This meta-analysis was conducted to investigate the effect of dietary propolis supplementation on broiler performance, carcass characteristics, and nutrient digestibility evaluated at the starter and finisher phases. An online literature search was conducted using scientific platforms of Science Direct, PubMed, and Google Scholar to identify the studies utilizing propolis as dietary supplementation in broiler chickens. A total of 39 publications comprising of 58 experiments met the inclusion criteria. A mixed model procedure for meta-analysis was performed, considering the studies as a random effect and levels of propolis as a fixed effect. Regression analysis suggested that average daily gain (ADG), body weight, and average daily feed intake (ADFI) at starter and finisher phases were quadratically affected by supplementing propolis in the diet (p<0.01). Propolis also lowered the feed conversion ratio (FCR) throughout the periods (p<0.05). In addition, a positive effect of propolis inclusion was also observed on breast meat percentage (p<0.05). However, there was a negative linear relationship between propolis and the digestibility of dry matter (DMD) and organic matter (OMD) (p<0.01) at the starter period. Conversely, there was a linear increase in DMD (p<0.05) and a tendency to improve apparent metabolizable energy (AME) and phosphorus digestibility at the finisher period (p<0.10). Overall, it can be concluded that dietary propolis supplementation promoted better growth performance and feed efficiency when given at ~1.66-2.13 g/kg diets for starter and finisher phases in the broiler chickens. The effect of propolis on nutrient digestibility was positive at the finisher phase while it was detrimental at the starter phase.
Abdelsameea, A. A., L. A. Mahgoub, & S. M. A. Raouf. 2013. Study of the possible hepatoprotective effect of propolis against the hepatotoxic effect of atorvastatin in albino rats. ZUMJ 19:388-396. https://doi.org/10.21608/zumj.2013.4306
Abdelsalam, A. M., A. Abd ElAzim, A. M. R. Othman, & E. M. Omar. 2019. Blood hematological and biochemical parameters and humoral immunity as affected by added dietary propolis supplementation of Cobb broiler chicks. Egypt. J. Nutr. Feed. 22:215-221. https://doi.org/10.21608/ejnf.2019.103495
Abou-Zeid, A., S. El-Damarawy, Y. Mariey, & S. El-Kasass. 2015. Effect of dietary propolis supplementation on performance and activity of antioxidant enzymes in broiler chickens. Egypt. J. Nutr. Feed. 18:391-400. https://doi.org/10.21608/ejnf.2015.104498
Abudabos, A. M., E. O. S. Hussein, M. H. Ali, & M. Q. Al-Ghadi. 2019. The effect of some natural alternative to antibiotics on growth and changes in intestinal histology in broiler exposed to Salmonella challenge. Poult. Sci. 98:1441-1446. https://doi.org/10.3382/ps/pey449
Açikgöz, Z., B. Yücel, & Ö. Altan. 2005. The effects of propolis supplementation on broiler performance and feed digestibility. Arch. Geflugelk. 69:117-122. https://doi.org/10.1590/S0103-90161998000100024
Alani, A. A. T., A. S. A. Alheeti, & E. N. S. Alani. 2019. Comparison between effect of adding propolis and antibiotic in in broiler chickens on productive performance and carcass traits. IOP Conf. Ser. Earth Environ. Sci. 388:012032. https://doi.org/10.1088/1755-1315/388/1/012032
Allen, H. K., U. Y. Levine, T. Looft, M. Bandrick, & T. A. Casey. 2013. Treatment, promotion, commotion: Antibiotic alternatives in food-producing animals. Trends Microbiol. 21:114-119. https://doi.org/10.1016/j.tim.2012.11.001
Al-Sultan, S. I., S. M. Abdel-Raheem, S. M. S. Abd-Allah, & A. M. Edris. 2019. Alleviation of chronic heat stress in broilers by dietary supplementation of novel feed additive combinations. Slov. Vet. Res. 56:269-279. https://doi.org/10.26873/SVR-766-2019
