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Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Effects of phytogenic inclusion level on broiler carcass yield, meat antioxidant capacity, availability of dietary energy, and expression of intestinal genes relevant for nutrient absorptive and cell growth–protein synthesis metabolic functions

Konstantinos C. Mountzouris A B , Vasileios Paraskeuas A , Eirini Griela A , George Papadomichelakis A and Konstantinos Fegeros A
+ Author Affiliations
- Author Affiliations

A Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, Athens 11855, Greece.

B Corresponding author. Email: kmountzouris@aua.gr

Animal Production Science 60(2) 242-253 https://doi.org/10.1071/AN18700
Submitted: 14 November 2018  Accepted: 4 May 2019   Published: 30 October 2019

Abstract

Context: Phytogenic applications in animal nutrition currently attract worldwide scientific attention for their potential to contribute positively to sustainable and high-quality animal production. However, further understanding and substantiation of dietary phytogenic functions is required.

Aims: The inclusion level of a phytogenic premix (PP) comprising functional flavouring substances from ginger, lemon balm, oregano and thyme was studied for its effects on broiler growth performance, carcass traits, nutrient digestibility, liver and meat total antioxidant capacity (TAC), and lipid oxidation. The expression of genes for nutrient transporter proteins (SGLT1, GLUT2, PEPT1, BOAT and LAT1), for FABP2 involved in cellular fatty acid uptake and metabolism, and for the mTORC1 complex relevant for protein synthesis were profiled along the intestine.

Methods: One-day-old Cobb broiler chickens (n = 500) were assigned to four treatments with five replicates of 25 chickens each. Starter (1–10 days), grower (11–22 days) and finisher (23–42 days) basal diets were supplemented with four levels of PP inclusion as treatments: 0, 750, 1000 and 2000 mg/kg diet, termed control, PP750, PP1000 and PP2000. Feed and water were available ad libitum. Data were analysed by ANOVA, taking the treatment as fixed effect. Statistically significant (P ≤ 0.05) effects were further analysed and means were compared using Tukey’s HSD test. Polynomial contrasts tested the linear and quadratic effect of PP inclusion levels.

Key results: Growth performance responses were not improved significantly (P > 0.05) by PP inclusion level. However, carcass (P = 0.030) and breast meat yield (P = 0.023) were higher in PP1000 than in the control. In addition, PP1000 had higher (P = 0.049) apparent metabolisable energy than PP2000 and the control. Increasing PP inclusion level increased breast (P = 0.005), thigh (P = 0.002) and liver (P = 0.040) TAC. Breast and thigh meat TAC reached a plateau at PP1000, whereas liver TAC continued to increase linearly. Lipid oxidation in breast meat and liver was delayed linearly (P ≤ 0.05) with increasing PP inclusion level. Expression of genes SGLT1, GLUT2, PEPT1, BOAT and FABP2 were not affected by PP inclusion. However, PP inclusion affected the expression of LAT1 (P < 0.001) in jejunum and of mTORC1 in duodenum (P = 0.010) and ceca (P = 0.025). In particular, expression increased with increasing PP inclusion level in a linear and quadratic pattern depending on the intestinal segment.

Conclusions: Overall, PP inclusion at 1000 mg/kg diet improved carcass and breast yield, dietary available energy, and overall meat and liver TAC. Preliminary evidence was highlighted for effects of PP in promoting expression of genes relevant for muscle protein synthesis.

Implications: This study has contributed new information on effects of a phytogenic premix on broiler meat yield and antioxidant capacity, digestibility, absorption and metabolic functions, further supporting phytogenic benefits for broiler production.

Additional keywords: essential oils, gut, meat quality, poultry.


