Efficacy of dietary quercetin supplementation with high-energy diet model in broilers: implications on zootechnical parameters, serum biochemistry, antioxidant status, patho-morphology and gene expression studies
Abhishek B. Parmar
A E * , Vipul R. Patel A , Jignesh M. Patel B , Umed V. Ramani C and Dhruv N. Desai D
+ Author Affiliations
- Author Affiliations
A Department of Animal Nutrition, College of Veterinary Science and Animal Husbandry, Navsari Agricultural University, Navsari 396450, Gujarat, India.
B Department of Veterinary Pathology, College of Veterinary Science and Animal Husbandry, Navsari Agricultural University, Navsari 396450, Gujarat, India.
C Department of Animal Biotechnology, College of Veterinary Science and Animal Husbandry, Navsari Agricultural University, Navsari 396450, Gujarat, India.
D Department of Veterinary Microbiology, College of Veterinary Science and Animal Husbandry, Navsari Agricultural University, Navsari 396450, Gujarat, India.
E Present address: Animal Nutrition Research Station, College of Veterinary Science and Animal Husbandry, Anand Agricultural University, Anand 388001, Gujarat, India.
Animal Production Science 62(6) 554-571 https://doi.org/10.1071/AN21218
Submitted: 22 August 2020 Accepted: 6 January 2022 Published: 1 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Currently, fat supplementation is one of the commonest strategies in poultry production for early economic return. However, it might cause various unidentified metabolic alterations in chickens. Flavonoid compound quercetin has potential to modulate oxidative stress and lipid metabolism.
Aim: The study was designed to evaluate the effect of dietary quercetin supplementation in broilers challenged with high-energy diet (HED).
Methods: In total, 192 days old Vencobb-400 broiler chicks were randomly allocated to four dietary treatments with four replicates (12 birds/replicate) per treatment. Four treatments included basal diet without any supplementation (T1), basal diet + quercetin (1 g/kg; T2), HED supplemented with vegetable oil [34 g/kg (2–3 weeks), 35 g/kg (4–6 weeks); T3], HED supplemented with vegetable oil [34 g/kg (2–3 weeks), 35 g/kg (4–6 weeks)] + quercetin (1 g/kg; T4) for the age of 2–3 (starter) and 4–6 (finisher) weeks.
Key results: Improvement was observed in the growth performance and feed conversion ratio in broilers with the dietary treatments (P ≤ 0.05). HED-supplemented group showed increased levels of metabolic stress, which was explained by the elevated concentrations of cortisol and malondialdehyde, and reduced serum/liver superoxide dismutase and glutathione peroxidase activity. Moreover, lipotoxicity was found due to the accumulation of fat, and lipid peroxidation caused various injuries to the vital organs such as liver and kidney, which were manifested by histopathological findings, and also upregulated the hepatic inflammatory interleukin (IL)-1β, IL-6, and tumour necrosis factor-α mRNA expression in the HED group. HED in combination with quercetin attenuates the altered serum metabolic markers, lipid peroxidation with subsequent rising in endogenous enzyme activity. In addition, it exhibited lipolytic action by lysis of accumulated fat and ameliorated the pathomorphic alteration in vital organs and downregulation of hepatic IL-1, IL-6 and TNF-α mRNA expression.
Conclusions: High dietary energy exhibits metabolic alteration and injuries to the vital organs. It is concluded that quercetin has potential to protect against the adverse effects induced by consumption of high-energy diet in broilers.
Implications: The supplementation of quercetin as an antioxidant seems to be beneficial for poultry production as an herbal feed additive for better performance, production, and health status.
Keywords: antioxidant, broilers, gene expression, high energy diet, lipid peroxidation, metabolic, pathomorphic, quercetin.
