The effects of adding essential oils (Thymus vulgaris L. and Mentha pulegium L.) and microbial phytase on intestinal microflora and immune level (humoral immunity (HI) and blood cells) in broilers
Subject Areas :eslam Ghalandari 1 , alireza safamehr 2 , ali nobakht 3 , Yousef Mehmannavaz 4 , saman mahdavi 5
1 - PhD student in Animal Nutrition, Islamic Azad University, Maragheh Branch, Maragheh, Iran
2 - Professor, Department of Animal Sciences, Islamic Azad University, Maragheh Branch, Maragheh, Iran
3 - Associate Professor, Department of Animal Sciences, Islamic Azad University, Maragheh Branch, Maragheh,
Iran
4 - Assistant Professor, Department of Animal Sciences, Islamic Azad University, Maragheh Branch, Maragheh,
Iran
5 - Assistant Professor, Department of Microbiology, Islamic Azad University, Maragheh Branch, Maragheh, Iran
Keywords: intestinal microflora, Broiler, immunity, microbial phytase, Essential oil,
Abstract :
Background & Aims: Although medicinal plants have been used in different ways in feeding poultry, including broiler chickens, the simultaneous use of essential oils and enzymes, especially microbial phytase enzyme, has been used less. Thyme and Mentha are plants that affect the immune system. The positive effects of phytase have been documented in poultry. The purpose of this research is to investigate the mutual effects of essential oils and phytase enzyme on intestinal microflora and immunity level of broiler chickens.Materials and Methods: This experiment examines intestinal microflora and immune level (humoral immunity (HI test) and blood cells) using three levels of thyme essential oil, Mentha essential oil and microbial phytase with 8 treatments and 4 repetitions and a total of 32 test units for 42 days. It was done on broilers. Culture methods (MRS-Agar and EMB) and ELISA method and commercial biochemistry kits were used to check intestinal microflora and immune level, respectively.Results: Examining the main effects showed that the treatments that consumed thyme essential oil had lower coliform population and total aerobic bacteria (TAB) compared to other treatments (p<0.05). The level of humoral immunity showed a significant difference among different experimental groups (p<0.05). The treatments that did not receive essential oils of thyme and Mentha had the lowest ratio of heterophils to lymphocytes (p<0.05).Conclusion: The results showed that the use of microbial phytase enzyme and thyme essential oil reduces the population of intestinal coliform bacteria and the use of thyme essential oil improves humoral immunity.
References:
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Association EP. Five years without antibiotic growth promoters (AGP) in the EU livestock production. Accessed Mar. 11, 2013. http://asso-epa.com/five years-withoutantibiotic-growth-promoters-agp-in-the-eu-livestock-production/. 2012.
Brochot, A., Guilbot, A., Haddioui, L., Roques, C. Antibacterial, antifungal, and antiviral effects of three essential oil blends. Microbiologyopen. 2017.
Adaszyńska‐Skwirzyńska, M., Szczerbińska, D. The antimicrobial activity of lavender essential oil (Lavandula angustifolia) and its influence on the production performance of broiler chickens. J Anim Physiol Anim Nut. 2018;102(4):1020–5.
Sabo, V. A., Knezevic P. Antimicrobial activity of Eucalyptus camaldulensisDehn. plant extracts and essential oils: A review. Indust. Crop Prod. 2019;132:13–429.
Sevim, B., Gümüş, E., Harman, H., Ayasan, T., Başer, E., Altay, Y. A, K. Effects of dietary rosemary essential oil on growth performance, carcass traits and some hematological values of chukar partridge. J Agric Food Sci Technol. 2020;8(2):430–5.
Chowdhury, S., Mandal, G.P., Patra, A.K., Kumar, P., Samanta, I. P, S., Samanta A. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim Feed Sci Technol. 2018;236:39–47.
Pirgozliev, V., Mansbridge, S. C., Rose, S. P., Mackenzie, A. M. B, A., Karadas, F., Bravo D. Dietary essential oils improve feed efficiency and hepatic antioxidant content of broiler chickens. Animal. 2019;13(3):502–8.
