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http://dx.doi.org/10.5713/ajas.20.0379

Effects of dietary flavonoids on performance, blood constituents, carcass composition and small intestinal morphology of broilers: a meta-analysis  

Prihambodo, Tri Rachmanto (Graduate Study Program of Nutrition and Feed Science, Faculty of Animal Science, IPB University)
Sholikin, Muhammad Miftakhus (Graduate Study Program of Nutrition and Feed Science, Faculty of Animal Science, IPB University)
Qomariyah, Novia (Graduate Study Program of Nutrition and Feed Science, Faculty of Animal Science, IPB University)
Jayanegara, Anuraga (Animal Feed and Nutrition Modelling (AFENUE) Research Group, Faculty of Animal Science, IPB University)
Batubara, Irmanida (Department of Chemistry, Faculty of Mathematics and Natural Sciences, IPB University)
Utomo, Desianto Budi (PT. Charoen Pokphand)
Nahrowi, Nahrowi (Department of Nutrition and Feed Technology, Faculty of Animal Science, IPB University)
Publication Information
Animal Bioscience / v.34, no.3_spc, 2021 , pp. 434-442 More about this Journal
Abstract
Objective: This study aims to evaluate the influence of dietary flavonoids on the growth performance, blood and intestinal profiles, and carcass characteristics of broilers by employing a meta-analysis method. Methods: A database was built from published studies which have reported on the addition of various levels of flavonoids from herbs into broiler diets and then monitored growth performance, blood constituents, carcass proportion and small intestinal morphology. A total of 42 articles were integrated into the database. Several forms of flavonoids in herbs were applied in the form of unextracted and crude extracts. The database compiled was statistically analyzed using mixed model methodology. Different studies were considered as random effects, and the doses of flavonoids were treated as fixed effects. The model statistics used were the p-values and the Akaike information criterion. The significance of an effect was stated when its p-value was <0.05. Results: Dietary flavonoids increased (quadratic pattern; p<0.05) the average daily gain of broilers in the finisher phase. There was a reduction (p<0.01) in the feed conversion ratio of the broilers both in the starter (linear pattern) and finisher phases (quadratic pattern). The mortality rate tended to decrease linearly (p<0.1) with the addition of flavonoids, while the carcass parameter was generally not influenced. A reduction (p<0.001) in cholesterol and malondialdehyde concentrations (both linearly) was observed, while super oxide dismutase activity increased linearly (p<0.001). Increasing the dose of flavonoids increased (p<0.01) the villus height (VH) and villus height and crypt depth (VH:CD) ratio (p<0.05) in the duodenum. Similarly, the VH:CD ratio was elevated (p<0.001) in the jejunum following flavonoid supplementation. Conclusion: Increasing levels of flavonoids in broilers diet leads to an improvement in growth performance, blood constituents, carcass composition and small intestinal morphology.
Keywords
Broiler; Flavonoid; Growth Performance; Carcass and Blood Composition; Small Intestinal Morphology; Meta-analysis;
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1 Song D, Wang YW, Hou YJ, Dong ZL, Wang WW, Li AK. The effects of dietary supplementation of microencapsulated Enterococcus faecalis and the extract of Camellia oleifera seed on growth performance, immune functions, and serum biochemical parameters in broiler chickens. J Anim Sci 2016; 94:3271-7. https://doi.org/10.2527/jas.2016-0286   DOI
2 Kishawy ATY, Amer SA, Abd El-Hack ME, Saadeldin IM, Swelum AA. 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 2019;32:1161-71. https://doi.org/10.5713/ajas.18.0522   DOI
3 Habibian M, Sadeghi G, Karimi A. Comparative effects of powder, aqueous and methanolic extracts of purslane (Portulaca oleracea L.) on growth performance, antioxidant status, abdominal fat deposition and plasma lipids in broiler chickens. Anim Prod Sci 2019;59:89-100. https://doi.org/10.1071/AN17352   DOI