References
Abdali D, Samson SE, Grover AK (2015) How effective are antioxidant supplements in obesity and diabetes? Medical Principles and Practice 24, 201–215.| How effective are antioxidant supplements in obesity and diabetes?Crossref | GoogleScholarGoogle Scholar | 25791371PubMed |
Abu Hafsa SH, Ibrahim SA (2018) Effect of dietary polyphenol-rich grape seed on growth performance, antioxidant capacity and ileal microflora in broiler chicks. Journal of Animal Physiology and Animal Nutrition 102, 268–275.
| Effect of dietary polyphenol-rich grape seed on growth performance, antioxidant capacity and ileal microflora in broiler chicks.Crossref | GoogleScholarGoogle Scholar | 28295656PubMed |
Aguiar VDSL, Dourado LRB, Lopes JB, Machado LP, Daphinne CNNND, Silva DRS, Santos ETD, Farias LA (2016) Cottonseed oil in diets for growing broilers. Revista Brasileira de Zootecnia 45, 208–218.
| Cottonseed oil in diets for growing broilers.Crossref | GoogleScholarGoogle Scholar |
Ahmadipour B, Khajali F (2019) Expression of antioxidant genes in broiler chickens fed nettle (Urtica dioica) and its link with pulmonary hypertension. Animal Nutrition 5, 264–269.
| Expression of antioxidant genes in broiler chickens fed nettle (Urtica dioica) and its link with pulmonary hypertension.Crossref | GoogleScholarGoogle Scholar | 31528728PubMed |
AOAC (2001) ‘Official methods of analysis.’ 16th edn. (Association of Official Analytical Communities: Washington, DC, USA)
Arslan M, Haq AU, Ashraf M, Iqbal J, Mund MD (2017) Effect of turmeric (Curcuma longa) supplementation on growth performance, immune response, carcass characteristics and cholesterol profile in broilers. Veterinaria 66, 16–20.
Ayed HB, Attia H, Ennouri M (2015) Effect of oil supplemented diet on growth performance and meat quality of broiler chickens. Advanced Techniques in Biology & Medicine 4, 1
| Effect of oil supplemented diet on growth performance and meat quality of broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Barham D, Trinder P (1972) An improved color reagent for the determination of blood glucose by the oxidase system. Analyst 97, 142–145.
| An improved color reagent for the determination of blood glucose by the oxidase system.Crossref | GoogleScholarGoogle Scholar | 5037807PubMed |
Bartels H, Böhmer M, Heierli C (1972) Serum kreatininbestimmung ohne enteiweissen. Clinica Chimica Acta 37, 193–197.
| Serum kreatininbestimmung ohne enteiweissen.Crossref | GoogleScholarGoogle Scholar |
Benzertiha A, Kierończyk B, Rawski M, Kołodziejski P, Bryszak M, Józefiak D (2019) Insect oil as an alternative to palm oil and poultry fat in broiler chicken nutrition. Animals 9, 116
| Insect oil as an alternative to palm oil and poultry fat in broiler chicken nutrition.Crossref | GoogleScholarGoogle Scholar |
Bergmeyer HU, Hørder M (1980) International federation of clinical chemistry. Scientific committee. Expert panel on enzymes. IFCC document stage 2, draft 1; 1979-11-19 with a view to an IFCC recommendation. IFCC methods for the measurement of catalytic concentration of enzymes. Part 3. IFCC method for alanine aminotransferase. Journal of Clinical Chemistry and Clinical Biochemistry 18, 521–534.
BIS (2007) ‘Indian Standard: poultry feed specifications.’ 5th revision edn. (Bureau of Indian Standards: New Delhi, India)
Bucolo G, David H (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clinical Chemistry 19, 476
| Quantitative determination of serum triglycerides by the use of enzymes.Crossref | GoogleScholarGoogle Scholar | 4703655PubMed |
Buzzetti E, Pinzani M, Tsochatzis EA (2016) The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism 65, 1038–1048.
| The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD).Crossref | GoogleScholarGoogle Scholar | 26823198PubMed |
Choi YI, Ahn HJ, Lee BK, Oh ST, An BK, Kang CW (2012) Nutritional and hormonal induction of fatty liver syndrome and effects of dietary lipotropic factors in egg-type male chicks. Asian-Australasian Journal of Animal Sciences 25, 1145–1152.
| Nutritional and hormonal induction of fatty liver syndrome and effects of dietary lipotropic factors in egg-type male chicks.Crossref | GoogleScholarGoogle Scholar | 25049674PubMed |
Davis JE, Cain J, Small C, Hales DB (2016) Therapeutic effect of flax-based diets on fatty liver in aged laying hens. Poultry Science 95, 2624–2632.
