doi: 10.15389/agrobiology.2020.4.682eng

UDC: 636.5:591.05:539:577.2

Supported financially by Russian Scienсe Foundation (project No. 16-16-10048 P)



V.A. Bagirov1, A.S. Ushakov1, G.K. Duskaev2, O.V. Kvan2,
Sh.G. Rakhmatullin2, E.V. Yausheva2, I.A. Vershinina2

1Ernst Federal Science Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail,;
2Federal Research Centre of Biological Systems and Agrotechnologies RAS, 29, ul. 9 Yanvarya, Orenburg, 460000 Russia, e-mail (* corresponding author),,,,

Bagirov V.A.
Rakhmatullin Sh.G.
Ushakov A.S.
Yausheva E.V.
Duskaev G.K.
Vershinina I.A.
Kvan O.V.

Received January 11, 2020


Today, the use of antibiotics in veterinary medicine, as well as growth stimulants in animal husbandry, is considered the main reason for the development of bacterial resistance to antibiotics. Plant-based water extracts can provide simple new approaches to control pathogenic bacteria. Active search for natural alternative sources of antimicrobials, including wild plants, are almost unlimited source of phytochemicals. Plant-based water extracts can also provide simple new approaches to controlling pathogenic bacteria. Some authors suggest that an increase in broiler growth after adding active components of plants may be associated with an improvement in the microbial composition of the intestine and metabolic function. Other plant substances can improve the profile of unsaturated fatty acids and amino acids in meat. Thus, in order to get a more complete picture of the potential use of plant extracts for the prevention or control of bacterial infections, the most significant studies concern the evaluation of the activity of plant extracts in relation to the quality of products and the intestinal microbiome of farm animals and poultry. The aim of our experiment was to study the effect of Quercus cortex extract on biochemical composition of broiler chicken meat and intestinal microbiomes. The studies were carried out with Smena 8 broiler chickens (the Common Use Center for the scientific equipment of the BST RAS, in 2019). In the experiment, 120 broiler chickens aged 7-day were randomly assigned to 4 groups (n = 30 each, in 4 repetitions). The control broilers were fed the Basic Diet (BD); group I — BD + Quercus cortex extract 1 (1 ml/kg lw); group II — BD + Quercus cortex extract 2 (2 ml/kg lw); group III — BD + Quercus cortex extract 3 (3 ml/kg lw). Analysis of chemical composition of broiler chicken meat showed that the additional inclusion of oak bark extract at a dose of 1 ml/kg of live weight in the diet of the studied poultry helps to improve the quality of meat due to a 27.3 % (р ≤ 0.01) increase in moisture, crude protein and ash, while reducing the level of crude fat. The dietary oak bark extract contributed to an increase in the amount of essential amino acids, for lysine by 1.63-3.43 % (p ≤ 0,01, for leucine-isoleucine by 2.20-5.00 % (p ≤ 0.05), for methionine by 0.55-1.93 % (p ≤ 0.05), for valine by 1.06-1.95 % (p ≤ 0.05), for phenylalanine (group I and II) by 0.45 % and 1.14 %, respectively (p ≤ 0.05), for threonine (group I and II) by 1.07 % (p ≤ 0.05) and 1.82 % (p ≤ 0.01). Levels of non-essential amino acids in the pectoral muscles of broiler chickens compared to control also changed, with the maximum observed for a dosage of 2 ml/kg lw of oak bark extract. The content of unsaturated fatty acids in groups I and III increased compared to the control (for palmitoleic acid by 1.00 and 0.70 %, respectively, p ≤ 0.05). Different dosages of dietary Quercus cortex extract have a significant effect on microbiota of the blind intestine. Changes affect phyla Firmicutes and Bacteroidetes, involved in metabolic energy resorption and degradation of proteins and polysaccharides. The abundance of phylum Bacteroidetes increased 3.96-fold and 2.10-fold in groups I and III compared to the control (p ≤ 0.05), while in group II these bacteria were not found. The number of members of Firmicutes phylum decreased 3.60-fold and 1.47-fold (in groups I and III vs. the control, p ≤ 0.05) while increased 1.26 times in group II vs. the control, p ≤ 0.05 ) Thus, broilers fed 1-3 ml/kg dietary Quercus cortex extract were superior to other birds in terms of amino acid and unsaturated fatty acid levels in carcass due intensification of digestion in intestine, which improves consumer quality of meat.