4 Ahmadipour B, Khajali F. Expression of antioxidant genes in broiler chickens fed nettle (Urtica dioica) and its link with pulmonary hypertension. Anim Nutr 2019;5:264-9. https://doi.org/10.1016/j.aninu.2019.04.004   DOI
5 Zhang BW, Li X, Sun WL, et al. Dietary flavonoids and acarbose synergistically inhibit α-glucosidase and lower postprandial blood glucose. J Agric Food Chem 2017;65: 8319-30. https://doi.org/10.1021/acs.jafc.7b02531   DOI
6 Borradaile NM, Carroll KK, Kurowska EM. Regulation of HepG2 cell apolipoprotein B metabolism by the citrus flavanones hesperetin and naringenin. Lipids 1999;34:591-8. https://doi.org/10.1007/s11745-999-0403-7   DOI
7 Rubio MS, Laurentiz AC, Sobrane F°ST, et al. Performance and serum biochemical profile of broiler chickens supplemented with Piper cubeba ethanolic extract. Braz J Poult Sci 2019;21:1-8. https://doi.org/10.1590/1806-9061-2018-0789   DOI
8 Saeid JM, Mohamed AB, AL-Baddy MA. Effect of aqueous extract of ginger (Zingiber officinale) on blood biochemistry parameters of broiler. Int J Poult Sci 2010;9:944-7. https://doi.org/10.3923/ijps.2010.944.947   DOI
9 Shen MM, Zhang LL, Chen YN, et al. Effects of bamboo leaf extract on growth performance, meat quality, and meat oxidative stability in broiler chickens. Poult Sci 2019;98:6787-96. https://doi.org/10.3382/ps/pez404   DOI
10 Shirzadi H, Shariatmadari F, Torshizi MAK, et al. Plant extract supplementation as a strategy for substituting dietary antibiotics in broiler chickens exposed to low ambient temperature. Arch Anim Nutr 2020;74:206-21. https://doi.org/10.1080/1745039X.2019.1693860   DOI
11 St-Pierre NR. Invited review: integrating quantitative findings from multiple studies using mixed model methodology. J Dairy Sci 2001;84:741-55. https://doi.org/10.3168/jds.S0022-0302(01)74530-4   DOI
12 Xu H. Inhibition kinetics of flavonoids on yeast α-glucosidase merged with docking simulations. Protein Pept Lett 2010;17: 1270-9. https://doi.org/10.2174/092986610792231492   DOI
13 Teteh A, Lawson E, Tona K, Decuypere E, Gbeassor M. Moringa oleifera leave: hydro-alcoholic extract and effects on growth performance of broilers. Int J Poult Sci 2013;12:401-5. https://doi.org/10.3923/ijps.2013.401.405   DOI
14 Vase-Khavari K, Mortezavi SH, Rasouli B, Khusro A, Salem AZM, Seidavi A. The effect of three tropical medicinal plants and superzist probiotic on growth performance, carcass characteristics, blood constitutes, immune response, and gut microflora of broiler. Trop Anim Health Prod 2019;51: 33-42. https://doi.org/10.1007/s11250-018-1656-x   DOI
15 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. Poult Sci 2011;90:566-78. https://doi.org/10.3382/ps.2010-00889   DOI
16 Chew YL, Chan EWL, Tan PL, Lim YY, Stanslas J, Goh JK. Assessment of phytochemical content, polyphenolic composition, antioxidant and antibacterial activities of Leguminosae medicinal plants in Peninsular Malaysia. BMC Complement Altern Med 2010;11:12. https://doi.org/10.1186/1472-6882-11-12   DOI
17 Kamboh AA, Zhu WY. Effect of increasing levels of bioflavonoids in broiler feed on plasma anti-oxidative potential, lipid metabolites, and fatty acid composition of meat. Poult Sci 2013;92:454-61. https://doi.org/10.3382/ps.2012-02584   DOI
18 Skibola CF, Smith MT. Potential health impacts of excessive flavonoid intake. Free Radic Biol Med 2000;29:375-83. https://doi.org/10.1016/S0891-5849(00)00304-X   DOI
19 Herrero-Encinas J, Blanch M, Pastor JJ, Mereu A, Ipharraguerre IR, Menoyo D. Effects of a bioactive olive pomace extract from Olea europaea on growth performance, gut function, and intestinal microbiota in broiler chickens. Poult Sci 2020; 99:2-10. https://doi.org/10.3382/ps/pez467   DOI
20 Abdel-Moneim MA, Hammady GA, Hassanin MS, El-Chaghaby GA. The effect of using marjoram extract as natural growth promoter on the performance and intestinal bacteria of broiler chickens. J Anim Poult Prod 2015;6:647-56. https://doi.org/10.21608/jappmu.2015.52946   DOI
