, nutrient digestibility and carcass characteristics. Int. J. Poult. Sci. 13(10), 568-574.

Tapiwa K.A. (2019). Polyphenols in sorghum, their effects on broilers and methods of reducing their effects: A Review. Biomed. J. Sci. Tech. Res. 19, 14058-14061.

Thema K., Mlambo V., Snyman N. and Mnisi C.M. (2019). Evaluating alternatives to zinc-bacitracin antibiotic growth promoter in broilers: Physiology and meat quality responses. Animals. 9(12), 1160-1171.

Thomas A.R., Gondoza H., Hoffman L.C., Oosthuizen V. and Naudé R.J. (2004). The roles of proteasome, and cathepsins B, L, H and D, in ostrich meat tenderisation. Meat Sci. 67, 113-120.

Thorat A.V., Kardile N.B. and Wagh R.P. (2018). Physio-chemical and sensory analysis of noodles fortified with cowpea and pomegranate peel powder. Int. J. Chem. Stud. 6(4), 3051-3054.

Tothova C., Sesztakova E., Bielik B. and Nagy O. (2019). Changes of total protein and protein fractions in broiler chickens during the fattening period. Vet. World. 12(4), 598-604.

Turrini E., Ferruzzi L. and Fimognari C. (2015). Potential effects of pomegranate polyphenols in cancer prevention and therapy. Oxidative Med. Cell. Long. 2015, 1-8.

Ullah N., Ali J., Khan F.A., Khurram M., Hussain A., Ur-Rahman I., Siddique Z.U. and Shafqatullah R.I. (2012). Proximate composition, minerals content, antibacterial and antifungal activity evaluation of pomegranate (Punica granatum L.) peels powder. Middle East J. Sci. Res. 11(3), 396-401.

United States Department of Agriculture (USDA). (2014). Plants. Punica granatum L. (pomegranate). United States Department of Agriculture. Natural resources conservation ervice. https://plants.usda.gov/home/plantProfile?symbol=PUGR2 Accessed Jan. 2014.

Venkitasamy C., Zhao L., Zhang R. and Pan Z. (2019). Pomegranate. Pp. 181-216 in Integrated Processing Technologies for Food and Agricultural By-Products. Z. Pan, R. Zhang and S. Zicari, Eds., Academic Press, Massachusetts, USA.

Viuda-Martos M., Fernandez-Lopez L. and Perez-Alvarez J.A. (2010b). Pomegranate and its many functional components as related to human health: A review. Comprehen. Rev. Food Sci. Food Saf. 9(6), 635-654.

Wang C., Han F., Jia P., Zhu Q., Tong Z., Lin T., Wang C., Liu Z., Peng Z., Wang G., Meng J., Zheng-Xiu A., Zhang Y., Ji-Guang D. and Hsing-Cheng H. (2021). Emissions, measurement, and control of odor in livestock farms: A review. Sci. Total Environ. 776, 1-11.

Wang D., Ozen C., Ibrahim M., Abu-Reidah I.M., Chigurupati S., Patra J.K., Horbanczuk J.O., Jozwik A., Tzvetkov N.T., Uhrin P. and Atanasov A.G. (2018). Vasculoprotective effects of pomegranate (Punica granatum L.). Front. Pharmacol. 9, 544-553.

Wang Z., Pan Z., Ma H. and Atungulu G.G. (2011). Extract of phenolics from pomegranate peels. Open Food Sci. J. 5, 17-25.

Whitehead T.R., Cotta M.A. and Spence C. (2012). Application of Tannins to Reduce Odor Emissions from Animal Waste. US Patent US8137660B1.

Williamson G. (2017). The role of polyphenols in modern nutria-tion. Nutr. Bullet. 42, 226-235.

Windisch W., Schedle K., Plitzner C. and Kroismayr A. (2008). Use of phytogenic products as feed additives for swine and poultry. J. Anim. Sci. 86(14), 140-148.

Xing T., Gao F., Tume R.K., Zhou G. and Xu X. (2019). Stress effects on meat quality: A mechanistic perspective. Compr. Rev. Food Sci. Food Saf. 18(2), 1-22.

Xiong Y. L. (2000). Protein oxidation and implications for muscle food quality. Pp. 85-111 in Antioxidants in Muscle Foods: Nutritional Strategies to Improve Quality. E. Decker, C. Faustman and C.J. Lopez-Bote, Eds., John Wiley and Sons, New York.

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 Hydroxytoluene on some productive, physiological, and immunological parameters of Japanese Quail. Egyptian J. Anim. Prod. 52, 105-113.

Zaib U.R., Ahsan U.I.H., Naasra A., Mohamed E.A.E., Muhammad S., Shahid U.R., Chunchun M., Mahmoud A., Maryam S., Kuldeep D. and Chan D. (2016). Growth performance, intestinal histomorphology, blood haematology and serum metabolites of broiler chickens fed diet supplemented with graded levels of acetic acid. Int. J. Pharmacol. 12(8), 874-883.

Zhao X., Yuan Z., Fang Y., Yin Y. and Feng L. (2013). Characterization and evaluation of major anthocyanins in pomegranate (Punica granatum L.) peel of different cultivars and their development phases. 236(1), 109-117.