| Therapeutic effect of flax-based diets on fatty liver in aged laying hens.Crossref | GoogleScholarGoogle Scholar | 27143762PubMed |
Donaldson J, Madziva MT, Erlwanger KH (2017) Metabolic health of guinea fowl and muscovy ducks fed a high-fat diet. Asian Journal of Animal and Veterinary Advances 12, 274–283.
| Metabolic health of guinea fowl and muscovy ducks fed a high-fat diet.Crossref | GoogleScholarGoogle Scholar |
Dong J, Zhang X, Zhang L, Bian H-X, Xu N, Bao B, Liu J (2014) Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including AMPKα1/SIRT1. Journal of Lipid Research 55, 363–374.
| Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including AMPKα1/SIRT1.Crossref | GoogleScholarGoogle Scholar | 24465016PubMed |
Doumas BT, Ard Watson W, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clinica Chimica Acta 31, 87–96.
| Albumin standards and the measurement of serum albumin with bromcresol green.Crossref | GoogleScholarGoogle Scholar |
Duncan DB (1955) Multiple ranges and multiple F test. Biometrics 11, 1–42.
| Multiple ranges and multiple F test.Crossref | GoogleScholarGoogle Scholar |
Emamat H, Foroughi F, Eini-Zinab H, Taghizadeh M, Rismanchi M, Hekmatdoost A (2016) The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes & Metabolic Disorders 15, 25
| The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease.Crossref | GoogleScholarGoogle Scholar |
Emamat H, Foroughi F, Eini-Zinab H, Hekmatdoost A (2018) The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry 33, 75–80.
| The effects of onion consumption on prevention of nonalcoholic fatty liver disease.Crossref | GoogleScholarGoogle Scholar | 29371773PubMed |
Fossati P, Prencipe L, Berti G (1980) Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid/4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clinical Chemistry 26, 227–231.
| Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid/4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine.Crossref | GoogleScholarGoogle Scholar | 7353268PubMed |
Fouad AM, El-Senousey HK (2014) Nutritional factors affecting abdominal fat deposition in poultry: a review. Asian-Australasian Journal of Animal Sciences 27, 1057–1068.
| Nutritional factors affecting abdominal fat deposition in poultry: a review.Crossref | GoogleScholarGoogle Scholar | 25050050PubMed |
Fouad AM, El-Senousey HK, Yang XJ, Yao JH (2013) Dietary l-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens. Animal 7, 1239–1245.
| Dietary l-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 23472611PubMed |
Gedikli S, Ozkanlar S, Gur C, Sengul E, Gelen V (2017) Preventive effects of quercetin on liver damages in high-fat diet-induced obesity. Journal of Histology and Histopathology 4, 7
| Preventive effects of quercetin on liver damages in high-fat diet-induced obesity.Crossref | GoogleScholarGoogle Scholar |
Goliomytis M, Tsoureki D, Simitzis PE, Charismiadou MA, Hager-Theodorides AL, Deligeorgis SG (2014) The effects of quercetin dietary supplementation on broiler growth performance, meat quality, and oxidative stability. Poultry Science 93, 1957–1962.
| The effects of quercetin dietary supplementation on broiler growth performance, meat quality, and oxidative stability.Crossref | GoogleScholarGoogle Scholar | 24894531PubMed |
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 |
Hassan FAM, Roushdy EM, Kishawy ATY, Zaglool AW, Tukur HA, Saadeldin IM (2019) Growth performance, antioxidant capacity, lipid-related transcript expression and the economics of broiler chickens fed different levels of rutin. Animals 9, 7–11.
| Growth performance, antioxidant capacity, lipid-related transcript expression and the economics of broiler chickens fed different levels of rutin.Crossref | GoogleScholarGoogle Scholar |
He S, Zhao S, Dai S, Liu D, Bokhari SG (2015) Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress. Animal Science Journal 86, 897–903.
| Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress.Crossref | GoogleScholarGoogle Scholar | 25780810PubMed |
Iskender H, Yenice G, Dokumacioglu E, Kaynar O, Hayirli A, Kaya A (2016) The effects of dietary flavonoid supplementation on the antioxidant status of laying hens. Revista Brasileira de Ciência Avícola 18, 663–668.
| The effects of dietary flavonoid supplementation on the antioxidant status of laying hens.Crossref | GoogleScholarGoogle Scholar |
Jyothi Priya R, Poorani K, Anandhi M (2018) A rare occurrence of fatty liver kidney syndrome (FLKS) in an adult crossbred chicken: a case study. International Journal of Science, Environment and Technology 7, 607–612.
