Review Article A NATURAL FEED ADDITIVE PHYTOBIOTIC, POMEGRANATE (PUNICA GRANATUM L.), AND THE HEALTH STATUS OF POULTRY The addition of antibiotic growth promotors in poultry diets results in a development of resistant bacterial strains and accumulation of drug residues in the meat and eggs. The new trend in poultry industry is the dietary addition of natural feed additives including phytobiotics. Pomegranate (Punica granatum L.) is a natural cheap feed source that has been extensively used in the livestock production. In poultry production system, pomegranate by-products such as peel powder or extract, seed oil, or juice showed high nutritional values, several health benefits, and good economic profits. Pomegranate displays a growth promoting effect and an enhancement of carcass traits of broilers, along with an improvement of the egg production traits parameters. Moreover, dietary pomegranate by-products showed a potential antioxidant and antimicrobial effects on the treated birds. Modulation of both humeral and cell mediated immune response, hypo-lipidemia, as well as enhancement of liver functions have been proved following dietary treatment with different pomegranate by-products. Therefore, this review article was designed to present the different effects of dietary pomegranate by-products on the production indices of broilers and layers, the antioxidant, antimicrobial, and immune status, as well as the blood parameters. https://macvetrev.mk/LoadArticlePdf/361 2023-7-12 113 128 https://doi.org/10.2478/macvetrev-2023-0022 antioxidant chicken immunity performance Punica granatum L Wafaa A. Abd El-Ghany wafaa.soliman@cu.edu.eg false 1 Poultry Diseases Department, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt LEAD_AUTHOR Abd El-Ghany, W.A. (2020). Paraprobiotics and postbiotics: contemporary and promising natural antibiotics alternatives and their applications in the poultry field. Open Vet J. 10(3): 323-330. PMid:33282704 PMCid:PMC7703615 1 https://doi.org/10.4314/ovj.v10i3.11 Abd El-Ghany, W.A. (2020). Microalgae in poultry field: a comprehensive perspectives. Adv Anim Vet Sci. 8(9): 888-897 2 https://doi.org/10.17582/journal.aavs/2020/8.9.888.897 Abd El-Ghany, W.A. (2021). Uses of immunoglobulins as an antimicrobials alternative in Veterinary Medicine. World Vet J. 11(1): 16-22. 3 https://doi.org/10.54203/scil.2021.wvj2 Abd El-Ghany, W.A., Abdel-Latif, M.A., Hosny, F., Alatfeehy, N.M., Noreldin, A.E., Quesnell, R.R., Chapman, R., et al. (2022). Comparative efficacy of postbiotic, probiotic, and antibiotic against necrotic enteritis in broiler chickens. Poult Sci. 101(8): 101988. PMid:35809347 PMCid:PMC9272375 4 https://doi.org/10.1016/j.psj.2022.101988 Abd El Ghany, W.A., Fouad, H., Quesnell, R., Sakai, L. (2022). The effect of a postbiotic produced by stabilized non-viable Lactobacilli on the health, growth performance, immunity, and gut status of colisepticaemic broiler chickens. Trop Anim Health Prod. 54(5): 286. PMid:36083376 PMCid:PMC9463281 5 https://doi.org/10.1007/s11250-022-03300-w Hady, M.M., Zaki, M.M., Abd El-Ghany, W.A., Korany, R.M.S. (2016). Assessment of the broilers performance, gut healthiness and carcass characteristics in response to dietary inclusion of dried coriander, turmeric and thyme. Int J Environ Agric Res. 2(6): 153-159. 6 Zaki, M.M., Abd El-Ghany, W.A., Hady, M.M., Korany, R.M.S. (2016). Effect of certain phytobiotics on the immune response of Newcastle disease vaccinated broiler chickens. Asian J Poult Sci. 10(3): 134-140. 7 https://doi.org/10.3923/ajpsaj.2016.134.140 Abd El-Ghany, W.A. (2020). Phytobiotics in poultry industry as growth promoters, antimicrobials and immunomodulators - a review. J World Poult Res. 10(4): 571-579. 8 https://doi.org/10.36380/jwpr.2020.65 Abd El-Ghany, W.A., Eraky, R. (2020). Influence of dietary Moringa oleifera on broilers performance,intestinal microbial population and humoral immune competence. J Hellenic Vet Med Soc. 70(4): 1805-1810. 9 https://doi.org/10.12681/jhvms.22224 Abd El-Ghany, W.A. (2020). A Review on the use of Azolla species in poultry production. J World Poult Res. 10(2): 378-384. 