Ao, Z. & M. Choct. 2013. Oligosaccharides affect performance and gut development of broiler chickens. Asian-Australas. J. Anim. Sci. 26:116-121. https://doi.org/10.5713/ajas.2012.12414
Attia, Y.A., A.E.A. Al-Hamid, M.S. Ibrahim, M.A. Al-Harthi, F. Bovera, & A.S. Elnaggar. 2014. Productive performance, biochemical and hematological traits of broiler chickens supplemented with propolis, bee pollen, and mannan oligosaccharides continuously or intermittently. Livest. Sci. 164:87-95. https://doi.org/10.1016/j.livsci.2014.03.005
Attia, Y. A., H. Al-Khalaifah, M. S. Ibrahim, A. E. A. Al-Hamid, M. A. Al-Harthi, & A. El-Naggar. 2017. Blood hematological and biochemical constituents, antioxidant enzymes, immunity and lymphoid organs of broiler chicks supplemented with propolis, bee pollen and mannan oligosaccharides continuously or intermittently. Poult. Sci. 96:4182-4192. https://doi.org/10.3382/ps/pex173
Biavatti, M. W., M. H. Bellaver, L. Volpato, C. Costa, & C. Bellaver. 2003. Preliminary studies of alternative feed additives for broilers: Alternanthera brasiliana extract, propolis extract and linseed oil. Rev. Bras. Cienc. Avic. 5:147-151. https://doi.org/10.1590/S1516-635X2003000200009
Chegini, S., A. Kiani, & H. Rokni. 2018. Alleviation of thermal and overcrowding stress in finishing broilers by dietary propolis supplementation. Ital. J. Anim. Sci. 17:377-385. https://doi.org/10.1080/1828051X.2017.1360753
Chegini, S., A. Kiani, B. Parizadian Kavan, & H. Rokni. 2019. Effects of propolis and stocking density on growth performance, nutrient digestibility, and immune system of heat-stressed broilers. Ital. J. Anim. Sci. 18:868-876. https://doi.org/10.1080/1828051X.2018.1483750
Daneshmand, A., G. H. Sadeghi, & A. Karimi. 2012. The effects of a combination of garlic, oyster mushroom and propolis extract in comparison to antibiotic on growth performance, some blood parameters and nutrients digestibility of male broilers. Rev. Bras. Cienc. Avic. 14:141-147. https://doi.org/10.1590/S1516-635X2012000200009
Daneshmand, A., G. H. Sadeghi, A. Karimi, A. Vaziry, & S. A. Ibrahim. 2015. Evaluating complementary effects of ethanol extract of propolis with the probiotic on growth performance, immune response and serum metabolites in male broiler chickens. Livest. Sci. 178:195-201. https://doi.org/10.1016/j.livsci.2015.04.012
Duarte, C. R. A., C. Eyng, A. E. Murakami, & T. C. Santos. 2014. Intestinal morphology and activity of digestive enzymes in broilers fed crude propolis. Can. J. Anim. Sci. 94:105-114. https://doi.org/10.4141/cjas2013-059
Dziedzic, A., R. Kubina, R. D. Wojtyczka, A. Kabala-Dzik, M. Tanasiewicz, & T. Morawiec. 2013. The antibacterial effect of ethanol extract of polish propolis on mutans streptococci and lactobacilli isolated from saliva. Evid. Based Complement. Alternat. Med. 2013:1-12. https://doi.org/10.1155/2013/681891
Denli, M., S. Cankaya, S. Silici, F. Okan, & A. N. Uluocak. 2005. Effect of dietary addition of Turkish propolis on the growth performance, carcass characteristics and serum variables of quail (Coturnix coturnix japonica). Asian-Australas. J. Anim. Sci. 18:848-854. https://doi.org/10.5713/ajas.2005.848
Ebling, P. D., A. M. Kessler, A. P. Villanueva, G. C. Pontalti, G. Farina, & A. M. L. Ribeiro. 2015. Rice and soy protein isolate in pre-starter diets for broilers. Poult. Sci. 94:2744-2752. https://doi.org/10.3382/ps/pev279
Eyng, C., A. E. Murakami, C. R. A. Duarte, & T. C. Santos. 2014. Effect of dietary supplementation with an ethanolic extract of propolis on broiler intestinal morphology and digestive enzyme activity. J. Anim. Physiol. Anim. Nutr. (Berl). 98:393-401. https://doi.org/10.1111/jpn.12116
Eyng, C., A. E. Murakami, A. A. Pedroso, C. R. A. Duarte, & K. P. Picoli. 2017. Caecal microbiota of chickens fed diets containing propolis. J. Anim. Physiol. Anim. Nutr. 101:484-492. https://doi.org/10.1111/jpn.12570