Juglal S, Govinden R, Odhav B. Spice oils for the control of co-occurring mycotoxin-producing fungi. J Food Prot. 2002;65(4):683–7.
Yang Y. F. Zhao L. L. Shao Y. X. Liao X. D. Zhang L. Y. Lin L. U. Luo X. G. Effects of dietary graded levels of cinnamon essential oil and its combination with bamboo leaf flavonoid on immune function, antioxidative ability and intestinal microbiota of broilers. J Int Agric. 2019;18(9):2123-2132.
Zhai, H., Liu, H., Wang, S., Wu, J., Kluenter AM. Potential of essential oils for poultry and pigs. Anim Nut. 2018;
Sabuna, C., Harimurti, S., Nurcahyo RW. Utilization of distillation waste of Lemon Grass (Cymbopogonnardus) as litter for reducing parasite diseases and its influence on broiler performance. In IOP Conference Series. Earth Environ Sci. 2019;381(1).
Sidiropoulou, E., Skoufos, I., Marugan-Hernandez, V., Giannenas I, Bonos, E., Aguiar-Martins, K., Tzora A. In vitro anticoccidial study of oregano and garlic essential oils and effects on growth performance, faecal oocyst output and intestinal microbiota in vivo. Front Vet Sci. 2020;
Hernández F, Madrid J, García V, Orengo J, Megías MD. Influence of two plant extracts on broilers performance, digestibility, and digestive organ size. Poult Sci. 2004;83(2):169–74.
Gülçin, İ., Gören, A.C., Taslimi, P., Alwasel, S.H., Kılıc, O., Bursal E. Anticholinergic, antidiabetic and antioxidant activities of Anatolian pennyroyal (Menthapulegium)-analysis of its polyphenol contents by LC-MS/MS. Biocat Agric Biotechnol. 2020;23:101441.
Mehdizadeh T. Hashemzadeh M Nazarizadeh A. Neyriz-Naghadehi M. Tat M. Ghalavand M. Dorostkar. R. Antimicrobial effects of Zataria multiflora essential oil and Lactobacillus acidophilus on Escherichia coli O157 stability in the Iranian probiotic white brined. J Food Saf. 2018;
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Lee KW, Everts H, Kappert HJ, Frehner M, Losa R, Beynen AC. Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. Br Poult Sci. 2003;44(3):450–7.
Mohammadi F. Choobkar N. Goudarzi M. Effects of Mentha Pulegium L and Zataria multiflora on Hematological Parameters, Oxidative Stress Biomarkers and Antibody Titter Resulted from Newcastle and Gumboro Vaccines in Broiler Chickens. Vet Res Biol Prod. 2019;128:116-129. (Persian).
Platel K, Srinivasan K. Digestive stimulant action of spices: A myth or reality? Indian J Med Res. 2004;119(5):167–79.
Najafi P, Torki M. Performance, blood metabolites and immunocoinpetaence of broiler chicks fed diets included essentioal oils of medicinal herbs. J Anim Vet Adv. 2010;9(7):1164–8.
Nobakht A, Norani J, Safamehr A. The effects of different amounts of Mentha pulegium L. (pennyroyal) on performance, carcass traits, hematological and blood biochemical parameters of broilers. J Med Plants Res. 2011;5(16):3763–8.
Ghalamkari, G., M. Toghyani, N. Landy ET. Investigation the effects using different levels of Mentha pulegium L. (pennyroyal) in comparison with an antibiotic growth promoter on performance, carcass traits and immune responses in broiler chickens. Asian Pac J Trop Biomed. 2012;
Shelton JL, Southern LL, Gaston LA, Foster A. Evaluation of the nutrient matrix values for phytase in broilers. J Appl Poult Res. 2004;13(2):213–21.