10 https://doi.org/10.36380/jwpr.2020.44 Abd El-Ghany, W.A. (2022). The potential uses of silymarin, a milk thistle (Silybum marianum) derivative, in poultry production system. Online J Anim Feed Res. 12(1): 46-52. 11 https://doi.org/10.51227/ojafr.2022.7 Abd El-Ghany, W.A., Babazadeh, D. (2022). Betaine: a potential nutritional metabolite in the poultry industry. Animals 12(19): 2624. PMid:36230366 PMCid:PMC9559486 12 https://doi.org/10.3390/ani12192624 Ross, I.A. (1999). Medicinal plants of world. Totowa, New Jersey: Humana press 13 Ercisli, S., Gadze, J., Agar, G., Yildirim, N., Hizarci, Y. (2011). Genetic relationships among wild pomegranate (Punica granatum) genotypes from Coruh Valley in Turkey. Genet Mol Res. 10(1): 459-464. PMid:21425096 14 https://doi.org/10.4238/vol10-1gmr1155 Pienaar, L. (2021). The Economic contribution of South Africa’s pomegranate industry. South Africa: Western Cape Department of Agriculture 15 Sharma, J., Ramchandra, K.K., Sharma, D., Meshram, D.T., Maity, A.N.N. (2014). Pomegranate: cultivation marketing and utilization. 16 Ismail, T., Sestili, P., Akhar, S. (2012). Pomegranate peel and fruit extracts: a review of potential anti-inflammatory and anti-infective effects. J Ethnopharmacol. 143(2): 397-405. PMid:22820239 17 https://doi.org/10.1016/j.jep.2012.07.004 Naveena, B.M., Sen, A.R., Vaithiyanathan, S., Babji, Y., Kondaiah, N. (2008). Comparative efficacy of pomegranate juice, pomegranate rind powder extract and BHT as antioxidants in cooked chicken patties. Meat Sci. 80(4): 1304-1308. PMid:22063872 18 https://doi.org/10.1016/j.meatsci.2008.06.005 Kandylis, P., Kokkinomagoulos, E. (2020). Food applications and potential health benefits of pomegranate and its derivatives. Foods. 9(2): 122. PMid:31979390 PMCid:PMC7074153 19 https://doi.org/10.3390/foods9020122 Akhtar, S., Ismail, T., Fraternale, D., Sestili, P. (2015). Pomegranate peel and peel extracts: Chemistry and food features. Food Chem. 174, 417-425. PMid:25529700 20 https://doi.org/10.1016/j.foodchem.2014.11.035 Ahmed, S.T., Islam, M.M., Bostami, A.B., Mun, H.S., Kim, Y.J., Yang, C.J. (2015). Meat composition, fatty acid profle and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by products. Food Chem. 188(1-2): 481-488. PMid:26041221 21 https://doi.org/10.1016/j.foodchem.2015.04.140 Ghasemi-Sadabadi, M., Ebrahimnezhad, Y., Maheri-Sis, N., Ghalehkandi, J.G., 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. PMid:34796346 PMCid:PMC8564296 22 https://doi.org/10.5187/jast.2021.e99 Ghasemi Sadabadi, M., Ebrahimnezhad, Y., Maheri-Sis, N., Shaddel-Teli, A., Ghalehkandi J.G., Veldkamp, T. (2022). Effects of supplementation of pomegranate processing by products and waste cooking oils as alternative feed resources in broiler nutrition. Sci Rep. 12, 21216. PMid:36481691 PMCid:PMC9731951 23 https://doi.org/10.1038/s41598-022-25761-7 Reddy, M.K., Gupta, S.K., Jacob, M.R., Khan, S.I., Ferreira, D. (2007). Antioxidant, antimalarial and antimicrobial activities of tannin-rich fractions, ellagitannins and phenolic acids from Punica granatum L. Planta Med. 73(5): 461-467. PMid:17566148 24 https://doi.org/10.1055/s-2007-967167 Ghasemi-Sadabadi, M., Ebrahimnezhad, Y., Maheri-Sis, N., Shaddel Teli, A., Ghiasi Ghalehkandi, J., Veldkamp, T. (2021). Supplementation of pomegranate processing waste and waste soybean cooking oil as an alternative feed resource with vitamin E in broiler nutrition: Effects on productive performance, meat quality and meat fatty acid composition. Arch Anim Nutr. 75(5): 355-375. PMid:34461782 25 https://doi.org/10.1080/1745039X.2021.1965414 Elsebai, A., El-Tahawy, W.S., El-Attar, F.M., ELnaggar, A.S. (2022). Effect of dietary inclusion of pomergranate peel powder (Punica grantum) on growth performance and some physiological parameters of broiler chicks. J Agric Environ Sci. 21(2): 19-44. 26 https://doi.org/10.21608/jaesj.2022.159602.1017 Eid, Y., Kirrella, A.A., Tolba, A., El-Deeb, M., Sayed, S., El-Sawy, H.B., Shukry, M., 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. PMid:33916329 PMCid:PMC8066172 27 https://doi.org/10.3390/ani11041022 Vasilopoulos, S., Dokou, S., Papadopoulos, G.A., Savvidou, S., Christaki, S., Kyriakoudi, A., Dotas, V., et al. (2022). Dietary supplementation with pomegranate and onion aqueous and cyclodextrin encapsulated extracts affects broiler performance parameters, welfare and meat characteristics. Poultry 1(2): 74-93. 