Abstract
In the present study, we evaluated the antihyperlipidemic and antioxidant effects of garlic and dill in comparison with atorvastatin to combat lipogenesis in broiler chickens. A total of 400 1-day-old chicks (Ross 308 strain) were randomly distributed into four experimental diets. Dietary treatments included a control diet, the control diet plus atorvastatin at 20 mg/kg, the control diet plus garlic dry powder (GDP) at 7.5 g/kg, and the control diet plus dill dry powder (DDP) at 7.5 g/kg. Chicks were maintained on experimental diets for 42 days under the recommended environmental conditions set out by the strain management manual. The results showed that weight gain, feed conversion ratio (FCR), and duodenal, jejunal, and ileal dimensions of villi (height, width, and the surface absorptive area) were improved by in-feed atorvastatin, GDP, or DDP when compared to the control (P < 0.05). The inclusion of atorvastatin or phytobiotic products increased circulatory levels of nitric oxide (NO) but decreased circulatory levels of malondialdehyde (MDA), triacylglycerol (TAG), and low-density lipoproteins cholesterol (LDL), with concomitant reductions in the T, R, and S waves amplitudes in the Lead 2 electrocardiogram (ECG) (P < 0.05). Dietary supplements caused an up-regulation of inducible nitric oxide synthase (iNOS), superoxide dismutase 1 (SOD1), and glutathione peroxidase (GPX) but reduced the expression of key hepatic lipogenic enzymes (fatty acid synthase (FAS) and hydroxy-methylglutaryl-CoA reductase (HMGCR) (P < 0.05). In conclusion, feed supplementation with atorvastatin, GDP, or DDP suppressed lipogenesis, enhanced antioxidant response, and improved gut and cardio-pulmonary function in broiler chicks subjected to hypobaric hypoxia.
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References
Adams, R.P. 2007. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry. 4th Edition Allured Publishing Corporation, Carol Stream.
Adibmoradi, M., Navidshad, B., Seifdavati, J. & Royan, M. 2006. Effect of dietary garlic meal on histological structure of small intestine in broiler chickens. Journal of Poultry Science, 43, 378-383. https://doi.org/10.2141/jpsa.43.378
Ahmadipour, B. 2018a. Securigera securidaca seed medicinal herb supplementation of diets improves pulmonary hypertensive response in broiler chickens reared at high altitude. Journal of Animal Physiology and Animal Nutrition, 102, 1601-7. https://doi.org/10.1111/jpn.12981
Ahmadipour, B., Hassanpour, H., Rafiei, F. & Khajali, F. 2015. Antioxidative, antihyperlipidemic, and growth-promoting effects. of Kelussia odoratissima in meat-type chickens. Poultry Science Journal, 3, 37–46. https://doi.org/10.22069/psj.2015.2326
Ahmadipour, B., Hassanpour, H. & Khajali, F. 2018b. Evaluation of hepatic lipogenesis and antioxidant status of broiler chickens fed mountain celery. BMC Veterinary Research, 14, 1-7. https://doi.org/10.1186/s12917-018-1561-6
Ahmadipour, B., Kalantar, M., Schreurs, N., Abbas Raza, S.H., Khan, R., Khan, S., Abd El-Aziz, A.H., Memon, S., Ullah, I. & Abaszadeh, S. 2020. Flavonoid bioactive compounds of hawthorn extract can promote growth, regulate electrocardiogram waves, and improve cardiac parameters of pulmonary hypertensive chickens. Poultry Science, 99, 974–980. https://doi.org/10.1016/j.psj.2019.10.022
Baharvand-Ahmadi, B. & Asadi-Samani, S. 2017. A mini-review on the most important effective medicinal plants to treat hypertension in ethnobotanical evidence of Iran. Journal of Nepharopharmacology, 6, 3–8. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc5295656/.