Kalkan Y, Kapakin KAT, Kara A, Atabay T, Karadeniz A, Simsek N, Karakus E, Can I, Yildirim S, Ozkanlar S, Sengul E (2012) Protective effect of Panax ginseng against serum biochemical changes and apoptosis in kidney of rats treated with gentamicin sulphate. Journal of Molecular Histology 43, 603–613.
| Protective effect of Panax ginseng against serum biochemical changes and apoptosis in kidney of rats treated with gentamicin sulphate.Crossref | GoogleScholarGoogle Scholar | 22487736PubMed |
Kang HK, Kim CH (2016) Effects of dietary supplementation with rice bran oil on the growth performance, blood parameters, and immune response of broiler chickens. Journal of Animal Science and Technology 58, 12
| Effects of dietary supplementation with rice bran oil on the growth performance, blood parameters, and immune response of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 26981258PubMed |
Khampeerathuch T, Mudsak A, Srikok S, Vannamahaxay S, Chotinun S, Chuammitri P (2018) Differential gene expression in heterophils isolated from commercial hybrid and Thai indigenous broiler chickens under quercetin supplementation. Journal of Applied Animal Research 46, 804–812.
| Differential gene expression in heterophils isolated from commercial hybrid and Thai indigenous broiler chickens under quercetin supplementation.Crossref | GoogleScholarGoogle Scholar |
Khatun J, Loh TC, Akit H, Foo HL, Mohamad R (2018) Influence of different sources of oil on performance, meat quality, gut morphology, ileal digestibility and serum lipid profile in broilers. Journal of Applied Animal Research 46, 479–485.
| Influence of different sources of oil on performance, meat quality, gut morphology, ileal digestibility and serum lipid profile in broilers.Crossref | GoogleScholarGoogle Scholar |
Kim DW, Mushtaq MMH, Parvin R, Kang HK, Kim JH, Na JC, Hwangbo J, Kim JD, Yang CB, Park BJ, Choi HC (2015) Various levels and forms of dietary α-lipoic acid in broiler chickens: Impact on blood biochemistry, stress response, liver enzymes, and antibody titers. Poultry Science 94, 226–231.
| Various levels and forms of dietary α-lipoic acid in broiler chickens: Impact on blood biochemistry, stress response, liver enzymes, and antibody titers.Crossref | GoogleScholarGoogle Scholar | 25630676PubMed |
Koronowicz AA, Banks P, Szymczyk B, Leszczyńska T, Master A, Piasna E, Szczepański W, Domagała D, Kopeć A, Piątkowska E (2016) Dietary conjugated linoleic acid affects blood parameters, liver morphology and expression of selected hepatic genes in laying hens. British Poultry Science 57, 663–673.
| Dietary conjugated linoleic acid affects blood parameters, liver morphology and expression of selected hepatic genes in laying hens.Crossref | GoogleScholarGoogle Scholar | 27267260PubMed | 27267260PubMed |
Lv Z, Xing K, Li G, Liu D, Guo Y (2018) Dietary genistein alleviates lipid metabolism disorder and inflammatory response in laying hens with fatty liver syndrome. Frontiers in Physiology 9, 1493
| Dietary genistein alleviates lipid metabolism disorder and inflammatory response in laying hens with fatty liver syndrome.Crossref | GoogleScholarGoogle Scholar | 30405443PubMed | 30405443PubMed |
Marcolin E, San-Miguel B, Vallejo D, Tieppo J, Marroni N, González-Gallego J, Tuñón MJ (2012) Quercetin treatment ameliorates inflammation and fibrosis in mice with nonalcoholic steatohepatitis. The Journal of Nutrition 142, 1821–1828.