28 https://doi.org/10.3390/poultry1020008 Kishawy, A.T., Omar, A.E., Gomaa, A.M. (2018). Growth performance and immunity of broilers fed rancid oil diets that supplemented with pomegranate peel extract and sage oil. Jpn J Vet Res. 64(Suppl 2): S31-S38. 29 Akarca, G., Başpinar, E. (2019). Determination of pomegranate peel and seed extracted in different solvents for antimicrobial effect. Turk J Agric Food Sci Technol. 7(1): 46-53. 30 Benchagra, L., Berrougui, H., Islam, M.O., Ramchoun, M., Boulbaroud, S., Hajjaji, A., Fulop, T., et al. (2021). Antioxidant effect of Moroccan pomegranate (Punica granatum l. sefri variety) extracts rich in punicalagin against the oxidative stress process. Foods 10(9): 2219. PMid:34574329 PMCid:PMC8469689 31 https://doi.org/10.3390/foods10092219 Ahmadipour, B., Pat, S., Khajali, F. (2018). The protective effect of pomegranate peel powder on pulmonary hypertension in broiler chickens. JSM Biomarkers. 4(1): 1013. 32 Ahmadipour, B., Pat, S., Abaszadeh, S., Hassanpour, H., 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. PMid:34132060 PMCid:PMC8464295 33 https://doi.org/10.1002/vms3.556 Tito, A., Colantuono, A., Pirone, L., Pedone, E., Intartaglia, D., Giamundo, G., Conte, I., et al. (2021). Pomegranate peel extract as an inhibitor of SARSCoV- 2 spike binding to human ACE2 receptor (in vitro): a promising source of novel antiviral drugs. Front Chem. 9, 638187. PMid:33996744 PMCid:PMC8114579 34 https://doi.org/10.3389/fchem.2021.638187 Hamady, G.A., Abdel-Moneim, M.A., El-Chaghaby, G.A., Abd-El-Ghany, Z.M., Hassanin, M.S. (2015). Effect of pomegranate peel extract as natural growth promoter on the productive performance and intestinal microbiota of broiler chickens. Afr J Agric Sci Technol. 3(12): 514-519. 35 Rezvani, M.R., Rahimi, S. (2017). Effects of adding pomegranate peel extract and commercial antioxidant to diets on performance, nutrient digestibility, gastrointestinal micro flora and antibody titer of broilers. J Vet Res. 72(2): 147-156. 36 Kishawy, A.T., Amer, S.A., Abd El-Hack, M.E., Saadeldin, I.M., 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-Australas J Anim Sci. 32(8): 1161-1171. PMid:30744351 PMCid:PMC6599952 37 https://doi.org/10.5713/ajas.18.0522 Sharifian, M., Hosseini-Vashan, S.J., Nasri, M.F., 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. 38 https://doi.org/10.1016/j.livsci.2019.06.021 Abdel Baset, S., Ashour, E.A., Abd El-Hack, M.E., El-Mekkawy, M.M. (2022). 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. PMid:33000991 39 https://doi.org/10.1080/10495398.2020.1825965 Rajani, J., Karimi Torshizi, M.A., Rahimi, S. (2011). Control of ascites mortality and improved performance and meat shelf-life in broilers using feed adjuncts with presumed antioxidant activity. Anim Feed Sci Tech. 170(3-4): 239-245. 40 https://doi.org/10.1016/j.anifeedsci.2011.09.001 Ahmed, S.T., 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. PMid:32908421 PMCid:PMC7477121 41 https://doi.org/10.2141/jpsa.0160116 Saleh, H., Golian, A., Kermanshahi, H., Mirakzehi, M.T. (2017). Effects of dietary α-tocopherol acetate, pomegranate peel, and pomegranate peel extract on phenolic content, fatty acid composition, and meat quality of broiler chickens. J Appl Anim Res. 45(1): 629-636. 42 https://doi.org/10.1080/09712119.2016.1248841 Saleh, H., Golian, A., Kermanshahi, H., 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. Ital J Anim Sci. 17(2): 386-395. 43 https://doi.org/10.1080/1828051X.2017.1362966 Rao, S.V.R., Raju, M.V.L.N., Prakash, B., Rajkumar, U., Reddy, E.P.K. (2019). Effect of supplementing moringa (Moringa oleifera) leaf meal and pomegranate (Punica granatum) peel meal on performance, carcass attributes, immune and antioxidant responses in broiler chickens. Anim Prod Sci. 59(2): 288-294. 