References

Akbarian A, Michiels J, Golian A, Buyse J, Wang Y, De Smet S (2014) Gene expression of heat shock protein 70 and antioxidant enzymes, oxidative status, and meat oxidative stability of cyclically heat-challenged finishing broilers fed Origanum compactum and Curcuma xanthorrhiza essential oils. Poultry Science 93, 1930–1941.
Gene expression of heat shock protein 70 and antioxidant enzymes, oxidative status, and meat oxidative stability of cyclically heat-challenged finishing broilers fed Origanum compactum and Curcuma xanthorrhiza essential oils.Crossref | GoogleScholarGoogle Scholar | 24931966PubMed |

Amad AA, Manner K, Wendler KR, Neumann K, Zentek J (2011) Effects of a phytogenic feed additive on growth performance and ileal nutrient digestibility in broiler chickens. Poultry Science 90, 2811–2816.
Effects of a phytogenic feed additive on growth performance and ileal nutrient digestibility in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 22080020PubMed |

Avila-Ramos F, Pro-Martinez A, Sosa-Montes E, Cuca-Garcia JM, Becerril-Perez CM, Figueroa-Velasco JL, Narciso-Gaytan C (2012) Effects of dietary oregano essential oil and vitamin E on the lipid oxidation stability of cooked chicken breast meat. Poultry Science 91, 505–511.
Effects of dietary oregano essential oil and vitamin E on the lipid oxidation stability of cooked chicken breast meat.Crossref | GoogleScholarGoogle Scholar | 22252366PubMed |

Batal AB, Parsons CM (2002) Effects of age on nutrient digestibility in chicks fed different diets Poultry Science 81, 400–407.
Effects of age on nutrient digestibility in chicks fed different dietsCrossref | GoogleScholarGoogle Scholar | 11902418PubMed |

Botsoglou NA, Fletouris DJ, Papageorgiou GE, Vassilopoulos VN, Mantis AJ, Trakatellis AG (1994) A rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissues, food, and feedstuff samples. Journal of Agricultural and Food Chemistry 42, 1931–1937.
A rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissues, food, and feedstuff samples.Crossref | GoogleScholarGoogle Scholar |

Botsoglou NA, Florou-Paneri P, Christaki E, Fletouris DJ, Spais AB (2002) Effect of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues. British Poultry Science 43, 223–230.
Effect of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues.Crossref | GoogleScholarGoogle Scholar | 12047086PubMed |

Bravo D, Utterback P, Parsons CM (2011) Evaluation of a mixture of carvacrol, cinnamaldehyde and capsicum oleoresin for improving growth performance and metabolizable energy in broiler chicks fed corn and soybean meal. Journal of Applied Poultry Research 20, 115–120.
Evaluation of a mixture of carvacrol, cinnamaldehyde and capsicum oleoresin for improving growth performance and metabolizable energy in broiler chicks fed corn and soybean meal.Crossref | GoogleScholarGoogle Scholar |

Bravo D, Pirgozliev V, Rose SP (2014) A mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin improves energy utilization and growth performance of broiler chickens fed maize-based diet. Journal of Animal Science 92, 1531–1536.
A mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin improves energy utilization and growth performance of broiler chickens fed maize-based diet.Crossref | GoogleScholarGoogle Scholar | 24496847PubMed |

Brenes A, Roura E (2010) Essential oils in broiler nutrition: main effects and modes of action. Animal Feed Science and Technology 158, 1–14.
Essential oils in broiler nutrition: main effects and modes of action.Crossref | GoogleScholarGoogle Scholar |

Cao G, Prior R (1999) Measurement of oxygen radical absorbance capacity in biological samples. Methods in Enzymology 299, 50–62.
Measurement of oxygen radical absorbance capacity in biological samples.Crossref | GoogleScholarGoogle Scholar | 9916196PubMed |

Cao L, Yang XJ, Li ZJ, Sun FF, Wu XH, Yao JH (2012) Reduced lesions in chickens with Clostridium perfringens-induced necrotic enteritis by Lactobacillus fermentum 1.2029. Poultry Science 91, 3065–3071.
Reduced lesions in chickens with Clostridium perfringens-induced necrotic enteritis by Lactobacillus fermentum 1.2029.Crossref | GoogleScholarGoogle Scholar | 23155014PubMed |

