Effect of Black Seed (Nigella sativa) on Antioxidant Status, Inflammatory Response, Biochemical Indices and Growth Performance in Broilers Subjected to Heat Stress

Document Type : Original Paper

Authors

1 Department of Animal Science, Payame Noor University, Tehran, Iran

2 Department of Animal Science, Faculty of Agriculture, Ilam University, Ilam, Iran

3 Department of Animal Breeding and Genetics, Guilan University, Rasht, Iran

Abstract

Heat stress has adverse effects on the health and performance of broilers. This study was conducted to investigate the protective effects of black seed (BS) supplementation on broilers subjected to heat stress (HS). A total of 500 (day-old) Ross-308 male broiler chicks were randomly assigned into five groups with five replicated pens (20 broilers per pen): thermoneutral (TN), heat stress (HS), and HS with a diet supplemented with three different levels of black seed (Nigella sativa) powder (BSP (at rates of 5g/kg (BSP-5), 10 g/kg (BSP-10), and 15 g/kg (BSP-15. Exposure to HS reduced feed intake, and weight gain and elevated feed conversion ratio (FCR), mortality (P < 0.05). Also, low antioxidant enzyme activity (such as glutathione peroxidase, superoxide dismutase, and catalase) and high malondialdehyde levels in serum, liver, and spleen were observed in the birds of the heat stress group compared to the TN treatment (P < 0.05). Moreover, HS elevated interleukin-6 and tumor necrosis factor-α and lowered interleukin-10 levels in serum, liver, and spleen (P < 0.05). In addition, heat stress causes an increase in ALT, AST, ALP, triglycerides, and cholesterol levels compared to the TV group (P < 0.05). Compared with the HS group, broilers in the BSP-10 group had a higher body weight gain, a lower feed conversion ratio, and mortality (P < 0.05). Broilers in the BSP-10 and BSP-10 groups showed higher levels of antioxidant enzyme activities and lower malondialdehyde in serum, liver, and spleen compared to the HS group. BSP supplementation at 10 and 15 mg/kg reduced TNF-α and interleukin-6 levels and enhanced interleukin-10 in serum, liver, and spleen compared to the HS group. Additionally, BSP supplementation at 15 mg/kg reduced the effect of the heat stress on ALT, AST, ALP, triglycerides, and cholesterol compared to the HS group. Obtained results showed that BSP in diet during heat stress may have a role in the reduction of the changes exerted by heat stress in broiler chickens.