44 https://doi.org/10.1071/AN17390 Akuru, E.A., Mpendulo, C.T., Oyeagu, C.E., Nantapo, C.W.T. (2021). Pomegranate (Punica granatum L.) peel powder meal supplementation in broilers: effect on growth performance, digestibility, carcass and organ weights, serum and some meat antioxidant enzyme biomarkers. Ital J Anim Sci. 20(1): 119-131. 45 https://doi.org/10.1080/1828051X.2020.1870877 Kamel, E.R., Shafk, B.M., Mamdouh, M., Elrafaay, S., Abdelfattah, F.A.I. (2021). Response of two strains of growing Japanese quail (Coturnix Coturnix Japonica) to diet containing pomegranate peel powder. Trop Anim Health Prod. 53(6): 549. PMid:34782923 46 https://doi.org/10.1007/s11250-021-02987-7 Mohamed, T.M., Sun, W., Bumbie, G.Z., Dosoky, W.M., Rao, Z., Hu, P., Wu, L., Tang, Z. (2022). Effect of dietary supplementation of Bacillus subtilis on growth performance, organ weight, digestive enzyme activities, and serum biochemical indices in broiler. Animals 12(12): 1558. PMid:35739895 PMCid:PMC9219452 47 https://doi.org/10.3390/ani12121558 Qnais, E.Y., Elokda, A.S., Abu Ghalyun, Y.Y., Abdulla, F.A. (2007). Antidiarrheal activity of the aqueous extract of Punica granatum (Pomegranate) peels. Pharm Biol. 45(9): 715-720. 48 https://doi.org/10.1080/13880200701575304 Reddy, B.U., Mullick, R., Kumar, A., Sudha, G., Srinivasan, N., Das, S. (2014). Small molecule inhibitors of HCV replication from pomegranate. Sci Rep. 4, 5411. PMid:24958333 PMCid:PMC4067622 49 https://doi.org/10.1038/srep05411 Perricone, V., Comi, M., Giromini, C., Rebucci, R., Agazzi, A., Savoini, G., 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 chickens. Animals (Basel). 10(5): 785. PMid:32366030 PMCid:PMC7277556 50 https://doi.org/10.3390/ani10050785 Middha, S.K., Usha, T., 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, 296236. PMid:23983682 PMCid:PMC3747345 51 https://doi.org/10.1155/2013/296236 Saeed, M., Naveed, M., Bibi, J., Kamboh, A.A., Arain, M.A., Shah, Q.A., Alagawany, M., et al. (2018). The promising pharmacological effects and therapeutic/medicinal applications of Punica Granatum L. (Pomegranate) as a functional food in humans and animals: a review. Recent Pat Inflamm Allergy Drug Discov. 12(1): 24-38. PMid:29473532 52 https://doi.org/10.2174/1872213X12666180221154713 Cho, J.H., Kim, H.J., Kim, I.H. (2014). Effects of phytogenic feed additive on growth performance, digestibility, blood metabolites, intestinal microbiota, meat color and relative organ weight after oral challenge with Clostridium perfringens in broilers. Livest Sci. 160, 82-88. 53 https://doi.org/10.1016/j.livsci.2013.11.006 Bostami, A.B.M.R., Ahmed, S.T., Islam, M.M. (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(3): 102-114. 54 Pascariu, S.M., Pop, I.M., Simeanu, D., Pavel, G., Solcan, C. (2017). Effects of wine by-products on growth performance, complete blood count and total antioxidant status in broilers. Rev Bras Cienc Avic. 19(2): 191-202. 55 https://doi.org/10.1590/1806-9061-2016-0305 Goni, I., Brenes, A., Centeno, C., Viveros, A., Saura-Calixto, F., Rebolé, A., Arija, I., 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. PMid:17297163 56 https://doi.org/10.1093/ps/86.3.508 Marzo, F., Urdaneta, E., Santidrian, S. (2002). Liver proteolytic activity in tannic acid-fed birds. Poult Sci. 81(1): 92-94. PMid:11885906 57 https://doi.org/10.1093/ps/81.1.92 Bravo, L., Abia, R., Eastwood, M.A., Saura-Calixtol, F. (1994). Degradation of polyphenols (catechin and tannic acid) in the rat intestinal tract. Effect on coloic fermentation and faecal output. Br J Nutr. 71(6): 933-946. PMid:8031740 58 https://doi.org/10.1079/BJN19940197 Saleh, H. (2015). Effects of natural antioxidant on the immune response, antioxidant enzymes and hematological broilers chickens. Iran Vet J. 11(3): 67-79. 59 Banaszkiewicz, T., Białek, A., Tokarz, A., Kaszperuk, K. (2018). Effect of dietary grape and pomegranate seed oil on the post-slaughter value and physicochemical properties of muscles of broiler chickens. Acta Sci Pol Technol Aliment. 