Farhadi, D., Karimi, A., Sadeghi, G., Rostamzadeh, J., Bedford M. Effects of a high dose of microbial phytase and myo-inositol supplementation on growth performance, tibia mineralization, nutrient digestibility, litter moisture content, and foot problems in broiler chickens fed phosphorus-deficient diets. Poult Sci. 2017;
Roofchaei, A., Rezaeipour, V., Vatandour, S., Zaefarian F. Influence of dietary carbohydrases, individually or in combination with phytase or an acidifier, on performance, gut morphology and microbial population in broiler chickens fed a wheat-based diet. Anim Nut. 2019;5(1):63–7.
Walk CL, Bedford MR, Santos TS, Paiva D, Bradley JR, Wladecki H, et al. Extra-phosphoric effects of superdoses of a novel microbial phytase. Poult Sci. 2013;92(3):719–25.
28. Manobhavan M, Elangovan A V, Sridhar M, Shet D, Ajith S, Pal DT, et al. Effect of super dosing of phytase on growth performance, ileal digestibility and bone characteristics in broilers fed corn-soya-based diets. J Anim Physiol Anim Nutr (Berl). 2016;100(1):93–100.
Adeola O, Sands J. Does supplemental dietary microbial phytase improve amino acid utilization? A perspective that it does not. J Anim Sci. 2003;81(14_suppl_2):E78----E85.
Steiner T. Phytogenics in animal nutrition. 2009. Nottingham University Press, Nottingham, U. K, ISB.
Mehri M, Sabaghi V, Bagherzadeh-Kasmani F. Mentha piperita (peppermint) in growing Japanese quails diet: Performance, carcass attributes, morphology and microbial populations of intestine. Anim Feed Sci Technol. 2015;207:104–11.
NRC. Nutrient Requirements of Poultry : Nutrient Requirements of chickens. Natl Acad Press. 1994;(Ninth Edition):National Academy Press, Washington, DC.
Hashemi SR, Zulkifli I, Davoodi H, Zunita Z, Ebrahimi M. Growth performance, intestinal microflora, plasma fatty acid profile in broiler chickens fed herbal plant (Euphorbia hirta) and mix of acidifiers. Anim Feed Sci Technol. 2012;178(3–4):167–74.
Allan WH and Gough REA. Standard haemagglutination inhibition test for Newcastle disease: A comparison of macro and micro methods. Vet Rec. 1973;95(6):120–3.
Sturkie PD. Avian physiologhy. (4nd ed). Phytogenics Anim Nutr. 1995;New York: Springer Verlag.
SAS. SAS Users guide: Statistics. Cary, NC. 2009;
Saki AA, Kalantar M, Khoramabadi V. Effects of Drinking Thyme Essence (Thymus vulgaris L.) on Growth, Performance, Immune Response and Intestinal Selected Bacterial Population in Broiler Chickens. Poult Sci J. 2014;2(2):113–23.
Aydin A, Pekel AY, Issa G, Demirel G, Patterson PH. Effects of dietary copper, citric acid, and microbial phytase on digesta pH and ileal and carcass microbiota of broiler chickens fed a low available phosphorus diet. J Appl Poult Res. 2010;19(4):422–31.
Rabizadeh S, Sears C. Diseases Specialist: How Gut Microflora Promote Health and Disease. Curr Infect Dis Rep. 2008;10:92–8.
EL-Sawah AA, Dahshan ALHM, El-Nahass E-S, El-Mawgoud AIA. Pathogenicity of Escherichia coli O157 in commercial broiler chickens. Beni-Suef Univ J Basic Appl Sci. 2018;7(4):620–5.
Li Z, Wang W, Liu D, Guo Y. Effects of Lactobacillus acidophilus on the growth performance and intestinal health of broilers challenged with Clostridium perfringens. J Anim Sci Biotechnol. 2018;9(1):25.
Hoffman-Pennesi D, Wu C. The effect of thymol and thyme oil feed supplementation on growth performance, serum antioxidant levels, and cecal Salmonella population in broilers. J Appl Poult Res. 2010;19(4):432–43.