Chen X, Naehrer K, Applegate T (2016) Interactive effects of dietary protein concentration and aflatoxin B1 on performance, nutrient digestibility, and gut health in broiler chicks. Poultry Science 95, 1312–1325.
Interactive effects of dietary protein concentration and aflatoxin B1 on performance, nutrient digestibility, and gut health in broiler chicks.Crossref | GoogleScholarGoogle Scholar | 26944977PubMed |

Choct M (2009) Managing gut health through nutrition. British Poultry Science 50, 9–15.
Managing gut health through nutrition.Crossref | GoogleScholarGoogle Scholar | 19234925PubMed |

Council of the European Union (2007) Council Directive of 28 June 2007 laying down minimum rules for the protection of chickens kept for meat production. Official Journal of the European Union L182, 19–28.

Council of the European Union (2010) Directive of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union L276, 33–79.

Deng H, Zheng A, Liu G, Chang W, Zhang S, Cai H (2014) Activation of mammalian target of rapamycin signaling in skeletal muscle of neonatal chicks: effects of dietary leucine and age Poultry Science 93, 114–121.
Activation of mammalian target of rapamycin signaling in skeletal muscle of neonatal chicks: effects of dietary leucine and ageCrossref | GoogleScholarGoogle Scholar | 24570430PubMed |

Falowo AB, Fayemi PO, Muchenje V (2014) Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: a review. Food Research International 64, 171–181.
Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: a review.Crossref | GoogleScholarGoogle Scholar | 30011637PubMed |

Fernandez-Alarcon M, Trottier N, Steibel J, Lunedo R, Campos D, Santana A, Pizauro J, Furlan R, Furlan L (2017) Interference of age and supplementation of direct-fed microbial and essential oil in the activity of digestive enzymes and expression of genes related to transport and digestion of carbohydrates and proteins in the small intestine of broilers. Poultry Science 96, 2920–2930.
Interference of age and supplementation of direct-fed microbial and essential oil in the activity of digestive enzymes and expression of genes related to transport and digestion of carbohydrates and proteins in the small intestine of broilers.Crossref | GoogleScholarGoogle Scholar | 28339792PubMed |

Ferrando C, Vergara P, Jiménez M, Goñalons E (1987) Study of the rate of passage of food with chromium-mordanted plant cells in chickens (Gallus gallus). Quarterly Journal of Experimental Physiology (Cambridge, England) 72, 251–259.
Study of the rate of passage of food with chromium-mordanted plant cells in chickens (Gallus gallus).Crossref | GoogleScholarGoogle Scholar |

Gajda AM, Storch J (2015) Enterocyte fatty acid binding proteins (FABPs): different functions of liver and intestinal FABPs in the intestine. Prostaglandins, Leukotrienes, and Essential Fatty Acids 93, 9–16.
Enterocyte fatty acid binding proteins (FABPs): different functions of liver and intestinal FABPs in the intestine.Crossref | GoogleScholarGoogle Scholar | 25458898PubMed |

Garcia J, Byrd J, Wong E (2018) Expression of nutrient transporters and host defense peptides in Campylobacter challenged broilers. Poultry Science 97, 3671–3680.
Expression of nutrient transporters and host defense peptides in Campylobacter challenged broilers.Crossref | GoogleScholarGoogle Scholar | 29931274PubMed |

Gilbert E, Li H, Emmerson D, Webb K, Wong E (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poultry Science 86, 1739–1753.
Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers.Crossref | GoogleScholarGoogle Scholar | 17626820PubMed |

Goberdhan D, Wilson C, Harris A (2016) Amino acid sensing by mTORC1: intracellular transporters mark the spot. Cell Metabolism 23, 580–589.
Amino acid sensing by mTORC1: intracellular transporters mark the spot.Crossref | GoogleScholarGoogle Scholar | 27076075PubMed |