17(3): 199-209. PMid:30269459 60 https://doi.org/10.17306/J.AFS.0563 Hamad, K.M., Kareem, K.Y. (2019). Growth performance, carcass quality, and economics of production of Japanese quails fed with pomegranate peel powder. Int J Eng Technol Manag Appl Sci. 10(14): 10A14L. 61 Akuru, E.A., Oyeagu, C.E., Mpendulo, T.C., Rautenbach, F., Oguntibeju, O.O. (2020). Effect of pomegranate (Punica granatum L) peel powder meal dietary supplementation on antioxidant status and quality of breast meat in broilers. Heliyon 6(12): e05709. PMid:33364487 PMCid:PMC7750561 62 https://doi.org/10.1016/j.heliyon.2020.e05709 Murugesan, G.R., Syed, B., Haldar, S., Pender, C. (2015). Corrigendum: phytogenic feed additives as an alternative to antibiotic growth promoters in broiler chickens. Front Vet Sci. 2, 21. 63 https://doi.org/10.3389/fvets.2015.00037 Al-Shammari, K.I.A., Batkowska, J., 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. 64 https://doi.org/10.3923/ijps.2019.122.128 Szymczyk, B., Szczurek, W. (2016). Effect of dietary pomegranate seed oil and linseed oil on broiler chickens performance and meat fatty acid profile. J Anim Feed Sci. 25(1): 37-44. 65 https://doi.org/10.22358/jafs/65585/2016 Rafiei, F., Khajali, F. (2021). Flavonoid antioxidants in chicken meat production: Potential application and future trends. World Poult Sci J. 77(2): 347-361. 66 https://doi.org/10.1080/00439339.2021.1891401 Saki, A.A., Rabet, M., Zamani, P., 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. Iran J Appl Anim Sci. 4(4): 803-808. 67 Abbas, R.J., Al-Salhie, K.C.K., 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): 231. 68 Ghahtan, N., Kohanmoo, M.A., Habibi, H. (2019). Evaluation of dietary medicinal plants and algae in laying Japanese quails. J World Poult Res. 9(2): 82-88. 69 https://doi.org/10.36380/jwpr.2019.10 Mutlu, S.I., 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. Turk J Vet Anim Sci. 45(1): 101-112. 70 https://doi.org/10.3906/vet-2002-58 Gultepe, E.E., Iqbal, A., Cetingul, I.S., Uyarlar, C., Ozcinar, U., Bayram, I. (2022). Effects of pomegranate (Punica granatum L.) juice as a shortterm water supplement during the peak production cycle in laying hens. Ankara Univ Vet Fak Derg. 69, 241-249. 71 https://doi.org/10.33988/auvfd.795175 Iqbal, A., Bayram, I., Gultepe, E.E., Uyarlar, C., Ümit, Õ, Cetingul İ.S. (2021). The Effect of different level of Pomegranate molasses on performance, egg quality trait, serological and hematological parameters in older laying hens: the use of pomegranate molasses as growth promoter in poultry nutrition. Progr Nutr. 22(4): e2020052. 72 Sharma, M.K., Dinh, T., Adhikari, P.A. (2020). Production performance, egg quality, and small intestine histomorphology of the laying hens supplemented with phytogenic feed additive. J Appl Poult Res. 29(2): 362-371. 73 https://doi.org/10.1016/j.japr.2019.12.001 Kostogrys, R.B., Filipiak-Florkiewicz, A., Dereń, K., Drahun, A., Czyżyńska-Cichoń, I., Cieślik, E., Szymczyk, B., Franczyk-Żarów, M. (2017). Effect of dietary pomegranate seed oil on laying hen performance and physicochemical properties of eggs. Food Chem. 221, 1096-1103. PMid:27979064 74 https://doi.org/10.1016/j.foodchem.2016.11.051 Johanningsmeier, S.D., Harris, G.K. (2011). Pomegranate as a functional food and nutraceutical source. Annu Rev Food Sci Technol. 2: 181-201. PMid:22129380 75 https://doi.org/10.1146/annurev-food-030810-153709 Seeram, N.P., Adams, L.S., Henning, S.M., Niu, Y., Zhang, Y., Nair, M.G., Heber, D. (2005). In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J Nutr Biochem. 16(6): 360-367. PMid:15936648 76 https://doi.org/10.1016/j.jnutbio.2005.01.006 Singh, B., Singh, J.P., Kaur, A., Singh, N. (2018). Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: a review. Food Chem. 261, 75-86. PMid:29739608 77 https://doi.org/10.1016/j.foodchem.2018.04.039 Ghosh, S., Chatterjee, P.N., Maity, A., Mukherjee, J., Batabyal, S., 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. PMid:32737663 78 https://doi.org/10.1007/s11250-020-02352-0 Ginsburg, I., Kohen, R., Koren, E. (2011). Microbial and host cells acquire enhanced oxidant-scavenging abilities by binding polyphenols. Arch Biochem Biophys. 506(1): 12-23. PMid:21081104 79 https://doi.org/10.1016/j.abb.2010.11.009 Faria, A., Monteiro, R., Mateus, N., Azevedo, I., Calhau, C. (2007). Effect of pomegranate (Punica granatum) juice intake on hepatic oxidative stress. Eur J Nutr. 46(5): 271-278. PMid:17514376 80 https://doi.org/10.1007/s00394-007-0661-z Gil, M.I., Tomás-Barberán, F.A., Hess-Pierce, B., Holcroft, D.M., Kader, A.A. (2000). Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J Agric Food Chem. 48(10): 4581-4589. PMid:11052704 81 https://doi.org/10.1021/jf000404a Gözlekçi, S., Saraçoğlu, O., Onursal, E., Ozgen, M. (2011). Total phenolic distribution of juice, peel, and seed extracts of four pomegranate cultivars. Pharmacogn Mag. 7(26): 161-164. PMid:21716925 PMCid:PMC3113357 82 https://doi.org/10.4103/0973-1296.80681 Benchagra, L., Berrougui, H., Islam, M.O., Ramchoun, M., Boulbaroud, S., Hajjaji, A., Fulop, T., et al. (2021). Antioxidant effect of Moroccan pomegranate (Punica granatum L. Sefri Variety) extracts rich in punicalagin against the oxidative stress process. Foods. 10(9): 2219. PMid:34574329 PMCid:PMC8469689 83 https://doi.org/10.3390/foods10092219 Afaq, F., Saleem, M., Krueger, C.G., Reed, J.D., Mukhtar, H. (2005). Anthocyaninand hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF- B pathways and inhibits skin tumorigenesis in CD-1 mice. Int J Cancer. 113(3): 423-433. PMid:15455341 84 https://doi.org/10.1002/ijc.20587 Singh, J.P., Kaur, A., Shevkani, K., Singh, N. (2016). Composition, bioactive compounds, and antioxidant activity of common Indian fruits and vegetables. J Food Sci Technol. 53(11): 4056-4066. PMid:28035161 PMCid:PMC5156649 85 https://doi.org/10.1007/s13197-016-2412-8 Kanatt, S.R., Chander, R., Sharma, A. (2010). Antioxidant and antimicrobial activity of pomegranate peel extract improves the shelf life of chicken products. Int J Food Sci Technol. 45(2): 216-222. 86 https://doi.org/10.1111/j.1365-2621.2009.02124.x Khor rami, P., Gholami-Ahangaran, M., 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. 8(2): 635-641. PMid:34981905 PMCid:PMC8959253 87 https://doi.org/10.1002/vms3.714 Dahham, S.S., Ali, M.N., Tabassum, H., Khan, M. (2010). Studies on antibacterial and antifungal activity of pomegranate (Punica granatum L.). Am-Eurasian J Agric Environ Sci. 9(3): 273-281. 88 Growther, L., Sukirtha, K., Savitha, N., Niren, A.S. (2012). Antibacterial activity of Punica granatum peel extracts against shiga toxin producing E. coli. Int J Life Sci Biotechnol Pharma Res. 1(4): 164-172. 89 Prashanth, D.J., Asha, M.K., Amit, A. (2001). Antibacterial activity of Punica granatum. Fitoterapia 72(2): 171-173. PMid:11223228 90 https://doi.org/10.1016/S0367-326X(00)00270-7 Voravuthikunchai, S.P., Sririrak, T., Limsuwan, S.,Supawita, T., Iida, T., Honda, T. (2005). Inhibitory effects of active compounds from Punica granatum pericarp on verocytotoxin production by enterohemorrhagic Escherichia coli O157:H7. J Health Sci. 51(5): 590-596. 91 https://doi.org/10.1248/jhs.51.590 McCarrell, E.M., Gould, S.W., Fielder, M.D., Kelly, A.F., El Sankary, W., Naughton, D.P. (2008). Antimicrobial activities of pomegranate rind extracts: enhancement by addition of metal salts and vitamin C. BMC Complement Altern Med. 8, 64. PMid:19077299 PMCid:PMC2628863 92 https://doi.org/10.1186/1472-6882-8-64 Nuamsetti, T., Dechayuenyong, P., Tantipaibulvut, S. (2012). Antibacterial activity of pomegranate fruit peels and arils. Sci Asia. 38, 319-322. 93 https://doi.org/10.2306/scienceasia1513-1874.2012.38.319 Juneja, V.K., Cadavez, V., Gonzales-Barron, U., Mukhopadhyay, S., Friedman, M. (2016). Effect of pomegranate powder on the heat inactivation of Escherichia coli O104:H4 in ground chicken. Food Control. 70, 26-34. 94 https://doi.org/10.1016/j.foodcont.2016.05.027 Pagliarulo, C., De Vito, V., Picariello, G., Colicchio, R., Pastore, G., Salvatore, P., 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. PMid:26213044 95 https://doi.org/10.1016/j.foodchem.2015.06.028 Wafa, B.A., Makni, M., Ammar, S., Khannous, L., Hassana, A.B., Bouaziz, M., Es-Safi, N.E., Gdoura, R. (2017). Antimicrobial effect of the Tunisian Nana variety Punica granatum L. extracts against Salmonella enterica (serovars Kentucky and Enteritidis) isolated from chicken meat and phenolic composition of its peel extract. Int J Food Microbiol. 