Keywords: microbiome, broiler chickens, oak bark extract, fatty acids, amino acids.



  1. Abiala M., Olayiwola J., Babatunde O., Aiyelaagbe O., Akinyemi S. Evaluation of therapeutic potentials of plant extracts against poultry bacteria threatening public health. BMC complementary and alternative medicine, 2016, 16: 417 CrossRef
  2. Ali S.M., Siddiqui R., Khan N.A. Antimicrobial discovery from natural and unusual sources. Journal of Pharmacy and Pharmacology, 2018, 70(10): 1287-1300 CrossRef
  3. Al-Tohamy R., Ali S.S., Saad-Allah K., Fareed M., Ali A., El-Badry A., El-Zawawyb N. A., Wua J., Suna J., Maof G., Rupani P.F. Phytochemical analysis and assessment of antioxidant and antimicrobial activities of some medicinal plant species from Egyptian flora. Journal of Applied Biomedicine, 2018, 16(4): 289-300 CrossRef
  4. Santos S.A., Martins C., Pereira C., Silvestre A.J., Rocha S.M. Current challenges and perspectives for the use of aqueous plant extracts in the management of bacterial infections: the case-study of Salmonella enterica Serovars. Int. J. Mol. Sci., 2019, 20(4): 940 CrossRef
  5. Suurbaar J., Mosobil R., Donkor A.M. Antibacterial and antifungal activities and phytochemical profile of leaf extract from different extractants of Ricinus communis against selected pathogens. BMC Res. Notes, 2017, 10(1): 660 CrossRef
  6. Zhu N., Wang J., Yu L., Zhang Q., Chen K., Liu B. Modulation of growth performance and intestinal microbiota in chickens fed plant extracts or virginiamycin. Front. Microbiol., 2019, 10: 1333 CrossRef
  7. Diaz Carrasco J.M., Redondo L.M., Redondo E.A., Dominguez J.E., Chacana A.P., Fernandez Miyakawa M.E. Use of plant extracts as an effective manner to control Clostridium perfringens induced necrotic enteritis in poultry. BioMed Research International, 2016, 2016: 3278359 CrossRef
  8. Ezzat H.N., Abood S.S., Jawad H.S. A review on the effects of neem (Azadirachta indica) as feed additive in poultry production. Jornal of Entomology and Zoology Studies, 2018, 6(1): 1331-1333.
  9. Oyeagu C.E., Mlambo V., Muchenje V., Marume U. Effect of dietary supplementation of aspergillus xylanase on broiler chickens performance. Iranian Journal o Applied Animal Science, 2019, 9(4): 693-708.
  10. Kishawy A.T., Amer S.A., El-Hack M.E., Saadeldin I.M., Swelum A.A. 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 Journal of Animal Sciences, 2019, 32(8): 1161-1171 CrossRef
  11. Mpofu D., Marume U., Mlambo V., Hugo A. The effects of Lippia javanica dietary inclusion on growth performance, carcass characteristics and fatty acid profiles of broiler chickens. Animal Nutrition, 2016, 2(3): 160-167 CrossRef
  12. Díaz Carrasco J.M., Redondo E.A., Pin Viso N.D., Redondo L.M., Farber M.D., Fernández Miyakawa M.E. Tannins and bacitracin differentially modulate gut microbiota of broiler chickens. BioMed Research International, 2018, 2018: 1879168 CrossRef
  13. Tosi G., Massi P., Antongiovanni M., Buccioni A., Minieri S., Marenchino L., Mele M. Efficacy test of a hydrolysable tannin extract against necrotic enteritis in challenged broiler chickens. Italian Journal of Animal Science, 2013, 12: e62 CrossRef
  14. Shokraneh M., Ghalamkari G., Toghyani M., Landy N. Influence of drinking water containing Aloe vera (Aloe barbadensis Miller) gel on growth performance, intestinal microflora, and humoral immune responses of broilers. Veterinary World, 2016, 9(11): 1197-1203 CrossRef
  15. Starčević K., Krstulović L., Brozić D., Maurić M., Stojević Z., Mikulec Ž., Mikulec M., Bajic M., Mašek T. Production performance, meat composition and oxidative susceptibility in broiler chicken fed with different phenolic compounds. J. Sci. Food Agric., 2015, 95(6): 1172-1178 CrossRef