Eyng, C., A. E. Murakami, T. C. Santos, T. G. V. Silveira, R. B. Pedroso, & D. A. L. Lourenço. 2015. Immune responses in broiler chicks fed propolis extraction residue-supplemented diets. Asian-Australas. J. Anim. Sci. 28:135-142. https://doi.org/10.5713/ajas.14.0066
Gheisari, A., S. Shahrvand, & N. Landy. 2017. Effect of ethanolic extract of propolis as an alternative to antibiotics as a growth promoter on broiler performance, serum biochemistry, and immune responses. Vet. World. 10:249-254. https://doi.org/10.14202/vetworld.2017.249-254
Guo, F.C., B.A. Williams, R.P. Kwakkel, & M.W.A. Verstegen. 2003. In vitro fermentation characteristics of two mushroom species, an herb, and their polysaccharide fractions, using chicken cecal contents as inoculum. Poult. Sci. 82:1608-1615. https://doi.org/10.1093/ps/82.10.1608
Hascik, P., L. Trembecká, M. Bobko, M. Kacaniova, J. Cubon, S. Kunova, & O. Bucko. 2016. Effect of diet supplemented with propolis extract and probiotic additives on performance, carcass characteristics and meat composition of broiler chickens. Potravinarstvo 10:223-231. https://doi.org/10.5219/581
Hascik, P., A. Pavelkova, H. Arpasova, J. Cubon, M. Kacaniova, & S. Kunová. 2019. The effect of bee products and probiotic on meat performance of broiler chickens. J. Microbiol. Biotechnol. Food Sci. 9:88-92. https://doi.org/10.15414/jmbfs.2019.9.1.88-92
Hassan, R. I. M., G. M. M. Mosaad, & H. Y. Abd El-Wahab. 2018. Effect of feeding propolis on growth performance of broilers. J. Adv. Vet. Res. 8:66-72.
Hidayat, C., Sumiati, A. Jayanegara, & E. Wina. 2020. Effect of zinc on the immune response and production performance of broilers: a meta-analysis. Asian-Australas. J. Anim. Sci. 33:465-479. https://doi.org/10.5713/ajas.19.0146
Hosseini, S.M., M. V. Azghandi, S. Ahani, & R. Nourmohammadi. 2016. Effect of bee pollen and propolis (bee glue) on growth performance and biomarkers of heat stress in broiler chickens reared under high ambient temperature. J. Anim. Feed Sci. 25:45-50. https://doi.org/10.22358/jafs/65586/2016
Jha, R., R. Das, S. Oak, & P. Mishra. 2020. Probiotics (Direct-Fed Microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: a systematic review. Animals 10:1863. https://doi.org/10.3390/ani10101863
Kačániová, M., K. Rovná, H. Arpášová, J. Čuboň, L. Hleba, J. Pochop, S. Kunová, & P. Haščík. 2012. In vitro and In vivo antimicrobial activity of propolis on the microbiota from gastrointestinal tract of chickens. J. Environ. Sci. Heal. - Part A. 47:1665-1671. https://doi.org/10.1080/10934529.2012.687248
Khafaji, S. S. O., T. K. ALjanabi, & S. M. Suhailaltaie. 2019. Evaluation the impact of different levels of propolis on some reproductive features in iraqi local roosters. Adv. Anim. Vet. Sci. 7:82-87. https://doi.org/10.17582/journal.aavs/2019/22.214.171.124
Khodanazary, A., A. Tatar & M. Khezri. 2011. Effects of different dietary levels of propolis on performance, carcass characteristics and immunity response of broiler chickens. J. Ethnopharmacol. 2:80-83.
Kinasih, I., U. Julita, Y. Suryani, T. Cahyanto, D. S. Annisa, A. Yuliawati, & R. E. Putra. 2018. Addition of black soldier fly larvae (Hermetia illucens L.) and propolis to broiler chicken performance. IOP Conf. Ser. Earth Environ. Sci. 187:012026. https://doi.org/10.1088/1755-1315/187/1/012026
Klarić, I., M. Domaćinović, V. Šerić, I. Miškulin, M. Pavić, & K. Paradinović. 2018. Effects of bee pollen and propolis on performance, mortality, and some haematological blood parameters in broiler chickens. Slov. Vet. Res. 55:23-34. https://doi.org/10.26873/SVR-385-2018
Kleczek, K., E. Wilkiewicz-Wawro, K. Wawro, W. Makowski, D. Murawska, & M. Wawro. 2014. The effect of dietary propolis supplementation on the growth performance of broiler chickens. Pol. J. Nat. Sci. 29:105-117.