| Quercetin treatment ameliorates inflammation and fibrosis in mice with nonalcoholic steatohepatitis.Crossref | GoogleScholarGoogle Scholar | 22915297PubMed | 22915297PubMed |
Marcolin É, Forgiarini LF, Rodrigues G, Tieppo J, Borghetti GS, Bassani VL, Picada JN, Marroni NP (2013) Retracted: Quercetin decreases liver damage in mice with non-alcoholic steatohepatitis. Basic & Clinical Pharmacology & Toxicology 112, 385–391.
| Retracted: Quercetin decreases liver damage in mice with non-alcoholic steatohepatitis.Crossref | GoogleScholarGoogle Scholar |
Marieb EN, Hoehn K (2010) Human anatomy and physiology.’ 8th edn. (Benjamin Cummings: San Francisco, CA, USA)
Mariee AD, Abd-Allah GM, El-Beshbishy HA (2012) Protective effect of dietary flavonoid quercetin against lipemic-oxidative hepatic injury in hypercholesterolemic rats. Pharmaceutical Biology 50, 1019–1025.
| Protective effect of dietary flavonoid quercetin against lipemic-oxidative hepatic injury in hypercholesterolemic rats.Crossref | GoogleScholarGoogle Scholar | 22775419PubMed | 22775419PubMed |
Milagro FI, Campión J, Martínez JA (2006) Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity 14, 1118–1123.
| Weight gain induced by high-fat feeding involves increased liver oxidative stress.Crossref | GoogleScholarGoogle Scholar | 16899792PubMed | 16899792PubMed |
Ologundudu A, Ologundudu AO, Ololade IA, Obi FO (2010) Effect of Hibiscus sabdariffa anthocyanins on 2,4-dinitrophenylhydrazine induced hematotoxicity in rabbits. African Journal of Biochemistry Research 3, 140–144.
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
| Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar | 11972351PubMed | 11972351PubMed |
Pisonero-Vaquero S, Martínez-Ferreras A, García-Mediavilla MV, Martínez-Florez S, Fernández A, Benet M, Olcoz JL, Jover R, González-Gallego J, Sánchez-Campos S (2015) Quercetin ameliorates dysregulation of lipid metabolism genes via the PI3K/AKT pathway in a diet-induced mouse model of nonalcoholic fatty liver disease. Molecular Nutrition & Food Research 59, 879–893.
| Quercetin ameliorates dysregulation of lipid metabolism genes via the PI3K/AKT pathway in a diet-induced mouse model of nonalcoholic fatty liver disease.Crossref | GoogleScholarGoogle Scholar |
Porras D, Nistal E, Martínez-Florez S, Pisonero-Vaquero S, Olcoz LJ, Jover R, González-Gallego J, García-Mediavilla MV, Sánchez-Campos SS (2017) Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation. Free Radical Biology and Medicine 102, 188–202.
| Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation.Crossref | GoogleScholarGoogle Scholar | 27890642PubMed | 27890642PubMed |
Prophet EB, Mills B, Arrington JB, Sobin LH (1994) ‘Laboratory methods in histotechnology.’ pp. 214–215. (Armed forces Institute of Pathology: Washington, DC, USA)
Ramamneh DA (2017) Effect of using liquid onion on broiler physiology, production and behaviour. Bulletin of Environment, Pharmacology and Life Sciences 6, 87–92.
Rozenboim I, Mahato J, Cohen NA, Tirosh O (2016) Low protein and high-energy diet: a possible natural cause of fatty liver hemorrhagic syndrome in caged White Leghorn laying hens. Poultry Science 95, 612–621.
| Low protein and high-energy diet: a possible natural cause of fatty liver hemorrhagic syndrome in caged White Leghorn laying hens.Crossref | GoogleScholarGoogle Scholar | 26755655PubMed | 26755655PubMed |
Saeed M, Naveed M, Arain MA, Arif M, Abd El-Hack ME, Alagawany M, Siyal FA, Soomro RN, Sun C (2017) Quercetin: nutritional and beneficial effects in poultry. World’s Poultry Science Journal 73, 355–364.