  16. Bourre J.M. Where to find omega-3 fatty acids and how feeding animals with diet enriched in omega-3 fatty acids to increase nutritional value of derived products for human: what is actually useful. J. Nutr. Health Aging, 2005, 9(4): 232-242.
  17. Karimi A., Moradi M.T. Total phenolic compounds and in vitro antioxidant potential of crude methanol extract and the correspond fractions of Quercus brantii L. acorn. Journal of HerbMed Pharmacology, 2015, 4(1): 35-39.
  18. Gessner D.K., Ringseis R., Eder K. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J. Anim. Physiol. Anim. Nutr., 2017, 101(4): 605-628 CrossRef
  19. Mondal S., Haldar S., Saha P., Ghosh T.K. Metabolism and tissue distribution of trace elements in broiler chickens' fed diets containing deficient and plethoric levels of copper, manganese, and zinc. Biol. Trace Elem. Res., 2010, 137(2): 190-205 CrossRef
  20. Schiavone A., Guo K., Tassone S., Gasco L., Hernandez E., Denti R., Zoccarato I. Effects of a natural extract of chestnut wood on digestibility, performance traits, and nitrogen balance of broiler chicks. Poultry Science, 2008, 87(3): 521-527 CrossRef
  21. Tonsor G.T., Wolf C.A. US farm animal welfare: an economic perspective. Animals, 2019, 9(6): 367 CrossRef
  22. Wilson R.T. Domestic livestock in African cities: production, problems and prospects. Open Urban Studies and Demography Journal, 2018, 4(1): 1-14 CrossRef
  23. Nkukwana T.T. Global poultry production: current impact and future outlook on the South African poultry industry. South African Journal of Animal Science, 2018, 48(5): 869-884 CrossRef
  24. Mancabelli L., Ferrario C., Milani C., Mangifesta M., Turroni F., Duranti S., Ventura M. Insights into the biodiversity of the gut microbiota of broiler chickens. Environmental Microbiology, 2016, 18(12): 4727-4738 CrossRef
  25. Duskaev G.K., Rakhmatullin S.G., Kazachkova N.M., Sheida Y.V. Mikolaychik I.N., Morozova L.A., Galiev B.H. Effect of the combined action of Quercus cortex extract and probiotic substances on the immunity and productivity of broiler chickens. Veterinary World, 2018, 11(10): 1416-1422 CrossRef
  26. Meehan C.J., Beiko R.G. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biology and Evolution, 2014, 6: 703-713 CrossRef
  27. Bagirov V.A., Duskaev G.K., Kazachkova N.M., Rakhmatullin S.G., Yausheva E.V., Kosyan D.B., Makaev S.A., Dusaeva K.B. Addition of Quercus cortex extract to broiler diet changes slaughter indicators and biochemical composition of muscle tissue. Agricultural Biology, 2018, 53(4): 799-810 CrossRef
  28. Wang J., Wang X., Li J., Chen Y., Yang W., Zhang L. Effects of dietary coconut oil as a medium-chain fatty acid source on performance, carcass composition and serum lipids in male broilers. Asian-Australasian Journal of Animal Sciences, 2015, 28(2): 223-230 CrossRef
  29. Jamroz D., Orda J., Kamel C., Wiliczkiewicz A., Wertelecki T., Skorupinska J. The influence of phytogenic extracts on performance, nutrient digestibility, carcass characteristics, and gut microbial status in broiler chickens. Journal of Animal and Feed Sciences, 2003, 12(3): 583-596 CrossRef
  30. Tvrzicka E., Kremmyda L.S., Stankova B., Zak, A. Fatty acids as biocompounds: their role in human metabolism, health and disease-a review. Part 1: classification, dietary sources and biological functions. Biomedical Papers of the Medical Faculty of Palacky University in Olomouc, 2011, 155(2): 117-130 CrossRef
  31. Ahmed S.T., Islam M.M., Bostami A.R., Mun H.S., Kim Y.J., Yang C.J. Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by-products. Food Chemistry, 2015, 188: 481-488 CrossRef