Ghazanfari, Sh. Adib Moradi, M. Rahimi Niat F. Effects of different levels of Artemisia sieberi essential oil on intestinal morphology characteristics, microflora population and immune system in broiler chickens. J Vet Res. 2015;70(2):195–202.
Tiihonen K, Kettunen H, Bento MHL, Saarinen M, Lahtinen S, Ouwehand AC, et al. The effect of feeding essential oils on broiler performance and gut microbiota. Br Poult Sci. 2010;51(3):381–92.
Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol. 1993;75(4):373–80.
Oskoueian E. Dalir M. A review of the most widely used medicinal plant active compounds and their effects on growth, health and production parameters in the poultry industry. Vet Res Biol Prod. 2019;125:: 2-12. (Persian).
Razieh Valipourian. Farid Shariatmadari. Mohammad Amir Karimi Torshizi. Effect of Garlic and Thyme’s essential oils blend after feed restriction period on the performance, growth rate and microbial population of broiler chickens. Anim Prod. 2018;20(4):565-576 persian.
Kyaw PHH, San Win K, Lay KK MK, KH MA and S. Effect of dietary garlic and thyme seed supplementation on the production performance,
Bento MHL AT and MH. The influence of tannin, pectin and polyethylene glycol on attachment of 15N-labelled rumen microorganisms to cellulose. Anim Feed Sci Technol. 2005;122:41–57.
Salimian, A. M., Tabeidian, S. A. and Irandoust H 2016. Dietary effects of cinnamon, turmeric and carnation powders on performance, morphological changes of intestine and blood serum oxidation status of broilers. J Anim Prod. 2016;18:141--150 (In Persian).
Bölükbaşi ŞC, Erhan MK, Kaynar Ö. The effect of feeding thyme, sage and rosemary oil on laying hen performance, cholesterol and some proteins ratio of egg yolk and Escherichia coli count in feces. Arch fur Geflugelkd. 2008;72(5):231–7.
Hashemipour, H., H. Kermanshahi, A. Golian, T. Veldkam P. Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poult Sci. 2013;92:2059–69.
Voljč M, Frankič T, Levart A, Nemec M, Salobir J. Evaluation of different vitamin e recommendations and bioactivity of α-tocopherol isomers in broiler nutrition by measuring oxidative stress in vivo and the oxidative stability of meat. Poult Sci. 2011;90(7):1478–88.
Al-Beitawi NA, El-Ghousein SS, Athamneh MZ. Effect of Adding Crushed Pimpinella Anisum, Nigella Sativa Seeds and Thymus Vulgaris Mixture to Antibiotics-Free Rations of Vaccinated and Non-Vaccinated Male Broilers on Growth Performance, Antibody Titer and Haematological Profile. Ital J Anim Sci. 2010;9(2):e43.
Safamehr A, Mirahmadi M, Nobakht A. Effect of nettle (Urtica dioica) medicinal plant on growth performance, immune responses, and serum biochemical parameters of broiler chickens. Int Res J Appl Basic Sci(Internet). 2012;3(4):721–8. Available from: http://www.irjabs.com
Eid YZ, Ohtsuka A, Hayashi K. Tea polyphenols reduce glucocorticoid-induced growth inhibition and oxidative stress in broiler chickens. Br Poult Sci. 2003;44(1):127–32.
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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(4):527–39.
Association EP. Five years without antibiotic growth promoters (AGP) in the EU livestock production. Accessed Mar. 11, 2013. http://asso-epa.com/five years-withoutantibiotic-growth-promoters-agp-in-the-eu-livestock-production/. 2012.
Brochot, A., Guilbot, A., Haddioui, L., Roques, C. Antibacterial, antifungal, and antiviral effects of three essential oil blends. Microbiologyopen. 2017.
Adaszyńska‐Skwirzyńska, M., Szczerbińska, D. The antimicrobial activity of lavender essential oil (Lavandula angustifolia) and its influence on the production performance of broiler chickens. J Anim Physiol Anim Nut. 2018;102(4):1020–5.