Keywords


Ahmadipour B, Hassanpour H, Asadi E, Khajali F, Rafiei F & Khajali F. 2015. Kelussia odoratissima Mozzaf-A promising medicinal herb to prevent pulmonary hypertension in broiler chickens reared at high altitude. Journal of Ethnopharmacology, 159: 49-54. DOI: 10.1016/j.jep.2014.10.043
Attia Y & Hassan SS. 2017. Broiler tolerance to heat stress at various dietary protein/ energy levels. European Poultry Science, 81.  DOI: 10.1399/eps.2017.171
Al-Beitawi NA, El-Ghousein SS & Nofal AH. 2009. Replacing bacitracin methylene disalicylate by crushed Nigella sativa seeds in broiler rations and its effects on growth, blood constituents and immunity. Livestock Science, 125(2-3): 304–307. DOI: 10.1016/j.livsci.2009.03.012
Azeem T, Ur-Rehman Z, Umar Z, Asif S, Arif MM, Rahman A. 2014. Effect of Nigella sativa on poultry health and production: a review. Science Letters, 2(2): 76–82. DOI: 10.1155/2021/2070375
AOAC. 2000. Official methods of analysis of the association of official analytical chemists. 17th ed. Washington (DC): Association of Official Analytical Chemists.
Alishah AS, Daneshyar M, Aghazadeh A. 2013. The effect of dietary sumac fruit powder (Rhus coriaria L.) on performance and blood antioxidant status of broiler chickens under continuous heat stress condition. Italian Journal of Animal Science, 12: 39-43. DOI: 10.4081/ijas.2013.e6
Asghar MU, Dogan SC, Wilk M & Korczynski M. 2022. Effect of dietary supplementation of black seed seeds (nigella sativa) on performance, carcass traits, and meat quality of Japanese quails (Coturnix coturnix japonica). Animals, 12: 1298. DOI: 10.3390/ani12101298
Abdou A & Rashed GG. 2015. Effect of black seed (Nigella sativa) and garlic (Allium sativum) feed supplements on productive performance and some physiological and immunological responses of Japanese quail. Egyptian Journal of Nutrition and Feeds, 18: 129–141.
Abu-Dieyeh ZHM & Abu-Darwish MS. 2008. Effect of feeding powdered black seed seeds (Nigella sativa L.) on growth performance of 4-8 week-old broilers. Journal of Animal Veterinary advances, 7:286-290.
Amin B & Hosseinzadeh H. 2016. Black seed (nigella sativa) and its active constituent, thymoquinone: an overview on the analgesic and anti-inflammatory effects. Planta Medica, 82: 8–16. DOI: 10.1055/s-0035-1557838
AL-Sagan AA, Khalil S, Hussein EOS & Attia YA. 2020. Effects of fennel seed powder supplementation on growth performance, carcass characteristics, meat quality, and economic efficiency of broilers under thermoneutral and chronic heat stress conditions. Animals, 10: 206. DOI:10.3390/ani10020206
Adam GO, Rahman MM, Kim GB, Kang HS, Kim JS & Kim SJ. 2016. Hepatoprotective effects of Nigella sativa seed extract against acetaminophen-induced oxidative stress. Asian Pacific Journal of Tropical Medicine, 9 (3): 221-227. DOI: 10.1016/ j.apjtm. 2016.01.039
Abdel-Wareth AA, Hammad S, Khalaphallah R, Salem WM & Lohakare J. 2019. Synbiotic as eco-friendly feed additive in diets of chickens under hot climatic conditions. Poultry Science, 98(10): 4575–4583. DOI: 10.3382/ps/pez115
Babaahmadi Milani M, Zamani Moghaddam AK, Khosravi Z & Mohebi A. 2020. Use of broccoli (Brassica oleracea L. var. Italica) in comparison to ascorbic acid to decrease pulmonary hypertension syndrome in broiler chickens. Iranian Journal Veterinary Medicine, 14 (4): 372-384. DOI: 10.22059/IJVM.2020.293989.1005046
Badary OA, Tah RA, Gamal-el-Di AM & Abdel-Wahab MH. 2003. Thymoquinone is a potent superoxide anion scavenger. Drug Chemistry and Toxicology, 26 (2):87-98. DOI: 10.1081/dct-120020404
Bahrampour K, Ziaei N & OA Esmaeilipou. 2021. Feeding nano particles of vitamin C and zinc oxide: Effect on growth performance, immune response, intestinal morphology and blood
constituents in heat stressed broiler chickens. Livestock Science, 253: 104719. DOI: 10.1016/j.livsci.2021.104719
Burits M & Bucar F. 2000. Antioxidant activity of Nigella sativa essential oil. Phytotherapy Research, 14 (5): 323-328. DOI: 10.1002/1099-1573(200008)14:5<323::aid-ptr621>3.0.co;2-q
Babinszky L, Halas V & Verstegen MWA. 2011. Impacts of climate change on animal production and quality of animal food products. In: Kheradmand, H. (Ed.), Climate Change - Socioeconomic Effects, 1–29. IntechOpen.
Bharati J, Dangi SS, Mishra SR, Chouhan VS, Verma V, Shankar O, Bharti MK, Paul A, Mahato DK, Rajesh G, Singh G, Maurya VP, Bag S, Kumar P & Sarkar M. 2017. Expression analysis of Toll like receptors and interleukins in Tharparkar cattle during acclimation to heat stress exposure. Journal of Thermal Biology, 65: 48–56. DOI: 10.1016/j.jtherbio.2017.02.002
Chand N, Naz S, Rehman Zia ur, & Khan, RU. 2018. Blood biochemical profile of four fast-growing broiler strains under high ambient temperature. Applied Biological Chemistry, 61 (3): 273–279. DOI: 10.1007/s13765-018-0358-4