Banach, M., Aronow, W.S., Serban, C., Sahabkar, S., Rysz, J., Voroneanu, L. & Covic, A. 2015. Lipids, blood pressure and kidney update 2014. Pharmacological Research, 95–96, 111–125. https://doi.org/10.1016/j.phrs.2015.03.009
Behrooj, N., Khajali, F. & Hassanpour, H. 2012. Feeding reduced‐protein diets to broilers subjected to hypobaric hypoxia is associated with the development of pulmonary hypertension syndrome. British Poultry Science, 53, 658–664. https://doi.org/10.1080/00071668.2012.727082
Bocan, T.M.A., Mazur, M.J., Muller, S.B., Brown, E.Q., Sliskovic, D.R., O’Brien, P.M., Creswell, M.W., Lee, H., Uhlendorf, P.D., Roth, B.D. & Newton, R.S. 1994. Antiatherosclerotic activity of inhibitors of 3-hydroxy-3-methylglutaryl coenzyme A reductase in cholesterol-fed rabbits: a biochemical and morphological evaluation. Atherosclerosis, 111, 127–142. https://doi.org/10.1016/0021-9150(94)90198-8
Bok, S.H., Park, S.Y., Park, Y.B., Lee, Jeon, S.M. & Jeong, T.S. 2002. Quercetin dihydrate and gallate supplements lower plasma and hepatic lipids and change activities of hepatic antioxidant enzymes in high cholesterol-fed rats. International Journal for Vitamin and Nutrition Research, 72, 161-9. https://doi.org/10.1024/0300-9831.72.3.161
British Pharmacopoeia Commission. 1988. British Pharmacopoeia, vol. 4. H.M.S.O, London, U.K, 137–138.
Chowdhury, S.D. & Smith, T. K. 2002. Effects of dietary garlic on cholesterol metabolism in laying hens. Poultry Science, 81,1856-1862. https://doi.org/10.1093/ps/81.12.1856
Dorak, M. 2006. Real Time PCR Taylor & Francis. Oxford: UK. https://doi.org/10.4324/9780203967317
Elbaz, A.M., Ibrahim, N.S., Shehata, A.M., Mohamed, N.G. & Abdel-Moneim, A.M.E. 2021. Impact of multi-strain probiotic, citric acid, garlic powder or their combinations on performance, ileal histomorphometry, microbial enumeration and humoral immunity of broiler chickens. Tropical Animal Health and Production, 53, 1-10. https://doi.org/10.1007/s11250-021-02554-0
Elkayam, A., Mirelman, D. & Peleg, E. 2003. The effects of allicin on weight in fructose-induced hyperinsulinemic, hyperlipidemic, hypertensive rats. American Journal of Hypertension, 16, 1053–1056. https://doi.org/10.1016/j.amjhyper.2003.07.011
Fallon, M.B., Abrams, G.A., Abdel-Razek, T.T., Dai, J., Chen, S.J., Chen, Y.F., Luo, B., Oparil, S. & Ku, D.D. 1998. Garlic prevents hypoxic pulmonary hypertension in rats. American Journal of Physiology, 275, L283-L287. https://doi.org/10.1152/ajplung.1998.275.2.l283
Fouty, B.W. & Rodman, D.M. 2003. Mevastatin can cause G1 arrest and induce apoptosis in pulmonary artery smooth muscle cells through a p27Kip1- independent pathway. Circulation Research, 92, 501-509. https://doi.org/10.1161/01.res.0000061180.03813.0f
Friesen, J.A. & Rodwell, V.W. 2004. The 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductases. Genome Biology, 5, 1-7. https://doi.org/10.1186/gb-2004-5-11-248
Gao, S., Liu, Z., Li, H., Little, P.J., Liu, P. & Xu, S. 2012. Cardiovascular actions and therapeutic potential of tanshinone IIA. Atherosclerosis, 220, 3–10. https://doi.org/10.1016/j.atherosclerosis.2011.06.041
Golrokh, A.J., Bouyeh, M., Seidavi, A., van den Hoven, R., Laudadio, V. & Tufarelli, V. 2016. Effect of different dietary levels of atorvastatin and L-carnitine on performance, carcass characteristics and plasma constitutes of broiler chickens. Journal of Poultry Science, 53, 201-207. https://doi.org/10.2141/jpsa.0150184
Hassanpour, H., Bahadoran, S., Farhadfar, F., Fallahi Chamali, Z., Nazari, H. & Kaewduangta, W. 2018. Identification of reliable reference genes for quantitative real-time PCR in lung and heart of pulmonary hypertensive chickens. Poultry Science, 97, 4048-4056. https://doi.org/10.3382/ps/pey258