  32. Ran C., Hu J., Liu W., Liu Z., He S., Dan B.C., Diem N.N., Ooi E.L., Zhou Z. Thymol and carvacrol affect hybrid tilapia through the combination of direct stimulation and an intestinal microbiota-mediated effect: insights from a germ-free zebrafish model. The Journal of Nutrition, 2016, 146(5): 1132-1140 CrossRef
  33. Chen W.L., Tang S.G., Jahromi M.F., Candyrine S.C., Idrus Z., Abdullah N., Liang J.B. Metagenomics analysis reveals significant modulation of cecal microbiota of broilers fed palm kernel expeller diets. Poultry Science, 2019, 98(1): 56-68 CrossRef
  34. Xiao Y., Xiang Y., Zhou W., Chen J., Li K., Yang, H. Microbial community mapping in intestinal tract of broiler chicken. Poultry Science, 2017, 96(5): 1387-1393 CrossRef
  35. Singh K., Shah T., Deshpande S., Jakhesara S., Koringa P., Rank D. High through put 16S rRNA gene-based pyrosequencing analysis of the fecal microbiota of high FCR and low FCR broiler growers. Molecular Biology Reports, 2012, 39: 10595-10602 CrossRef
  36. Viveros A., Chamorro S., Pizarro M., Arija I., Centeno C., Brenes A. Effects of dietary polyphenol-rich grape products on intestinal microflora and gut morphology in broiler chicks. Poultry Science, 2011; 90(3): 566-578 CrossRef
  37. Molnar A.K., Podmaniczky B., Kurti P., Tenk I., Glavits R., Virag G., Szabo Z. Effect of different concentrations of Bacillus subtilis on growth performance, carcase quality, gut microflora and immune response of broiler chickens. British Poultry Science, 2011, 52: 658-665 CrossRef
  38. Wexler H.M. Bacteroides: the good, the bad, and the Nitty-Gritty. Clinical Microbiology Reviews, 2007, 20: 593-621 CrossRef
  39. Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., Glöckner F. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 2013, 41(1): 1-11 (doi:10.1093/nar/gks808">CrossRef
  40. Fisinin V.I., Ushakov A.S., Duskaev G.K., Kazachkova N.M., Nurzhanov B.S., Rakhmatullin S.G., Levakhin G.I. Mixtures of biologically active substances of oak bark extracts change immunological and productive indicators of broilers. Agricultural Biology [Sel’skokhozyaistvennaya Biologiya], 2018, 53(2): 385-392 CrossRef
  41. Wagle B.R., Upadhyay A., Arsi K., Shrestha S., Venkitanarayanan K., Donoghue A.M., Donoghue D.J. Application of β-resorcylic acid as potential antimicrobial feed additive to reduce Campylobacter colonization in broiler chickens. Frontiers in Microbiology, 2017, 8: 599 CrossRef
  42. Olnood C.G., Beski S.S., Choct M., Iji P.A. Novel probiotics: their effects on growth performance, gut development, microbial community and activity of broiler chickens. Animal Nutrition, 2015, 1(3): 184-191 CrossRef
  43. Hartmann M., Berditsch M., Hawecker J., Ardakani M.F., Gerthsen D., Ulrich A.S. Damage of the bacterial cell envelope by antimicrobial peptides gramicidin S and PGLa as revealed by transmission and scanning electron microscopy. Antimicrobial Agents and Chemotherapy, 2010, 54: 3132-3142 CrossRef
  44. Li Y., Xu Q., Huang Z., Lv L., Liu X., Yin C., Yuan J. Effect of Bacillus subtilis CGMCC 1.1086 on the growth performance and intestinal microbiota of broilers. Journal of Applied Microbiology, 2016, 120(1): 195-204 CrossRef
  45. Deryabin D., Tolmacheva A. Antibacterial and anti-quorum sensing molecular composition derived from Quercus cortex (Oak bark) extract. Molecules, 2015, 20(9): 17093-17108 CrossRef
  46. Cushnie T.P.T., Lamb A.J. Recent advances in understanding the antibacterial properties of flavonoids. International Journal of Antimicrobial Agents, 2011, 38(2): 99-107 CrossRef
  47. Manzanilla E.G., Perez J.F., Martin M., Kamel C., Baucells F., Gasa J. Effect of plant extracts and formic acid on the intestinal equilibrium of early-weaned pigs. Journal of Animal Science, 2004, 82(11): 3210-3218 CrossRef