241, 123-131. PMid:27776287 96 https://doi.org/10.1016/j.ijfoodmicro.2016.10.007 Abdollahzadeh, S.H., Mashouf, R.Y., Mortazavi, H., Moghaddam, M.H., Roozbahani, N., Vahedi, M. (2011). Antibacterial and antifungal activities of Punica granatum peel extracts against oral pathogens. J Dent (Tehran) 8(1): 1-6. 97 Oraki, H.H., Demirci, A.S., Gümü¸S.T. (2011). Antibacterial and antifungal activity of pomegranate (Punica granatum L. cv.) peel. Elec J Env Agricult Food Chem. 10(3): 1958-1969. 98 Singh, B., Singh, J.P., Kaur, A., Singh, N. (2019). Antimicrobial potential of pomegranate peel: a review. Int J Food Sci Technol. 54(4): 959-965. 99 https://doi.org/10.1111/ijfs.13964 Scalbert, A. (1991). Antimicrobial properties of tannins. Phytochemistry 30(12): 3875-3883. 100 https://doi.org/10.1016/0031-9422(91)83426-L Viuda-Martos, M., Fernández-López, J., Pérez-Álvarez, J.A. (2010). Pomegranate and its many functional components as related to human health: a review. Compr Rev Food Sci Food Saf. 9(6): 635-654. PMid:33467822 101 https://doi.org/10.1111/j.1541-4337.2010.00131.x Vidanarachchi, J.K., Mikkelsen, L., Sims, I., Iji, P., Choct, M. (2005). Phytobiotics: Alternatives to antibiotic growth promoters in monogastric animal feeds. Recent Adv Anim Nutr Australia. 15, 131-144. 102 Ferreira, S.B., Palmeira, J.D., Souza, J.H., Almeida, J.M., Figueiredo, M.C.P., Pequeno, A.S., Arruda, T.A., et al. (2010). Evaluation of the antimicrobial activity in vitro of the hydroalcoholic extract Stryphnodendron adstringens against of Staphylococcus aureus strains. Braz J Clin Anal 42, 27-31. 103 Tang, Y., Zhang, X., Wang, Y., Guo, Y., Zhu, P., Li, G., Zhang, J., et al. (2022). Correction: Dietary ellagic acid ameliorated Clostridium perfringensinduced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota. J Anim Sci Biotechnol. 13(1): 66. PMid:35562813 PMCid:PMC9103450 104 https://doi.org/10.1186/s40104-022-00724-0 Sarica, S., Urkmez, D. (2016). The use of grape seed-, olive leaf-and pomegranate peel-extracts as alternative natural antimicrobial feed additives in broiler diets. Europ Poult Sci. 80, 1-13. 105 https://doi.org/10.1399/eps.2016.121 Fahmy, Z.H., El-Shennawy, A.M., El-Komy, W., Ali, E., Hamid, S.S.A. (2009). Potential antiparasitic activity of pomegranate extracts against Schistosomules schis and mature worms of Schistosoma mansoni: in vitro and in vivo study. Aust J Basic Appl Sci. 3(4): 4634-4643. 106 El-Sherbini, G.T., Shoukry, N.M. (2012). In vitro effect of pomegranate peel extract on Trichomonas tenax. Life Sci J. 9(3): 791-797. 107 Al-Mathal, E.M., Alsalem, A.A. (2013). Pomegranate (Punica granatum) peel is effective in a murine model of experimental Cryptosporidium parvum ultrastructural studies of the ileum. Exp Parasitol. 134(4): 482-494. PMid:23684569 108 https://doi.org/10.1016/j.exppara.2013.05.004 Boonmasawai, S., Sungpradit, S., Jirapattharasate, C., Nakthong, C., Piasai, L. (2013). Effects of alcoholic extract from pomegranate (Punica granatum L.) peels on gastrointestinal nematode egg counts in doe. J Appl Anim Sci. 6(2): 27-37. 109 Bunviboolvat, P., Taechaarpornkul, N., Saratham, J., Sungpradit, S., Jirapattharasate, C., Nakthong, C., Piasai, L., et al. (2013). Anthelmintic effects of ethanolic extracts from pomegranate peels, mangosteen peels and tamarind seeds on gastrointestinal nematode egg counts in lambs. J Appl Anim Sci. 6(2): 39-48. 110 Al-Megrin, W. (2016). Efficacy of pomegranate (Punica granatum) peel extract against Hymenolepis nana in infections mice. Biosci Biotechnol Res Asia. 13(1): 103-108. 111 https://doi.org/10.13005/bbra/2010 Al-Megrin, W.A. (2017). In vivo study of pomegranate (Punica granatum) peel extract efficacy against Giardia lamblia in infected experimental mice. Asian Pac J Trop Biomed. 7(1): 59-63. 112 https://doi.org/10.1016/j.apjtb.2016.08.018 Elfalleh, W., Hannachi, H., Tlili, N., Yahia, Y., Nasri, N., Ferchichi, A. (2012). Total phenolic contents and antioxidant activities of pomegranate peel, seed, leaf and flower. J Med Plant Res. 6(32): 4724-4730. 113 https://doi.org/10.5897/JMPR11.995 Bazargani-Gilani, B., Aliakbarlu, J., Tajik, H. (2015). Effect of pomegranate juice dip ping and chitosan coating enriched with Zataria multifora Boiss essential oil on the shelf-life of chicken meat during refrigerated storage. Innov Food Sci Emerg Technol. 