Goodarzi M, Nanekarani S, Landy N (2014) Effect of dietary supplementation with onion (Allium cepa L.) on performance, carcass traits and intestinal microflora composition in broiler chickens. Asian Pacific Journal of Tropical Disease 4, S297–S301.
Effect of dietary supplementation with onion (Allium cepa L.) on performance, carcass traits and intestinal microflora composition in broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Gyawali R, Ibrahim SA (2012) Impact of plant derivatives on the growth of foodborne pathogens and the functionality of probiotics. Applied Microbiology and Biotechnology 95, 29–45.
Impact of plant derivatives on the growth of foodborne pathogens and the functionality of probiotics.Crossref | GoogleScholarGoogle Scholar | 22622837PubMed |

Hafeez A, Manner K, Schiederb C, Zentek J (2016) Effect of supplementation of phytogenic feed additives (powdered vs encapsulated) on performance and nutrient digestibility in broiler chickens. Poultry Science 95, 622–629.
Effect of supplementation of phytogenic feed additives (powdered vs encapsulated) on performance and nutrient digestibility in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 26706360PubMed |

Haselmeyer A, Zentek J, Chizzola R (2015) Effects of thyme as a feed additive in broiler chickens on thymol in gut contents, blood plasma, liver and muscle. Journal of the Science of Food and Agriculture 95, 504–508.
Effects of thyme as a feed additive in broiler chickens on thymol in gut contents, blood plasma, liver and muscle.Crossref | GoogleScholarGoogle Scholar | 24862829PubMed |

Hashemipour H, Kermanshahi H, Golian A, Veldkamp T (2013) Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poultry Science 92, 2059–2069.
Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 23873553PubMed |

Hellemans J, Vandesompele J (2011) ‘Quantitative PCR data analysis: unlocking the secret to successful results. The essential guide.’ (Ed. S Kennedy, N Oswald) (Caister Academic Press: Poole, UK)

Hernandez F, Madrid J, Garcia V, Orengo J, Megias MD (2004) Influence of two plant extracts on broiler performance digestibilities and digestive organ size. Poultry Science 83, 169–174.
Influence of two plant extracts on broiler performance digestibilities and digestive organ size.Crossref | GoogleScholarGoogle Scholar | 14979566PubMed |

Hippenstiel F, Abdel-Wareth AAA, Kehraus S, Südekum KH (2011) Effects of selected herbs and essential oils, and their active components on feed intake and performance of broilers: a review. Archiv für Geflügelkunde 75, 226–234.

Hong JC, Steiner T, Aufi A, Lien TF (2012) Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livestock Science 144, 253–262.
Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers.Crossref | GoogleScholarGoogle Scholar |

Hu X, Guo Y, Huang B, Bun S, Zhang L, Li J, Liu D, Long F, Yang X, Jiao P (2010) The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poultry Science 89, 1967–1794.
The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens.Crossref | GoogleScholarGoogle Scholar | 20709983PubMed |

Hughes AL, Piontkivska H (2011) Evolutionary diversification of the avian fatty acid-binding proteins. Gene 490, 1–5.
Evolutionary diversification of the avian fatty acid-binding proteins.Crossref | GoogleScholarGoogle Scholar | 21986036PubMed |

Jamroz D, Wiliczkiewicz I A, Wertelecki T, Orda J, Skorupinska J (2005) Use of active substances of plant origin in chicken diets based on maize and locally grown cereals. British Poultry Science 46, 485–493.
Use of active substances of plant origin in chicken diets based on maize and locally grown cereals.Crossref | GoogleScholarGoogle Scholar | 16268107PubMed |

Khattak F, Ronchi A, Castelli P, Sparks N (2014) Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poultry Science 93, 132–137.
Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 24570432PubMed |

Kırkpınar F, Bora Ünlü H, Özdemir G (2011) Effects of oregano and garlic essential oils on performance, carcass, organ and blood characteristics and intestinal microflora of broilers. Livestock Science 137, 219–225.
Effects of oregano and garlic essential oils on performance, carcass, organ and blood characteristics and intestinal microflora of broilers.Crossref | GoogleScholarGoogle Scholar |