21 Jobe MC, Ncobela CN, Kunene NW, Opoku AR. Effects of Cassia abbreviata extract and stocking density on growth performance, oxidative stress and liver function of indigenous chickens. Trop Anim Health Prod 2019;51:2567-74. https://doi.org/10.1007/s11250-019-01979-y   DOI
22 Jiang XR, Zhang HJ, Wang J, et al. Effect of dried tangerine peel extract supplementation on the growth performance and antioxidant status of broiler chicks. Ital J Anim Sci 2016; 15:642-8. https://doi.org/10.1080/1828051X.2016.1222246   DOI
23 Khoobani M, Hasheminezhad SH, Javandel F, et al. Effects of dietary chicory (Chicorium intybus L.) and probiotic blend as natural feed additives on performance traits, blood biochemistry, and gut microbiota of broiler chickens. Antibiotics 2020;9:5. https://doi.org/10.3390/antibiotics9010005   DOI
24 Tadera K, Minami Y, Takamatsu K, Matsuoka T. Inhibition of α-glucosidase and α-amylase by flavonoids. J Nutr Sci Vitaminol 2006;52:149-53. https://doi.org/10.3177/jnsv.52.149   DOI
25 Sauvant D, Schmidely P, Daudin JJ, St-Pierre NR. Meta-analyses of experimental data in animal nutrition. Animal 2008;2:1203-14. https://doi.org/10.1017/S1751731108002280   DOI
26 Srividya AR, Dhanabal SP, Misra VK, Suja G. Antioxidant and antimicrobial activity of Alpinia officinarum. Indian J Pharm Sci 2010;72:145-8. https://doi.org/10.4103/0250-474X.62233   DOI
27 Abolfathi ME, Tabeidian SA, Shahraki ADF, Tabatabaei SN, Habibian M. Comparative effects of n-hexane and methanol extracts of elecampane (Inula helenium L.) rhizome on growth performance, carcass traits, feed digestibility, intestinal antioxidant status and ileal microbiota in broiler chickens. Arch Anim Nutr 2019;73:88-110. https://doi.org/10.1080/1745039X.2019.1581027   DOI
28 Nardoia M, Romero C, Brenes A, et al. Addition of fermented and unfermented grape skin in broilers' diets: effect on digestion, growth performance, intestinal microbiota and oxidative stability of meat. Animal 2020;14:1371-81. https://doi.org/10.1017/S1751731119002933   DOI
29 Nkukwana TT, Muchenje V, Masika PJ, Hoffman LC, Dzama K. The effect of Moringa oleifera leaf meal supplementation on tibia strength, morphology and inorganic content of broiler chickens. S Afr J Anim Sci 2014;44:228-39. https://doi.org/10.4314/sajas.v44i3.4   DOI
30 Rosak C, Mertes G. Effects of acarbose on proinsulin and insulin secretion and their potential significance for the intermediary metabolism and cardiovascular system. Curr Diabetes Rev 2009;5:157-64. https://doi.org/10.2174/157339909788920910   DOI
31 Biavatti MW, Bellaver MH, Volpato L, Costa C, Bellaver C. Preliminary studies of alternative feed additives for broilers: Alternanthera brasiliana extract, propolis extract and linseed oil. Braz J Poult Sci 2003;5:147-51. https://doi.org/10.1590/S1516-635X2003000200009   DOI
32 Ammar NM, Al-Okbi SY. Effect of four flavonoids on blood glucose of rats. Arch Pharm Res 1988;11:166-8. https://doi.org/10.1007/BF02857723   DOI
33 Zhou Y, Mao S, Zhou M. Effect of the flavonoid baicalein as a feed additive on the growth performance, immunity, and antioxidant capacity of broiler chickens. Poult Sci 2019;98: 2790-9. https://doi.org/10.3382/ps/pez071   DOI
34 Maron DF, Smith TJS, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Glob Health 2013;9:48. https://doi.org/10.1186/1744-8603-9-48   DOI
35 Huyghebaert G, Ducatelle R, Immerseel FV. An update on alternatives to antimicrobial growth promoters for broilers. Vet J 2011;187:182-8. https://doi.org/10.1016/j.tvjl.2010.03.003   DOI
36 Abdel-Azeem AS, Basyony M. Some blood biochemical, antioxidant biomarkers, lipid peroxidation, productive performance and carcass traits of broiler chicks supplemented with Alpinia galangal rhizomes extract during heat stress. Egypt Poult Sci J 2019;39:345-63. https://doi.org/10.21608/epsj.2019.35009   DOI
37 Aengwanich W, Suttajit M, Narkkong NA. Effects of polyphenols extracted from tamarind (Tamarindus indica L.) seed coat on differential white blood cell count in broilers (Gallus domesticus) exposed to high environmental temperature. Int J Poult Sci 2009;8:957-62. https://doi.org/10.3923/ijps.2009.957.962   DOI