Hernandez-Perera, O., Perez-Sala, D., Navarro-Antolin, J., Sanchez-Pascuala, R., Hernandex, G., Diaz, C. & Lamas, S. 1998. Effects of the 3-hydroxy-3-methylglutaryl- CoA reductase inhibitors atorvastatin and simvastatin on the expression of endothelin-1 and endothelial nitric oxide synthase in vascular endothelial cells. Journal of Clinical Investigation, 101, 2711-2719. https://doi.org/10.1172/jci1500
Ibrahim, D., Ismail, T.A., Khalifa, E., Abd El-Kader, S.A., Mohamed, D.I., Mohamed, D.T., Shahin, S.E. and Abd El-Hamid, M.I. 2021. Supplementing garlic nanohydrogel optimized growth, gastrointestinal integrity and economics and ameliorated necrotic enteritis in broiler chickens using a Clostridium perfringens challenge model. Animals, 11, 2027. https://doi.org/10.3390/ani11072027
Jachimowicz, K., Winiarska-Mieczan, A. & Tomaszewska, E. 2022. The impact of herbal additives for poultry feed on the fatty acid profile of meat. Animals, 12, 1054. https://doi.org/10.3390/ani12091054
Jeong, Y.Y., Ryu, J.H., Shin, J.H., Kang, M.J., Kang, J.R., Han, J. & Kang, D. 2016. Comparison of Anti-Oxidant and Anti-Inflammatory Effects between Fresh and Aged Black Garlic Extracts. Molecules, 21, 430. https://doi.org/10.3390/molecules21040430
Jorge, P.A.R., Almeida, E.A., Ozaki, M.R., Jorge, M. & Carneiro, A. 2005. Effects of atorvastatin, fluvastatin, pravastatin, and simvastatin on endothelial function, lipid peroxidation, and aortic atherosclerosis in hypercholesterolemic rabbits. Arquivos Brasileiros de Cardiologia, 84, 314-319. https://doi.org/10.1590/s0066-782x2005000400008
Khajali, F. 2022. Managing broiler production challenges at high altitude. Veterinary Medicine Science, 8, 1519-1527. https://doi.org/10.1002/vms3.784
Khajali, F. & Wideman, R.F. 2016. Nutritional approaches to ameliorate pulmonary hypertension in broiler chickens. Journal of Animal Physiology and Animal Nutrition (Berl), 100, 3-14. https://doi.org/10.1111/jpn.12315
Khalid, R. 2001. Historical perspective on garlic and cardiovascular disease. Journal of Nutrition, 31, 977–979. https://doi.org/10.1093/jn/131.3.977s
Kim, Y.J., Jin, S.K. &Yang, H. S. 2009. Effect of dietary garlic bulb and husk on the physicochemical properties of chicken meat. Poultry Science, 88, 398-405. https://doi.org/10.3382/ps.2008-00179
Kim-Park, S. & Ku, D. 2001.Garlic Elicits A Nitric Oxide-Dependent Relaxation And Inhibits Hypoxic Pulmonary Vasoconstriction In Rats. Pharmacology and Physiology, 27, 2. https://doi.org/10.1046/j.1440-1681.2000.03333.x
Kirby, K.Y., McNew, R.W., Anthony, N.B., Kirby, J.D., Marson, N.E., Hughes, J.D. & Wideman, R.F. 1999. Electrocardiographic evaluation of broilers following unilateral occlusion of an extrapulmonary primary bronchus. Poultry Science, 78, 242–254. https://doi.org/10.1556/004.2018.011
Kojuri, J., Vosoughi, A.R. & Akrami, M. 2007. Effects of anethum graveolens and garlic on lipid profile in hyperlipidemic patients. Lipids in Health and Disease, 6, 1-5. https://doi.org/10.1186/1476-511x-6-5
Lissin, L.W. & Cooke, J.P. 2000. Phytoestrogens and cardiovascular health. Journal of American College of Cardiology, 35, 1403-1410. https://doi.org/10.1016/s0735-1097(00)00590-8
Laufs, U., Endres, M., Custodis, F., Gertz, K., Nickenig, G., Liao, J.K. & Bohm, M. 2000. Suppression of endothelial nitric oxide production after withdrawal of statin treatment is mediated by negative feedback regulation of Rho GTPase gene transcription. Circulation, 102, 3104-3110. https://doi.org/10.1161/01.cir.102.25.3104
Lorkowska, B. & Chlopicki, S. 2005. Statins as coronary vasodilators in isolated bovine coronary arteries–involvement of PGI2 and NO. Prostaglandins, Leukotrienes and Essential Fatty Acids, 72, 133–138. https://doi.org/10.1016/j.plefa.2004.10.012