Kornbrust DJ, Mavis RD (1980) Relative susceptibility of microsomes from lung, heart, liver, kidney, brain and testes to lipid peroxidation: correction with vitamin E content. Lipids 15, 315–322.
Relative susceptibility of microsomes from lung, heart, liver, kidney, brain and testes to lipid peroxidation: correction with vitamin E content.Crossref | GoogleScholarGoogle Scholar | 7392825PubMed |

Lee KW, Kappert HJ, Frehner M, Losa R, Beynen AC (2003) Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. British Poultry Science 44, 450–457.
Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens.Crossref | GoogleScholarGoogle Scholar | 12964629PubMed |

Lee KW, Everts H, Beynen AC (2004) Essential oils in broiler nutrition. International Journal of Poultry Science 3, 738–752.
Essential oils in broiler nutrition.Crossref | GoogleScholarGoogle Scholar |

Luna A, Labaque MC, Zygadlo JA, Marin RH (2010) Effects of thymol and carvacrol feed supplementation on lipid oxidation in broiler meat. Poultry Science 89, 366–370.
Effects of thymol and carvacrol feed supplementation on lipid oxidation in broiler meat.Crossref | GoogleScholarGoogle Scholar | 20075292PubMed |

Marcinčáková D, Čertík M, Marcinčák S, Popelka P, Šimková J, Klempová T, Petrovič V, Tučková M, Bača M (2011) Effect of dietary supplementation of Melissaofficinalis and combination of Achilleamillefolium and Crataegusoxyacantha on broiler growth performance, fatty acid composition and lipid oxidation of chicken meat. Italian Journal of Animal Science 10, e43
Effect of dietary supplementation of Melissaofficinalis and combination of Achilleamillefolium and Crataegusoxyacantha on broiler growth performance, fatty acid composition and lipid oxidation of chicken meat.Crossref | GoogleScholarGoogle Scholar |

Mott C, Siegel P, Webb K, Wong E (2008) Gene expression of nutrient transporters in the small intestine of chickens from lines divergently selected for high or low juvenile body weight. Poultry Science 87, 2215–2224.
Gene expression of nutrient transporters in the small intestine of chickens from lines divergently selected for high or low juvenile body weight.Crossref | GoogleScholarGoogle Scholar | 18931170PubMed |

Mountzouris KC, Paraskeuas V, Feggeros K (2009) Phytogenic compounds in broiler nutrition. In ‘Phytogenics in animal nutrition’. (Ed. T Steiner) 97–110. (Nottingham University Press: Nottingham, UK)

Mountzouris KC, Paraskeuas V, Tsirtsikos P, Palamidi I, Steiner T, Schatzmayr G, Fegeros K (2011) Assessment of a phytogenic feed additive effect on broiler growth performance, nutrient digestibility and caecal microflora composition. Animal Feed Science and Technology 168, 223–231.
Assessment of a phytogenic feed additive effect on broiler growth performance, nutrient digestibility and caecal microflora composition.Crossref | GoogleScholarGoogle Scholar |

Mountzouris KC, Paraskeuas V, Griela E, Papadomichelakis G, Fegeros K (2018) Phytogenic premix effects on gene expression of intestinal antioxidant enzymes and broiler meat antioxidant capacity. In ‘Proceedings XVth European Poultry Conference’. Abstract ID 401. p. 75. (World’s Poultry Science Association: Beekbergen, The Netherlands)

Mueller K, Blum NM, Kluge H, Mueller AS (2012) Influence of broccoli extract and various essential oils on performance and expression of xenobiotic- and antioxidant enzymes in broiler chickens British Journal of Nutrition 108, 588–602.
Influence of broccoli extract and various essential oils on performance and expression of xenobiotic- and antioxidant enzymes in broiler chickensCrossref | GoogleScholarGoogle Scholar | 22085616PubMed |