Mahmoud, U. T., M. A. Abdel-Rahman, & M. H. A. Darwish. 2013. The effect of chinese propolis supplementation on ross broiler performance and carcass characteristics. J. Adv. Vet. Res. 3:154-160.
Mahmoud, U. T., O. A. Amen, T. J. Applegate, & H. W. Cheng. 2017. Brazilian propolis effects on growth, productivity performance, gut characteristics and physiological changes in broiler chickens. Int. J. Poult. Sci. 16:169-179. https://doi.org/10.3923/ijps.2017.169.179
Miles, R. D., G. D. Butcher, P. R. Henry, & R. C. Littell. 2006. Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poult. Sci. 85:476-485. https://doi.org/10.1093/ps/85.3.476
Mountzouris, K. C., P. Tsitrsikos, I. Palamidi, A. Arvaniti, M. Mohnl, G. Schatzmayr, & K. Fegeros. 2010. Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult. Sci. 89:58–67 http://dx.doi.org/10.3382/ps.2009-00308
Nasution, A. Y., P. Adi, & P. A. Santosa. 2015. Effect of propolis extract on levels of SGOT (serum glutamic oxaloacetic transaminase) and SGPT (serum glutamic pyruvic transaminase) in white rats (Rattus norvegicus) wistar strain on a high-fat diet. Majalah Kesehatan FKUB 2:120-126.
Noy, Y. & D. Sklan. 1999. Energy utilization in newly hatched chicks. Poult. Sci. 78:1750-1756. https://doi.org/10.1093/ps/78.12.1750
Oakley, B. B. & M. H. Kogut. 2016. Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression. Front. Vet. Sci. 3:11. https://doi.org/10.3389/fvets.2016.00011
Pimenta, H. C., I. M. ari. P. Violante, C. R. alp. de Musis, Á. H. Borges, & A. M. ari. F. Aranha. 2015. In vitro effectiveness of Brazilian brown propolis against Enterococcus faecalis. Braz. Oral Res. 29:1-6. https://doi.org/10.1590/1807-3107BOR-2015.vol29.0058
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, Eispack, S. Heisterkamp, & B. V. Willigen. 2020. “Package ‘Nlme’ March. R Core Team. 1-335.
Prakatur, I., M. Miskulin, M. Pavic, K. Marjanovic, V. Blazicevic, I. Miskulin, & M. Domacinovic. 2019. Intestinal morphology in broiler chickens supplemented with propolis and bee pollen. Animals 9:301. https://doi.org/10.3390/ani9060301
Przybyłek, I., & T. M. Karpiński. 2019. Antibacterial properties of propolis. Molecules 24:11-13. https://doi.org/10.3390/molecules24112047
R Core Team. 2020. R: A Language and Environment for Statistical Computing. R Core Team
Rabie, A. H., A. M. El-Kaiaty, M. S. Hassan, & F. R. Stino. 2018. Influence of some honey bee products and a growth promoter supplementation on productive and physiological performance of broiler chickens. Egypt. Poult. Sci. J. 38:513-531.
Romier, B., Y. J. Schneider, Y. Larondelle, & A. During. 2009. Dietary polyphenols can modulate the intestinal inflammatory response. Nutr. Rev. 67:363-378. https://doi.org/10.1111/j.1753-4887.2009.00210.x
Sahin, H. A. & E. Ozturk. 2018. Effects of raw propolis or water and ethanol extracts of propolis on performance, immune system, and some blood parameters of broiler breeders. Rev. Bras. Zootec. 47:e20170161. https://doi.org/10.1590/rbz4720170161
Sauvant, D., P. Schmidely, & J. J. Daudin. 2008. Meta-analyses of experimental data in animal nutrition*. Animal. 2:1203-1214. https://doi.org/10.1017/S1751731108002280
Seven, P. T. & I. Seven. 2008. Effect of dietary turkish propolis as alternative to antibiotic on performance and digestibility in broilers exposed to heat stress. J. Appl. Anim. Res. 34:193-196. https://doi.org/10.1080/09712119.2008.9706970
Seven, I., T. Aksu, & P. Tatli-Seven. 2010. The effects of propolis on biochemical parameters and activity of antioxidant enzymes in broilers exposed to lead-induced oxidative stress. Asian-Australas. J. Anim. Sci. 23:1482-1489. https://doi.org/10.5713/ajas.2010.10009