  48. Wei H., Chen G., Wang R., Peng, J. Oregano essential oil decreased susceptibility to oxidative stress-induced dysfunction of intestinal epithelial barrier in rats. Journal of Functional Foods, 2015, 18: 1191-1199 CrossRef
  49. Mansoori B., Acamovic T. The effect of tannic acid on the excretion of endogenous methionine, histidine and lysine with broilers. Animal Feed Science and Technology, 2007, 134(3-4): 198-210 CrossRef
  50. Kreydiyyeh S.I. Inhibitors in tea of intestinal absorption of phenylalanine in rats. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 1996, 113(1): 67-71 CrossRef
  51. Koreleski J., Swiatkiewicz S. Dietary supplementation with plant extracts, xantophylls and synthetic antioxidants: effect on fatty acid profile and oxidative stability of frozen stored chicken breast meat. Journal of Animal and Feed Sciences, 2007, 16(3): 463-471 CrossRef
  52. Wang Y., Dong Z., Song D., Zhou H., Wang W., Miao H., Li. A. Effects of microencapsulated probiotics and prebiotics on growth performance, antioxidative abilities, immune functions, and caecal microflora in broiler chickens. Food and Agricultural Immunology, 2018, 29(1): 859-869 CrossRef
  53. Cui Y.M., Wang J., Lu W., Zhang H.J., Wu S.G., Qi G.H. Effect of dietary supplementation with Moringa oleifera leaf on performance, meat quality, and oxidative stability of meat in broilers. Poultry Science, 2018, 97(8): 2836-2844 CrossRef
  54. Kumar P., Patra A.K., Mandal G.P., Debnath B.C. Carcass characteristics, chemical and fatty acid composition and oxidative stability of meat from broiler chickens fed black cumin (Nigella sativa) seeds. J. Anim. Physiol. Anim. Nutr., 2018, 102(3): 769-779 CrossRef
  55. Ubua J.A., Ozung P.O., Inagu P.G., Aboluja B.A. Blood characteristics of broiler chickens as influenced by dietary inclusion of neem (Azadirachta indica) leaf meal. Canadian Journal of Agriculture and Crops, 2018, 3(2): 72-80 CrossRef
  56. Patel A.P., Bhagwat S.R., Pawar M.M., Prajapati K.B., Chauhan H.D., Makwana R.B. Evaluation of Emblica officinalis fruit powder as a growth promoter in commercial broiler chickens. Veterinary World, 2016, 9(2): 207-210 CrossRef
  57. Sizova E., Miroshnikov S., Lebedev S., Kudasheva A., Ryabov N. To the development of innovative mineral additives based on alloy of Fe and Co antagonists as an example. Agricultural Biology [Sel’skokhozyaistvennaua Biologiya], 2016, 51(4): 553-562. CrossRef
  58. Nworgu F.C., Ogungbenro S.A., Solesi K.S. Performance and some blood chemistry indices of broiler chicken served fluted pumpkin (Telfaria occidentalis) leaves extract supplement. American-Eurasian J. Agric & Environ. Sci., 2007, 2(1): 90-98.
  59. Alagawany M., El-Hack M.E., Farag M.R., Sachan S., Karthik K., Dhama K. The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environmental Science and Pollution Research, 2018, 25(11): 10611-10618 CrossRef
  60. Gotep J.G., Tanko J.T., Forcados G.E., Muraina I.A., Ozele N., Dogonyaro B.B., Oladipo O.O., Makoshi M.S., Akanbi O.B., Kinjir H., Samuel A.L., Onyiche T.E., Ochigbo G.O., Aladelokun O.B., Ozoani H.A., Viyoff V.Z., Dapuliga C.C., Atiku A.A., Okewole P.A., Shamaki D., Ahmed M.S., Nduaka C.I. Therapeutic and safety evaluation of combined aqueous extracts of azadirachta indica and Khaya senegalensis in chickens experimentally infected with eimeria oocysts. Journal of Parasitology Research, 2016, 2016: 4692424 CrossRef
  61. Heymsfield S.B., Wadden T.A. Mechanisms, pathophysiology, and management of obesity. New England Journal of Medicine, 2017, 376(3): 254-266 CrossRef






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