Myers WD, Ludden PA, Nayigihugu V, Hess BW (2004) Technical Note. A procedure for the preparation and quantitative analysis of samples for titanium dioxide Journal of Animal Science 82, 179–183.
Technical Note. A procedure for the preparation and quantitative analysis of samples for titanium dioxideCrossref | GoogleScholarGoogle Scholar | 14753360PubMed |

Napolitano L, Scalise M, Galluccio M, Pochini L, Albanese L, Indiveri C (2015) LAT1 is the transport competent unit of the LAT1/CD98 heterodimeric amino acid transporter. The International Journal of Biochemistry & Cell Biology 67, 25–33.
LAT1 is the transport competent unit of the LAT1/CD98 heterodimeric amino acid transporter.Crossref | GoogleScholarGoogle Scholar |

Paraskeuas V, Mountzouris KC (2019) Modulation of broiler gut microbiota and gene expression of toll-like receptors and tight junction proteins by diet type and inclusion of phytogenics. Poultry Science 98, 2220–2230.
Modulation of broiler gut microbiota and gene expression of toll-like receptors and tight junction proteins by diet type and inclusion of phytogenics.Crossref | GoogleScholarGoogle Scholar | 30597072PubMed |

Paraskeuas V, Fegeros K, Palamidi I, Theodoropoulos G, Mountzouris KC (2016a) Phytogenic administration and reduction of dietary energy and protein levels affects growth performance, nutrient digestibility and antioxidant status of broilers. Journal of Poultry Science 53, 264–273.
Phytogenic administration and reduction of dietary energy and protein levels affects growth performance, nutrient digestibility and antioxidant status of broilers.Crossref | GoogleScholarGoogle Scholar |

Paraskeuas V, Fegeros K, Hunger C, Theodorou G, Mountzouris KC (2016b) Dietary inclusion level effects of a phytogenic characterized by menthol and anethole on broiler growth performance, biochemical parameters including total antioxidant capacity and gene expression of immune-related biomarkers. Animal Production Science 57, 33–41.
Dietary inclusion level effects of a phytogenic characterized by menthol and anethole on broiler growth performance, biochemical parameters including total antioxidant capacity and gene expression of immune-related biomarkers.Crossref | GoogleScholarGoogle Scholar |

Paraskeuas V, Fegeros K, Palamidi I, Hunger C, Mountzouris KC (2017) Growth performance, nutrient digestibility, antioxidant capacity, blood biochemical biomarkers and cytokines expression in broiler chickens fed different phytogenic levels. Animal Nutrition 3, 114–120.
Growth performance, nutrient digestibility, antioxidant capacity, blood biochemical biomarkers and cytokines expression in broiler chickens fed different phytogenic levels.Crossref | GoogleScholarGoogle Scholar | 29767099PubMed |

Paris N, Wong E (2013) Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria maxima-infected chickens. Poultry Science 92, 1331–1335.
Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria maxima-infected chickens.Crossref | GoogleScholarGoogle Scholar | 23571343PubMed |

Peng QY, Li JD, Li Z, Duan ZY, Wu YP (2016) Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 214, 148–153.
Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RTPCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RTPCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |

Prior RL, Hoang H, Gu L, Wu X, Bacchiocca M, Howard L (2003) Assays for hydrophilic and lipophilic antioxidant capacity (oxygen radical absorbance capacity (ORACFL)) of plasma and other biological and food samples. Journal of Agricultural and Food Chemistry 51, 3273–3279.
Assays for hydrophilic and lipophilic antioxidant capacity (oxygen radical absorbance capacity (ORACFL)) of plasma and other biological and food samples.Crossref | GoogleScholarGoogle Scholar | 12744654PubMed |

Ri CS, Jiang XR, Kim MH, Wang J, Zhang HJ, Wu SG, Bontempo V, Qi GH (2017) Effects of dietary oregano powder supplementation on the growth performance, antioxidant status and meat quality of broiler chicks. Italian Journal of Animal Science 16, 246–252.
Effects of dietary oregano powder supplementation on the growth performance, antioxidant status and meat quality of broiler chicks.Crossref | GoogleScholarGoogle Scholar |