Sabo, V. A., Knezevic P. Antimicrobial activity of Eucalyptus camaldulensisDehn. plant extracts and essential oils: A review. Indust. Crop Prod. 2019;132:13–429.
Sevim, B., Gümüş, E., Harman, H., Ayasan, T., Başer, E., Altay, Y. A, K. Effects of dietary rosemary essential oil on growth performance, carcass traits and some hematological values of chukar partridge. J Agric Food Sci Technol. 2020;8(2):430–5.
Chowdhury, S., Mandal, G.P., Patra, A.K., Kumar, P., Samanta, I. P, S., Samanta A. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim Feed Sci Technol. 2018;236:39–47.
Pirgozliev, V., Mansbridge, S. C., Rose, S. P., Mackenzie, A. M. B, A., Karadas, F., Bravo D. Dietary essential oils improve feed efficiency and hepatic antioxidant content of broiler chickens. Animal. 2019;13(3):502–8.
Juglal S, Govinden R, Odhav B. Spice oils for the control of co-occurring mycotoxin-producing fungi. J Food Prot. 2002;65(4):683–7.
Yang Y. F. Zhao L. L. Shao Y. X. Liao X. D. Zhang L. Y. Lin L. U. Luo X. G. Effects of dietary graded levels of cinnamon essential oil and its combination with bamboo leaf flavonoid on immune function, antioxidative ability and intestinal microbiota of broilers. J Int Agric. 2019;18(9):2123-2132.
Zhai, H., Liu, H., Wang, S., Wu, J., Kluenter AM. Potential of essential oils for poultry and pigs. Anim Nut. 2018;
Sabuna, C., Harimurti, S., Nurcahyo RW. Utilization of distillation waste of Lemon Grass (Cymbopogonnardus) as litter for reducing parasite diseases and its influence on broiler performance. In IOP Conference Series. Earth Environ Sci. 2019;381(1).
Sidiropoulou, E., Skoufos, I., Marugan-Hernandez, V., Giannenas I, Bonos, E., Aguiar-Martins, K., Tzora A. In vitro anticoccidial study of oregano and garlic essential oils and effects on growth performance, faecal oocyst output and intestinal microbiota in vivo. Front Vet Sci. 2020;
Hernández F, Madrid J, García V, Orengo J, Megías MD. Influence of two plant extracts on broilers performance, digestibility, and digestive organ size. Poult Sci. 2004;83(2):169–74.
Gülçin, İ., Gören, A.C., Taslimi, P., Alwasel, S.H., Kılıc, O., Bursal E. Anticholinergic, antidiabetic and antioxidant activities of Anatolian pennyroyal (Menthapulegium)-analysis of its polyphenol contents by LC-MS/MS. Biocat Agric Biotechnol. 2020;23:101441.
Mehdizadeh T. Hashemzadeh M Nazarizadeh A. Neyriz-Naghadehi M. Tat M. Ghalavand M. Dorostkar. R. Antimicrobial effects of Zataria multiflora essential oil and Lactobacillus acidophilus on Escherichia coli O157 stability in the Iranian probiotic white brined. J Food Saf. 2018;
Bouhtit, F., Najar, M., Agha, D.M., Melki, R., Najimi, M., Sadki, K. L, P., Hamal, A., Lagneaux, L., Merimi M. The biological response of mesenchymal stromal cells to thymol and carvacrol in comparison to their essential oil: An innovative new study. Food Chem Toxic. 2019;
Lee KW, Everts H, Kappert HJ, Frehner M, Losa R, Beynen AC. Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. Br Poult Sci. 2003;44(3):450–7.
Mohammadi F. Choobkar N. Goudarzi M. Effects of Mentha Pulegium L and Zataria multiflora on Hematological Parameters, Oxidative Stress Biomarkers and Antibody Titter Resulted from Newcastle and Gumboro Vaccines in Broiler Chickens. Vet Res Biol Prod. 2019;128:116-129. (Persian).