Mansoori, A., Salimi, Z., Hosseini, S.A., Hormoznejad, R. & Asadi, M. 2021. The Effect of Anethum Graveolens L. (Dill) on Lipid Profile in Adults with Cardiovascular Risk Factors: A Systematic Review and Meta-Analysis of Controlled Clinical Trials. Critical Comments in Biomedicine, 2, 100–102. https://doi.org/10.18502/CCB.V2I1.5870
Meimandipour, A., Nouri Emamzadeh, A. & Soleimani, A. 2017. Effects of nanoencapsulated aloe vera, dill and nettle root extract as feed antibiotic substitutes in broiler chickens. Archives Animal Breeding, 60, 1-7. https://doi.org/10.5194/aab-60-1-2017
Minhas, R., Bansal, Y. & Bansal, G. 2020. Inducible nitric oxide synthase inhibitors: A comprehensive update. Medicinal Research Reviews, 40, 823-855. https://doi.org/10.1002/med.21636
Mitchell, J.A., Ali, F., Bailey, L., Moreno, L. & Harrington, L.S. 2008. Role of nitric oxide and prostacyclin as vasoactive hormones released by the endothelium. Experimental Physiology, 93, 141–147. https://doi.org/10.1113/expphysiol.2007.038588
Nair, V. & Turner, G. 1984. The thiobarbituric acid test for lipid peroxidation: Structure of the adduct with malondialdehyde. Lipids, 19, 804–805. https://doi.org/10.1007/BF02534475
Nuutila, A.M., Puupponen-Pimia, R., Aarni, M. & Oksman-Caldentey, K. 2003. Comparison of antioxidant activities of onion and garlic extracts by inhibition of lipid peroxidation and radical scavenging activity. Food Chemistry, 81, 485-493. https://doi.org/10.1016/S0308-8146(02)00476-4
Piechota-Polanczyk, A., Kopacz, A., Kloska, D., Zagrapan, B., Neumayer, C., Grochot-Przeczek, A., Huk, A., Brostjan, C., Dulak, J. & Jozkowicz, A. 2018. Simvastatin treatment upregulates HO-1 in patients with abdominal aortic aneurysm but independently of Nrf2. Oxidative Medicine Cellular longevity, 28, 1-16. https://doi.org/10.1155/2018/2028936
Pirany, N., Bakrani Balani, A., Hassanpour, H. & Mehraban, H. 2020. Differential expression of genes implicated in liver lipid metabolism in broiler chickens differing in weight. British Poultry Science, 61, 10-16. https://doi.org/10.1080/00071668.2019.1680802
Pourali, M., Mirghelenj, S.A. & Kermanshahi, H. 2010. Effect of garlic powder on productive performance an immune response of broiler chickens challenged with Newcastle disease virus. Global Veterinaria, 4, 616–621. http://www.idosi.org/gv/gv4(6)10/16.
Rafiei, F. & Khajali, F. 2021. Flavonoid antioxidants in chicken meat production: Potential application and future trends. World's Poultry Science Journal, 77, 347-361. https://doi.org/10.1080/00439339.2021.1891401
Rikitake, Y. & Liao, J.K. 2005. Rho GTPases, statins, and nitric oxide. Circulation Research, 97, 1232–1235. https://doi.org/10.1161/01.res.0000196564.18314.23
Rusli, R.K., Sadarman, S., Hidayat, C., Sholikin, M.M., Hilmi, M., Yuniza, A. & Irawan, A. 2022. A meta-analysis to evaluate the effects of garlic supplementation on performance and blood lipids profile of broiler chickens. Livestock Science, 263, 105022. https://doi.org/10.1016/j.livsci.2022.105022
Ruijter, J., Ramakers, C., Hoogaars, W., Karlen, Y., Bakker, O., Van den Hoff, M. & Moorman, A. 2009. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research, 37, 1–12. https://doi.org/10.1093/nar/gkp045
Sakamoto, K., Hirose, H., Onizuka, A., Hayashi, M., Futamura, N., Kawamura, Y. & Ezaki, T. 2000. Quantitative study of changes in intestinal morphology and mucus gel on total parenteral nutrition in rats. Journal of Surgical Research, 94, 99–106. https://doi.org/10.1006/jsre.2000.5937
SAS Institute. 2007. SAS User’s Guide in Statistics. 9th Edition, SAS Institute, Inc., Cary.
Song, X., Liu, H., Wang, X., Li, Z., Huang, C. 2014. Atorvastatin combined with poly-unsaturated fatty acid confers better improvement of dyslipidemia and endothelium function. Lipids Health and Diseases, 13, 1-5. https://doi.org/10.1186/1476-511X-13-186
Stevens, L. 1996. Avian Biochemistry and Molecular Biology. First Edition. Cambridge University Press, Scotland, UK, pp. 46-56.