38 Arlette NT, Nadia NAC, Jeanette Y, Gertrude MT, Josue WP, Mbida M. Anticoccidial effects of Ageratum conyzoides (Asteraceae) and Vernonia amygdalina (Asteraceae) leaves extracts on broiler chickens. South Asian J Parasitol 2019;2: 1-10. https://doi.org/10.9734/SAJP/2019/43746   DOI
39 Wang L, Piao XL, Kim SW, Piao XS, Shen YB, Lee HS. Effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities in broiler chickens under high ambient temperature. Poult Sci 2008;87:1287-94. https://doi.org/10.3382/ps.2008-00023   DOI
40 Zhang X, Cao F, Sun Z, et al. Effect of feeding Aspergillus niger-fermented Ginkgo biloba-leaves on growth, small intestinal structure and function of broiler chicks. Livest Sci 2012;147: 170-80. https://doi.org/10.1016/j.livsci.2012.04.018   DOI
41 Salam S, Sunarti D, dan Isroli. The effect of black cumin (Nigella sativa) grinding supplementation on aspartate aminotransferase (AST), alanine aminotransferase (ALT) and liver weight on broiler. J Peternakan Indones 2014;16:40-5. https://doi.org/10.25077/jpi.16.1.40-45.2014   DOI
42 Akbarian A, Golian A, Gilani A, et al. Effect of feeding citrus peel extracts on growth performance, serum components, and intestinal morphology of broilers exposed to high ambient temperature during the finisher phase. Livest Sci 2013;157: 490-7. https://doi.org/10.1016/j.livsci.2013.08.010   DOI
43 Daramola OT. Medicinal plants leaf meal supplementation in broiler chicken diet: effects on performance characteristics, serum metabolite and antioxidant status. Anim Res Int 2019; 16:3334-42.
44 Oso AO, Suganthi RU, Reddy GBM, et al. Effect of dietary supplementation with phytogenic blend on growth performance, apparent ileal digestibility of nutrients, intestinal morphology, and cecal microflora of broiler chickens. Poult Sci 2019;98:4755-66. https://doi.org/10.3382/ps/pez191   DOI
45 Park JH, Pi SH, Kim IH. Growth performance, blood profile, nutrient digestibility and meat quality of broilers fed on diets supplemented with Scutellaria baicalensis extract. Eur Poult Sci 2016;80:1-10. https://doi.org/10.1399/eps.2016.155   DOI
46 Park JH, Kang SN, Chu GM, Jin SK. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts. Livest Sci 2014;165:87-94. https://doi.org/10.1016/j.livsci.2014.04.014   DOI
47 Sadeghi G, Karimi A, Shafeie F, Vaziry A, Farhadi D. The effects of purslane (Portulaca oleracea L.) powder on growth performance, carcass characteristics, antioxidant status, and blood metabolites in broiler chickens. Livest Sci 2016;184:35-40. https://doi.org/10.1016/j.livsci.2015.12.003   DOI
48 Pournazari M, AA-Qotbi A, Seidavi A, Corazzin M. Prebiotics, probiotics and thyme (Thymus vulgaris) for broilers: performance, carcass traits and blood variables. Rev Colomb Cienc Pecu 2017;30:3-10. https://doi.org/10.17533/udea.rccp.v30n1a01   DOI
49 Ologhobo AD, Apata DF, Oyejide A, Akinpelu O. Toxicity of raw limabeans (Phaseolus lunatus L.) and limabean fractions for growing chicks. Br Poult Sci 1993;34:505-22. https://doi.org/10.1080/00071669308417606   DOI
50 Ouyang K, Xu M, Jiang Y, Wang W. Effects of alfalfa flavonoids on broiler performance, meat quality, and gene expression. Can J Anim Sci 2016;96:332-41. https://doi.org/10.1139/cjas-2015-0132   DOI
51 Rashidi N, Ghorbani MR, Tatar A, Salari S. Response of broiler chickens reared at high density to dietary supplementation with licorice extract and probiotic. J Anim Physiol Anim Nutr 2019;103:100-7. https://doi.org/10.1111/jpn.13007   DOI
52 Pirgozliev V, Mansbridge SC, Rose SP, Lillehoj HS, Bravo D. Immune modulation, growth performance, and nutrient retention in broiler chickens fed a blend of phytogenic feed additives. Poult Sci 2019;98:3443-9. https://doi.org/10.3382/ps/pey472   DOI
53 Placha I, Takacova J, Ryzner M, et al. Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. Br Poult Sci 2014;55:105-14. https://doi.org/10.1080/00071668.2013.873772   DOI
54 Rahimi S, Teymouri Zadeh Z, Karimi Torshizi MA, Omidbaigi R, Rokni H. Effect of the three herbal extracts on growth performance, immune system, blood factors and intestinal selected bacterial population in broiler chickens. J Agric Sci Technol 2011;13:527-39.