| Quercetin: nutritional and beneficial effects in poultry.Crossref | GoogleScholarGoogle Scholar |
Sahu BD, Kuncha M, Sindhura GJ, Sistla R (2013) Hesperidin attenuates cisplatin-induced acute renal injury by decreasing oxidative stress, inflammation and DNA damage. Phytomedicine 20, 453–460.
| Hesperidin attenuates cisplatin-induced acute renal injury by decreasing oxidative stress, inflammation and DNA damage.Crossref | GoogleScholarGoogle Scholar | 23353054PubMed | 23353054PubMed |
Selvam R, Saravanakumar M, Suresh S, Chandrasekeran CV, Prashanth D (2018) Evaluation of polyherbal formulation and synthetic choline chloride on choline deficiency model in broilers: implications on zootechnical parameters, serum biochemistry and liver histopathology. Asian-Australasian Journal of Animal Sciences 31, 1795–1806.
| Evaluation of polyherbal formulation and synthetic choline chloride on choline deficiency model in broilers: implications on zootechnical parameters, serum biochemistry and liver histopathology.Crossref | GoogleScholarGoogle Scholar | 29642669PubMed | 29642669PubMed |
Sikder K, Das N, Kesh BS, Dey S (2014) Quercetin and β-sitosterol prevent high fat diet induced dyslipidemia and hepatotoxicity in swine albino mice. Indian Journal of experimental Biology 52, 60–66.
Song Y, Ruan J, Luo J, Wang T, Yang F, Cao H, Huang J, Hu G (2017) Abnormal histopathology, fat percent and hepatic apolipoprotein A I and apolipoprotein B100 mRNA expression in fatty liver hemorrhagic syndrome and their improvement by soyabean lecithin. Poultry Science 96, 3559–3563.
| Abnormal histopathology, fat percent and hepatic apolipoprotein A I and apolipoprotein B100 mRNA expression in fatty liver hemorrhagic syndrome and their improvement by soyabean lecithin.Crossref | GoogleScholarGoogle Scholar | 28938763PubMed | 28938763PubMed |
Sonkusale P, Bhandarker AG, Kurkare NV, Ravikanth K, Maini S, Sood D (2011) Hepatoprotective activity of superliv liquid and repchol in CCL4 induced FLKS syndrome in broilers. International Journal of Poultry Science 10, 49–55.
| Hepatoprotective activity of superliv liquid and repchol in CCL4 induced FLKS syndrome in broilers.Crossref | GoogleScholarGoogle Scholar |
Ting Y, Chang W-T, Shiau D-K, Chou P-H, Wu M-F, Hsu C-L (2018) Antiobesity efficacy of quercetin-rich supplement on diet-induced obese rats: effects on body composition, serum lipid profile, and gene expression. Journal of Agricultural and Food Chemistry 66, 70–80.
| Antiobesity efficacy of quercetin-rich supplement on diet-induced obese rats: effects on body composition, serum lipid profile, and gene expression.Crossref | GoogleScholarGoogle Scholar | 29249156PubMed |
Tokuda K, Tanimoto K (1993) A new method of measuring bilirubin in serum by vanadic acid. Japanese Journal of Clinical Chemistry 22, 116–122.
| A new method of measuring bilirubin in serum by vanadic acid.Crossref | GoogleScholarGoogle Scholar |
Trinder P (1969) Enzymatic calorimetric determination of triglycerides by GOP-PAP method. Annals of Clinical Biochemistry 6, 24–27.
| Enzymatic calorimetric determination of triglycerides by GOP-PAP method.Crossref | GoogleScholarGoogle Scholar |
Trott KA, Giannitti F, Rimoldi G, Hill A, Woods L, Barr B, Anderson M, Mete A (2014) Fatty liver hemorrhagic syndrome in the backyard chicken: a retrospective histopathologic case series. Veterinary Pathology 51, 787–795.