Richards MP, Proszkowiec-Weglarz M (2007) Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poultry Science 86, 1478–1490.
Mechanisms regulating feed intake, energy expenditure, and body weight in poultry.Crossref | GoogleScholarGoogle Scholar | 17575199PubMed |

Sadek KM, Ahmed HA, Ayoub M, Elsabagh M (2014) Evaluation of Digestarom and thyme as phytogenic feed additives for broiler chickens. European Poultry Science 78, eps.2014.55
Evaluation of Digestarom and thyme as phytogenic feed additives for broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Saxton R, Sabatini D (2017) mTOR signaling in growth, metabolism, and disease. Cell 169, 361–371.
mTOR signaling in growth, metabolism, and disease.Crossref | GoogleScholarGoogle Scholar | 28388417PubMed |

Speier J, Yadgary L, Uni Z, Wong E (2012) Gene expression of nutrient transporters and digestive enzymes in the yolk sac membrane and small intestine of the developing embryonic chick. Poultry Science 91, 1941–1949.
Gene expression of nutrient transporters and digestive enzymes in the yolk sac membrane and small intestine of the developing embryonic chick.Crossref | GoogleScholarGoogle Scholar | 22802189PubMed |

Tsinas A, Giannenas I, Voidarou C, Tzora A, Skoufos J (2011) Effects of an oregano based dietary supplement on performance of broiler chickens experimentally infected with Eimeria acervulina and Eimeria maxima. Journal of Poultry Science 48, 194–200.
Effects of an oregano based dietary supplement on performance of broiler chickens experimentally infected with Eimeria acervulina and Eimeria maxima.Crossref | GoogleScholarGoogle Scholar |

Uni Z, Tako E, Gal-Garber O, Sklan D (2003) Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo. Poultry Science 82, 1747–1754.
Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo.Crossref | GoogleScholarGoogle Scholar | 14653469PubMed |

Vila-Donat P, Marin S, Sanchis V, Ramos AJ (2018) A review on the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal fee decontamination. Food and Chemical Toxicology 114, 246–259.
A review on the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal fee decontamination.Crossref | GoogleScholarGoogle Scholar | 29476792PubMed |

Wang Q, Li H, Li N, Leng L, Wang Y (2006) Tissue expression and association with fatness traits of liver fatty acid-binding protein gene in chicken. Poultry Science 85, 1890–1895.
Tissue expression and association with fatness traits of liver fatty acid-binding protein gene in chicken.Crossref | GoogleScholarGoogle Scholar | 17032819PubMed |

Windisch WM, Schedle K, Plitzner C, Kroismayr A (2008) Use of phytogenic products as feed additives for swine and poultry. Journal of Animal Science 86, E140–E148.
Use of phytogenic products as feed additives for swine and poultry.Crossref | GoogleScholarGoogle Scholar |

Yin H, Sumners L, Dalloul R, Miska K, Fetterer R, Jenkins M, Zhu Q, Wong E (2015) Changes in expression of an antimicrobial peptide, digestive enzymes, and nutrient transporters in the intestine of E. praecox-infected chickens. Poultry Science 94, 1521–1526.
Changes in expression of an antimicrobial peptide, digestive enzymes, and nutrient transporters in the intestine of E. praecox-infected chickens.Crossref | GoogleScholarGoogle Scholar | 26015586PubMed |

Zhang GF, Yang ZB, Wang Y, Yang WR, Jiang SZ, Gai GS (2009) Effects of ginger root (Zingiber officinale) processed to different particle sizes on growth performance, antioxidant status, and serum metabolites of broiler chickens. Poultry Science 88, 2159–2166.
Effects of ginger root (Zingiber officinale) processed to different particle sizes on growth performance, antioxidant status, and serum metabolites of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 19762870PubMed |

Zidan DE, Kahilo KA, El-Far AH, Sadek KM (2016) Ginger (Zingiber officinale) and thymol dietary supplementation improve the growth performance, immunity and antioxidant status in broilers. Global Veterinaria 16, 530–538.