55 Cho M, Smit MN, He L, Kopmels FC, Beltranena E. Effect of feeding zero- or high-tannin faba bean cultivars and dehulling on growth performance, carcass traits and yield of saleable cuts of broiler chickens. J Appl Poult Res 2019;28:1305-23. https://doi.org/10.3382/japr/pfz099   DOI
56 Bai S, He C, Zhang K, et al. Effects of dietary inclusion of Radix bupleuri and Radix astragali extracts on the performance, intestinal inflammatory cytokines expression, and hepatic antioxidant capacity in broilers exposed to high temperature. Anim Feed Sci Technol 2020;259:114288. https://doi.org/10.1016/j.anifeedsci.2019.114288   DOI
57 Tirawattanawanich C, Chantakru S, Nimitsantiwong W, Tongyai S. The effects of tropical environmental conditions on the stress and immune responses of commercial broilers, Thai indigenous chickens, and crossbred chickens. J Appl Poult Res 2011;20:409-20. https://doi.org/10.3382/japr.2010-00190   DOI
58 Awad EA, Najaa M, Zulaikha ZA, Zulkifli I, Soleimani AF. Effects of heat stress on growth performance, selected physiological and immunological parameters, caecal microflora, and meat quality in two broiler strains. Asian-Australas J Anim Sci 2020;33:778-87. https://doi.org/10.5713/ajas.19.0208   DOI
59 He J, Ma L, Qiu J, et al. Effects of compound organic acid calcium on growth performance, hepatic antioxidation and intestinal barrier of male broilers under heat stress. Asian-Australas J Anim Sci 2020;33:1156-66. https://doi.org/10.5713/ajas.19.0274   DOI
60 Vidanarachchi JK, Mikkelsen LL, Constantinoiu CC, Choct M, Iji PA. Natural plant extracts and prebiotic compounds as alternatives to antibiotics in broiler chicken diets in a necrotic enteritis challenge model. Anim Prod Sci 2013;53: 1247-59. https://doi.org/10.1071/AN12374   DOI
61 Dong ZL, Wang YW, Song D, et al. Effects of microencapsulated probiotics and plant extract on antioxidant ability, immune status and caecal microflora in Escherichia coli K88-challenged broiler chickens. Food Agric Immunol 2019;30: 1123-34. https://doi.org/10.1080/09540105.2019.1664419   DOI
62 Brenes A, Viveros A, Goni I, Centeno C, Saura-Calixto F, Arija I. Effect of grape seed extract on growth performance, protein and polyphenol digestibilities, and antioxidant activity in chickens. Span J Agric Res 2010;8:326-33. https://doi.org/10.5424/sjar/2010082-1199   DOI
63 Chamorro S, Viveros A, Centeno C, Romero C, Arija I, Brenes A. Effects of dietary grape seed extract on growth performance, amino acid digestibility and plasma lipids and mineral content in broiler chicks. Animal 2013;7:555-61. https://doi.org/10.1017/S1751731112001851   DOI
64 Dilawar MA, Saturno JFL, Mun HS, Kim DH, Jeong MG, Yang CJ. Influence of two plant extracts on broiler performance, oxidative stability of meat and odorous gas emissions from excreta. Ann Anim Sci 2019;19:1099-113. https://doi.org/10.2478/aoas-2019-0046   DOI
65 Duarte CRA, Eyng C, Murakami AE, Santos TC. Intestinal morphology and activity of digestive enzymes in broilers fed crude propolis. Can J Anim Sci 2014;94:105-14. https://doi.org/10.4141/cjas2013-059   DOI
66 Goodarzi M, Landy N, Nanekarani S. Effect of onion (Allium cepa L.) as an antibiotic growth promoter substitution on performance, immune responses and serum biochemical parameters in broiler chicks. Health 2013;5:1210-5. https://doi.org/10.4236/health.2013.58164   DOI
67 Tim Cushnie TP, Lamb AJ. Antimicrobial activity of flavonoids. Int J Antimicrob Agents 2005;26:343-56. https://doi.org/10.1016/j.ijantimicag.2005.09.002   DOI
68 Tekce E, Cinar K, Bayraktar B, Takma C, Gul M. Effects of an essential oil mixture added to drinking water for temperature-stressed broilers: performance, meat quality, and thiobarbituric acid-reactive substances. J Appl Poult Res 2020;29: 77-84. https://doi.org/10.3382/japr/pfz030   DOI