Seven, I., T. Aksu, & P. Tatli-Seven. 2012. The effects of propolis and vitamin C supplemented feed on performance, nutrient utilization and carcass characteristics in broilers exposed to lead. Livest. Sci. 148:10-15. https://doi.org/10.1016/j.livsci.2012.05.001
Sforcin, J. M. 2016. Biological properties and therapeutic applications of propolis. Phytother. Res. 30:894-905. https://doi.org/10.1002/ptr.5605
Shaddel-Tili, A., B. Eshratkhah, H. Kouzehgari, & M. Ghasemi-Sadabadi. 2017. The effect of different levels of propolis in diets on performance, gastrointestinal morphology and some blood parameters in broiler chickens. Bulg. J. Vet. Med. 20:215-224. https://doi.org/10.15547/bjvm.986
Shalmany, K. S. & M. Shivazad. 2006. The effect of diet propolis supplementation on Ross broiler chicks performance. Int. J. Poult. Sci. 5:84-88. https://doi.org/10.3923/ijps.2006.84.88
Silva, R. P. D., B. A. S. Machado, G. De Abreu Barreto, S. S. Costa, L. N. Andrade, R. G. Amaral, A. A. Carvalho, F.F. Padilha, J. D. V. Barbosa, & M. A. Umsza-Guez. 2017. Antioxidant, antimicrobial, antiparasitic, and cytotoxic properties of various Brazilian propolis extracts. PLoS One 12:1-18. https://doi.org/10.1371/journal.pone.0173397
St-Pierre, N. R. 2001. Invited review: Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84:741-55. https://doi.org/10.3168/jds.S0022-0302(01)74530-4
Taheri, H. R., H. R. Rahmani, & J. Pourreza. 2005. Humoral immunity of broilers is affected by oil extracted propolis (OEP) in the diet. Int. J. Poult. Sci. 4:414-417. https://doi.org/10.3923/ijps.2005.414.417
Tatli Seven, P., I. Seven, M. Yilmaz, & Ü.G. Şimşek. 2008. The effects of Turkish propolis on growth and carcass characteristics in broilers under heat stress. Anim. Feed Sci. Technol. 146:137-148. https://doi.org/10.1016/j.anifeedsci.2007.11.003
Tayeb, I. T. & B. F. Sulaiman. 2014. Effect of propolis supplementation on productive performance in local quail. Iran. J. Appl. Anim. Sci. 4:621-627.
Tekeli, A., H. Kutlu, L. Celik, & F. Doran. 2010. Determination of the effects of Z. officinale and propolis extracts on intestinal microbiology and histological characteristics in broilers. Int. J. Poult. Sci. 9:898-906. https://doi.org/10.3923/ijps.2010.898.906
Temizer, I. K., A. Güder, & O. G. Çelemli. 2017. Botanical origin and antioxidant activities of propolis from the Irano-Turanian region. Istanbul J. Pharm. 47:107-111.
Torki, M., J. Soltani, & H. Mohammadi. 2015. Effects of adding ethanol extract of propolis and cumin essential oil to diet on the performance, blood parameters, immune response and carcass traits of broiler chicks. Iran. J. Appl. Anim. Sci. 5:911-918.
Wang, B. J., Y. H. Lien, & Z. R. Yu. 2004. Supercritical fluid extractive fractionation-study of the antioxidant activities of propolis. Food Chemist. 86:237-243. https://doi.org/10.1016/j.foodchem.2003.09.031
Wang, J., S. Li, Q. Wang, B. Xin, & H. Wang. 2007. Trophic effect of bee pollen on small intestine in broiler chickens. J. Med. Food. 10:276-280. https://doi.org/10.1089/jmf.2006.215
Wang, S., Q. Ye., Q. Zeng, & S. Qiao. 2019. Functions of macrophages in the maintenance of intestinal homeostasis. J. Immunol. Res. 2019:1-9. https://doi.org/10.1155/2019/1512969
Zafarnejad, K., N. Afzali, & M. Rajabzadeh. 2017. Effect of bee glue on growth performance and immune response of broiler chickens. J. Appl. Anim. Res. 45:280-284. https://doi.org/10.1080/09712119.2016.1174130
Ziaran, H. R., H. R. Rahmani, & J. Pourreza. 2005. Effect of dietary oil extract of propolis on immune response and broiler performance. Pak. J. Biol. Sci. 8:1485-1490. https://doi.org/10.3923/pjbs.2005.1485.1490
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