29, 280-287. 114 https://doi.org/10.1016/j.ifset.2015.04.007 Hayrapetyan, H., Hazeleger, W.C., Beumer, R.R. (2012). Inhibition of Listeria mono cytogenes by pomegranate (Punica granatum) peel extract in meat paté at different temperatures. Food Control. 23(1): 66-72. 115 https://doi.org/10.1016/j.foodcont.2011.06.012 Kumar, K.P., Reddy, V.R., Prakash, M.G. (2018). Effect of supplementing pomegranate (Punica granatum) peel extract on serum biochemical parameters and immune response in broilers during summer. Pharma Innov J. 7(3): 597-601. 116 Fadavi, A, Barzegar, M., Azizi, M.H. (2006). Determination of fatty acids and total lipid content in oilseed of 25 pomegranates varieties grown in Iran. J Food Compos Anal. 19(6-7): 676-680. 117 https://doi.org/10.1016/j.jfca.2004.09.002 Melo, I.L.P., Carvalho, E.B.T., Mancini-Filho, J. (2014). Pomegranate seed oil (Punica Granatum L.): a source of punicic acid (Conjugated α-Linolenic Acid). J Hum Nutr Food Sci. 2(1): 1024. 118 Wang, Y.W., Field, C.J., Sim, J.S. (2000). Dietary polyunsaturated fatty acids alter lymphocyte subset proportion and proliferation, serum immunoglobulin g concentration, and immune tissue development in chicks. Poult Sci. 79(12): 1741-1748. PMid:11194036 119 https://doi.org/10.1093/ps/79.12.1741 Yaseen, A.T, El-Kholy, M.E.S.H, El-Razik, W.M.A., Soliman, M.H. (2016). Effect of using pomegranate peel extract as feed additive on performance, serum lipids and immunity of broiler chicks. Zagazig Vet J. 42(1): 87-92. 120 https://doi.org/10.21608/zvjz.2014.59473 Hou, C., Zhang, W., Li, J., Du, L., Lv, O., Zhao, S., Li, J. (2019). Beneficial effects of pomegranate on lipid metabolism in metabolic disorders. Mol Nutr Food Res. 63(16): e1800773. PMid:30677224 121 https://doi.org/10.1002/mnfr.201800773 Aviram, M., Fuhrman, B. (2001). Flavonoid antioxidants protect LDL from oxidation and attenuate atherosclerosis. Curr Opin Lipidol. 12(1): 41-48. PMid:11176202 122 https://doi.org/10.1097/00041433-200102000-00008 Esmaillzadeh, A., Tahbaz, F., Gaieni, I., Alavi-Majd, H., Azadbakht, L. (2006). Cholesterollowering effect of concentrated pomegranate juice consumption in type II diabetic patients with hyperlipidemia. Int J Vitam Nutr Res. 76(3): 147-151. PMid:17048194 123 https://doi.org/10.1024/0300-9831.76.3.147 Lv, O., Wang, L., Li, J., Ma, Q., Zhao, W. (2016). Effects of pomegranate peel polyphenols on lipid accumulation and cholesterol metabolic transformation in L-02 human hepatic cells via the PPARγ-ABCA1/CYP7A1 pathway. Food Funct. 7(12): 4976-4983. PMid:27845788 124 https://doi.org/10.1039/C6FO01261B Zhao, W., Li, J., He, X., Lv, O., Cheng, Y., Liu, R. (2014). In vitro steatosis hepatic cell model to compare the lipid-lowering effects of pomegranate peel polyphenols with several other plant polyphenols as well as its related cholesterol efflux mechanisms. Toxicol Rep. 1, 945-954. PMid:28962306 PMCid:PMC5598384 125 https://doi.org/10.1016/j.toxrep.2014.10.013 Wu, S., Tian, L. (2017). Diverse phytochemicals and bioactivities in the ancient fruit and modern functional food pomegranate (Punica granatum). Molecules 22(10): 1606. PMid:28946708 PMCid:PMC6151597 126 https://doi.org/10.3390/molecules22101606 Manthou, E., Georgakouli, K., Deli, C.K., Sotiropoulos, A., Fatouros, I.G., Kouretas, D., Haroutounian, S., et al. (2017). Effect of pomegranate juice consumption on biochemical parameters and complete blood count. Exp Ther Med. 14(2): 1756-1762. PMid:28781633 PMCid:PMC5526177 127 https://doi.org/10.3892/etm.2017.4690 Mollazadeh, H., Sadeghnia, H.R., Hoseini, A., Farzadnia, M., Boroushaki, M.T. (2016). Effects of pomegranate seed oil on oxidative stress markers, serum biochemical parameters and pathological findings in kidney and heart of streptozotocininduced diabetic rats. Ren Fail. 38(8): 1256-1266. PMid:27453190 128 https://doi.org/10.1080/0886022X.2016.1207053 Attia, N.Y.A., Abd El-Aleem, I.M., El-Tobgy, K.M.K., Mohamed, H.F. (2014). Biochemical studies on pomegranate. Ann Agric Sci., Moshtohor 52(4): 481-494. 129 https://doi.org/10.21608/assjm.2014.111897