Platel K, Srinivasan K. Digestive stimulant action of spices: A myth or reality? Indian J Med Res. 2004;119(5):167–79.
Najafi P, Torki M. Performance, blood metabolites and immunocoinpetaence of broiler chicks fed diets included essentioal oils of medicinal herbs. J Anim Vet Adv. 2010;9(7):1164–8.
Nobakht A, Norani J, Safamehr A. The effects of different amounts of Mentha pulegium L. (pennyroyal) on performance, carcass traits, hematological and blood biochemical parameters of broilers. J Med Plants Res. 2011;5(16):3763–8.
Ghalamkari, G., M. Toghyani, N. Landy ET. Investigation the effects using different levels of Mentha pulegium L. (pennyroyal) in comparison with an antibiotic growth promoter on performance, carcass traits and immune responses in broiler chickens. Asian Pac J Trop Biomed. 2012;
Shelton JL, Southern LL, Gaston LA, Foster A. Evaluation of the nutrient matrix values for phytase in broilers. J Appl Poult Res. 2004;13(2):213–21.
Farhadi, D., Karimi, A., Sadeghi, G., Rostamzadeh, J., Bedford M. Effects of a high dose of microbial phytase and myo-inositol supplementation on growth performance, tibia mineralization, nutrient digestibility, litter moisture content, and foot problems in broiler chickens fed phosphorus-deficient diets. Poult Sci. 2017;
Roofchaei, A., Rezaeipour, V., Vatandour, S., Zaefarian F. Influence of dietary carbohydrases, individually or in combination with phytase or an acidifier, on performance, gut morphology and microbial population in broiler chickens fed a wheat-based diet. Anim Nut. 2019;5(1):63–7.
Walk CL, Bedford MR, Santos TS, Paiva D, Bradley JR, Wladecki H, et al. Extra-phosphoric effects of superdoses of a novel microbial phytase. Poult Sci. 2013;92(3):719–25.
28. Manobhavan M, Elangovan A V, Sridhar M, Shet D, Ajith S, Pal DT, et al. Effect of super dosing of phytase on growth performance, ileal digestibility and bone characteristics in broilers fed corn-soya-based diets. J Anim Physiol Anim Nutr (Berl). 2016;100(1):93–100.
Adeola O, Sands J. Does supplemental dietary microbial phytase improve amino acid utilization? A perspective that it does not. J Anim Sci. 2003;81(14_suppl_2):E78----E85.
Steiner T. Phytogenics in animal nutrition. 2009. Nottingham University Press, Nottingham, U. K, ISB.
Mehri M, Sabaghi V, Bagherzadeh-Kasmani F. Mentha piperita (peppermint) in growing Japanese quails diet: Performance, carcass attributes, morphology and microbial populations of intestine. Anim Feed Sci Technol. 2015;207:104–11.
NRC. Nutrient Requirements of Poultry : Nutrient Requirements of chickens. Natl Acad Press. 1994;(Ninth Edition):National Academy Press, Washington, DC.
Hashemi SR, Zulkifli I, Davoodi H, Zunita Z, Ebrahimi M. Growth performance, intestinal microflora, plasma fatty acid profile in broiler chickens fed herbal plant (Euphorbia hirta) and mix of acidifiers. Anim Feed Sci Technol. 2012;178(3–4):167–74.
Allan WH and Gough REA. Standard haemagglutination inhibition test for Newcastle disease: A comparison of macro and micro methods. Vet Rec. 1973;95(6):120–3.
Sturkie PD. Avian physiologhy. (4nd ed). Phytogenics Anim Nutr. 1995;New York: Springer Verlag.
SAS. SAS Users guide: Statistics. Cary, NC. 2009;
Saki AA, Kalantar M, Khoramabadi V. Effects of Drinking Thyme Essence (Thymus vulgaris L.) on Growth, Performance, Immune Response and Intestinal Selected Bacterial Population in Broiler Chickens. Poult Sci J. 2014;2(2):113–23.