| Fatty liver hemorrhagic syndrome in the backyard chicken: a retrospective histopathologic case series.Crossref | GoogleScholarGoogle Scholar | 24091813PubMed | 24091813PubMed |
Tufarelli V, Bozzo G, Perillob A, Laudadio V (2015) Effects of feeding different lipid sources on hepatic histopathology features and growth traits of broiler chickens. Acta Histochemica 117, 780–783.
| Effects of feeding different lipid sources on hepatic histopathology features and growth traits of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 26277050PubMed | 26277050PubMed |
Vieira dos Santos M, Espíndola G, Lobo RN, Fuentes MdF, Carvalho L, Santos AB (2009) Desempenho e qualidade dos ovos de poedeiras comerciais submetidas às dietas com diferentes óleos vegetais. Revista Brasileira de Saúde e Produção Animal 10, 1516
Wu XL, Zou XY, Zhang M, Hu HQ, Wei XL, Jin ML, Cheng HW, Jiang S (2021) Osteocalcin prevents insulin resistance, hepatic inflammation, and activates autophagy associated with high-fat diet-induced fatty liver hemorrhagic syndrome in aged laying hens. Poultry Science 100, 73–83.
| Osteocalcin prevents insulin resistance, hepatic inflammation, and activates autophagy associated with high-fat diet-induced fatty liver hemorrhagic syndrome in aged laying hens.Crossref | GoogleScholarGoogle Scholar | 33357709PubMed | 33357709PubMed |
Xiong M, Li S, Peng X, Feng Y, Yu G, Xin Q, Gong Y (2010) Adipogenesis in ducks interfered by small interfering ribonucleic acids of peroxisome proliferator-activated receptor γ gene. Poultry Science 89, 88–95.
| Adipogenesis in ducks interfered by small interfering ribonucleic acids of peroxisome proliferator-activated receptor γ gene.Crossref | GoogleScholarGoogle Scholar | 20008806PubMed | 20008806PubMed |
Yang F, Ruan J, Wang T, Luo J, Cao H, Song Y, Huang J, Hu G (2017) Improving effect of dietary soybean phospholipids supplement on hepatic and serum indexes relevant to fatty liver hemorrhagic syndrome in laying hens. Animal Science Journal 88, 1860–1869.
| Improving effect of dietary soybean phospholipids supplement on hepatic and serum indexes relevant to fatty liver hemorrhagic syndrome in laying hens.Crossref | GoogleScholarGoogle Scholar | 28677164PubMed | 28677164PubMed |
Yang Y, Du L, Hosokawa M, Miyashita K (2020) Spirulina lipids alleviate oxidative stress and inflammation in mice fed a high-fat and high-sucrose Diet. Marine Drugs 18, 148
| Spirulina lipids alleviate oxidative stress and inflammation in mice fed a high-fat and high-sucrose Diet.Crossref | GoogleScholarGoogle Scholar |
Ying H-Z, Liu Y-H, Yu B, Wang Z-Y, Zang J-N, Yu C-H (2013) Dietary quercetin ameliorates nonalcoholic steatohepatitis induced by a high-fat diet in gerbils. Food and Chemical Toxicology 52, 53–60.
| Dietary quercetin ameliorates nonalcoholic steatohepatitis induced by a high-fat diet in gerbils.Crossref | GoogleScholarGoogle Scholar | 23123425PubMed | 23123425PubMed |
Zafarnejad K, Afzali N, Rajabzadeh M (2017) Effect of bee glue on growth performance and immune response of broiler chickens. Journal of Applied Animal Research 45, 280–284.
| Effect of bee glue on growth performance and immune response of broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Zavareie HN, Toghyani M (2018) Effect of dietary phospholipids on performance, intestinal morphology and fat digestibility in broiler chicks. Journal of Livestock Science 9, 107–115.
Zhang ZF, Zhou TX, Kim IH (2013) Effects of dietary olive oil on growth performance, carcass parameters, serum characteristics, and fatty acid composition of breast and drumstick meat in broilers. Asian-Australasian Journal of Animal Sciences 26, 416–422.
| Effects of dietary olive oil on growth performance, carcass parameters, serum characteristics, and fatty acid composition of breast and drumstick meat in broilers.Crossref | GoogleScholarGoogle Scholar | 25049805PubMed | 25049805PubMed |