Sun, M., Chai, L., Lu, F., Zhao, Y., Li, Q., Cui, B., Gao, R. & Liu, Y. 2018. Efficacy and Safety of Ginkgo Biloba Pills for Coronary Heart Disease with Impaired Glucose Regulation: Study Protocol for a Series of N-of-1 Randomized, Double- Blind, Placebo-Controlled Trials. Evidence-Based Complementary Alternative Medicine, 2018, 7571629. https://doi.org/10.1155/2018/7571629
Takahashi, N., Yao, L., Kim, M., Sasako, H., Aoyagi, M., Shono, J., Tsuge, N., Goto, T. & Kawada, T. 2013. Dill seed extract improves abnormalities in lipid metabolism through peroxisome proliferator-activated receptor-alpha (PPAR-alpha) activation in diabetic obese mice. Molecular Nutrition and Food Research, 57, 1295-9. https://doi.org/10.1002/mnfr.201200767
Thomson, M., Al-Qattan, K.K., Js, D. & Ali, M. 2016. Anti-diabetic and antioxidant potential of aged garlic extract (AGE) in streptozotocin-induced diabetic rats. BMC Complementary Medicine and Therapies, 16, 17. https://doi.org/10.1186/s12906-016-0992-5
Tollba, A.A.H. & Hassan, M.S.H. 2003. Using some natural additives to improve physiological and productive performance of broiler chicks under high temperature conditions. Black cumin (Niglla sativa) or garlic (Allium sativum). Poultry Science, 23, 327–340.
Varmaghany, S., Karimi Torshizi, M.A., Rahimi, S.H., Lotfollahian, H. & Hassanzadeh, M. 2015. The effects of increasing levels of dietary garlic bulb on growth performance, systolic blood pressure, hematology, and ascites syndrome in broiler chickens. Poultry Science, 94, 1812–1820. https://doi.org/10.3382/ps/pev148
Vispute, M.M., Sharma, D., Biswas, A.K., Rokade, J.J., Chaple, A.R., Biswas, A., Gopi, M. & Kapgate, M. G. 2021. Dietary Hemp (Cannabis sativa L.) and Dill Seed (Anethum graveolens) Improve Physicochemical Properties, Oxidative Stability, and Sensory Attributes of Broiler Meat. ACS Food Science and Thechnology, 3, 453-461. https://doi.org/10.1021/acsfoodscitech.0c00049
Wang, Q., Guo, Z.Y., Zhang, Y.T., Xue, J.J., Chen, Z.C., Cheng, S.Y., Ou, M.D., Cheng, K.L. & Zeng, W. J. 2016. The Effects and Mechanism of Atorvastatin on Pulmonary Hypertension Due to Left Heart Disease. PLOS ONE, 11, e0157171. https://doi.org/10.1371/journal.pone.0157171
Williams, B., Poulter, N.R., Brown, M.J., Davis, M., McInnes, G.T., Potter, J.F., Sever, P. S. & Thom, S.M. 2004. British hypertension society guidelines for hypertension management. (BHS-IV): summary. British Medicine Journal, 328, 634–640. https://doi.org/10.1136/bmj.328.7440.634
Zhou, H., Deeb, N., Evock-Clover, C.M., Ashwel, C.M. & Lamont, S.J. 2006. Genome-wide linkage analysis to identify chromosomal regions affecting phenotypic traits in the chicken. II. Body composition. Poultry Science, 85, 1712–1721. https://doi.org/10.1093/ps/85.10.1712
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Authors would like to thank the financial support from Shahrekord University.
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The data in this study was developed as a part of the first author’s PhD thesis and the study was supported by the University of Shahrekord, Iran.
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SA and BA conceived and designed research and conducted experiments. SA, BA, and NP contributed to the collection of samples and the data. BA and FK analyzed the data. BA, FK, and H.H wrote the manuscript. All the authors read and approved the final manuscript.
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Abaszadeh, S., Ahmadipour, B., Pirany, N. et al. Effect of dietary inclusion of atorvastatin, garlic, and dill on growth performance, antioxidant defense, gut, and cardio-pulmonary function, and lipogenesis in broiler chickens. Trop Anim Health Prod 55, 216 (2023). https://doi.org/10.1007/s11250-023-03639-8
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DOI: https://doi.org/10.1007/s11250-023-03639-8