Aydin A, Pekel AY, Issa G, Demirel G, Patterson PH. Effects of dietary copper, citric acid, and microbial phytase on digesta pH and ileal and carcass microbiota of broiler chickens fed a low available phosphorus diet. J Appl Poult Res. 2010;19(4):422–31.
Rabizadeh S, Sears C. Diseases Specialist: How Gut Microflora Promote Health and Disease. Curr Infect Dis Rep. 2008;10:92–8.
EL-Sawah AA, Dahshan ALHM, El-Nahass E-S, El-Mawgoud AIA. Pathogenicity of Escherichia coli O157 in commercial broiler chickens. Beni-Suef Univ J Basic Appl Sci. 2018;7(4):620–5.
Li Z, Wang W, Liu D, Guo Y. Effects of Lactobacillus acidophilus on the growth performance and intestinal health of broilers challenged with Clostridium perfringens. J Anim Sci Biotechnol. 2018;9(1):25.
Hoffman-Pennesi D, Wu C. The effect of thymol and thyme oil feed supplementation on growth performance, serum antioxidant levels, and cecal Salmonella population in broilers. J Appl Poult Res. 2010;19(4):432–43.
Ghazanfari, Sh. Adib Moradi, M. Rahimi Niat F. Effects of different levels of Artemisia sieberi essential oil on intestinal morphology characteristics, microflora population and immune system in broiler chickens. J Vet Res. 2015;70(2):195–202.
Tiihonen K, Kettunen H, Bento MHL, Saarinen M, Lahtinen S, Ouwehand AC, et al. The effect of feeding essential oils on broiler performance and gut microbiota. Br Poult Sci. 2010;51(3):381–92.
Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol. 1993;75(4):373–80.
Oskoueian E. Dalir M. A review of the most widely used medicinal plant active compounds and their effects on growth, health and production parameters in the poultry industry. Vet Res Biol Prod. 2019;125:: 2-12. (Persian).
Razieh Valipourian. Farid Shariatmadari. Mohammad Amir Karimi Torshizi. Effect of Garlic and Thyme’s essential oils blend after feed restriction period on the performance, growth rate and microbial population of broiler chickens. Anim Prod. 2018;20(4):565-576 persian.
Kyaw PHH, San Win K, Lay KK MK, KH MA and S. Effect of dietary garlic and thyme seed supplementation on the production performance,
Bento MHL AT and MH. The influence of tannin, pectin and polyethylene glycol on attachment of 15N-labelled rumen microorganisms to cellulose. Anim Feed Sci Technol. 2005;122:41–57.
Salimian, A. M., Tabeidian, S. A. and Irandoust H 2016. Dietary effects of cinnamon, turmeric and carnation powders on performance, morphological changes of intestine and blood serum oxidation status of broilers. J Anim Prod. 2016;18:141--150 (In Persian).
Bölükbaşi ŞC, Erhan MK, Kaynar Ö. The effect of feeding thyme, sage and rosemary oil on laying hen performance, cholesterol and some proteins ratio of egg yolk and Escherichia coli count in feces. Arch fur Geflugelkd. 2008;72(5):231–7.
Hashemipour, H., H. Kermanshahi, A. Golian, T. Veldkam P. Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poult Sci. 2013;92:2059–69.
Voljč M, Frankič T, Levart A, Nemec M, Salobir J. Evaluation of different vitamin e recommendations and bioactivity of α-tocopherol isomers in broiler nutrition by measuring oxidative stress in vivo and the oxidative stability of meat. Poult Sci. 2011;90(7):1478–88.
Al-Beitawi NA, El-Ghousein SS, Athamneh MZ. Effect of Adding Crushed Pimpinella Anisum, Nigella Sativa Seeds and Thymus Vulgaris Mixture to Antibiotics-Free Rations of Vaccinated and Non-Vaccinated Male Broilers on Growth Performance, Antibody Titer and Haematological Profile. Ital J Anim Sci. 2010;9(2):e43.
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