Chand N, Ali P, Alhidar IA, Abelrahman MM, Albadani H, Khan MA, Seidavi A, Laudadio V, Tufarelli V & Khan RU. 2021. Protective Effect of grape (Vitis vinifera) seed powder and zinc-glycine complex on growth traits and gut health of broilers following Eimeria tenella challenge. Antibiotics, 10: 186. DOI: 10.3390/antibiotics10020186
Cheikh-Rouhou S, Besbes S, Hentati B, Blecker C, Deroanne C & Attia H. 2007. Nigella sativa L.: chemical composition and physicochemical characteristics of lipid fraction. Food Chemistry, 101: 673–68. DOI: 10.1016/j.foodchem.2006.02.022
Cheng K, Yan E, Song Z, Li S, Zhang H, Zhang L, Wang C & Wang T. 2019a. Protective effect of resveratrol against hepatic damage induced by heat stress in a rat model is associated with the regulation of oxidative stress and inflammation. Journal of Thermal Biology, 82: 70–75. DOI: 10.1016/j.jtherbio.2019.03.012
Cheng Y, Chen Y, Chen R, Su Y, Zhang R, He Q, Wang K, Wen C & Zhou Y. 2019b. Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers. Poultry Science. 98(10): 4767–4776. DOI: 10.3382/ps/pez192
Bouchama A & Knochel JP. 2002. Heat stroke. New England Journal of Medicine, 346: 1978–1988.
El-Hack A, Mohamed E, Mahgoub SA, Hussein M & Saadeldin IM. 2018.  Improving growth performance and health status of meat-type quail by supplementing the diet with black seed cold-pressed oil as a natural alternative for antibiotics. Environmental Science and Pollution Research, 25: 1157–1167. DOI: 10.1007/s11356-017-0514-0 
Farah N, Benghuzzi H, Tucci M & Cason Z. 2005. The effects of isolated antioxidants from black seed on the cellular metabolism of A549 cells. Biomedical Sciences Instrumentation, 41: 211-216.
Fatima A, Naila C, Shabana N, Muhammad S, Najeeb Ullah Kh & Rifat UK. 2022. Coping heat stress by crushed fennel (Foeniculum vulgare) seeds in broilers: Growth, redox balance and humoral immune response. Livestock Science, 265: 105082. DOI:/10.1016/j.livsci.2022.105082
Fathi M, Tanha T & Saeedyan S. 2022. Influence of dietary lycopene on growth performance, antioxidant status, blood parameters and mortality in broiler chicken with cold-induced ascites. Archive of Animal Nutrition, 8: 1-11. DOI: 10.1080/1745039X.2022.2046451
Habeeb AA M & AA El-Tarabany. 2012. Effect of nigella sativa or curcumin on daily body weight gain, feed intake and some physiological functions in growing zaraibi goats during hot summer season. Third International Conference on Radiation Sciences and Applications, 12 – 16 November 2012/ Hurghada, Egypt.
Haq I, Hafeez A & Khan RU. 2020. Protective effect of Nigella sativa and Saccharomyces
cerevisiae
on zootechnical characteristics, fecal Escherichia coli and hematopoietic
potential in broiler infected with experimental Colibacillosis. Livestock Science, 239: 104119. DOI: 10.1016/j.livsci.2020.104119
Ilhan A, Gurel A, Armutcu F, kamisli S & Iraz M. 2005. Antiepileptogenic and antioxidant effects of Nigella sativa oil against pentylenetetrazol-induced killing in mice, Neuropharmacol, 49: 456-464.
Israr M, Chand N, Khan RU, Alhidary IA, Abdelrhman MM, Al-Baddani HH,
Laudadio V & Tufarelli V. 2021. Dietary grape (Vitis vinifera) seeds powder and
organic zn-gly chelate complex for mitigating heat stress in broiler chickens: growth
parameters, malanodialdehyde, paraoxonase-1 and antibody titer. Agriculture, 11:
1087. DOI: 10.3390/agriculture11111087
Jang SI, Young-Hyun Ko, Yang-Soo Moon & Sea-Hwan Sohn. 2014. Effects of vitamin C or E on the Pro-inflammatory cytokines, heat shock protein 70 and antioxidant status in broiler chicks under summer conditions. Asian-Australasian Journal of Animal Sciences, 27(5): 749-56. DOI: 10.5713/ajas.2013.13852
Jiang F, Gao Y, Dong C & Xiong S. 2018. ODC1 inhibits the inflammatory response and ROS-induced apoptosis in macrophages. Biochemical and Biophysical Research Communications, 504(4): 734–741. DOI: 10.1016/j.bbrc.2018.09.023
Kutlu HR &Forbes JM. 1993. Changes in growth and blood parameters in heat-stressed broiler chicks in response to dietary ascorbic acid. Livestock Production Science, 36: 335-350. DOI: 10.1016/0301-6226(93)90050-R
Khan SH, Ansari J, Haq AU & Abbas G. 2012. Black seed seeds as phytogenic product in broiler diets and its effects on performance, blood constituents, immunity and caecal microbial population. Italian Journal of Animal Science, 11: e77. 438-444. DOI: 10.4081/ijas. 2012.e77
Khan RU, Fatima A, Naz S, Ragni M, Tarricone S & Tufarelli V. 2022. Perspective, opportunities and challenges in using fennel (Foeniculum vulgare) in poultry health and production as alternative to antibiotics: a review. Antibiotics 11 (2): 278. DOI: 10.3390/antibiotics11020278
Kawai T & Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nature Immunology, 11: 373–384. DOI: 10.1038/ni.1863
Lara LJ & Rostagno MH. 2013. Impact of heat stress on poultry production. Animals (Basel)), 3(2): 356–369. DOI: 10.3390/ani3020356
Liu L, He J, Xie H, Yang Y, Li J & Zou Y. 2014. Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poultry Science, 93(1): 54–62. DOI: 10.3382/ps.2013-03423
Lan R, Linlin W, Qingqing C, Shengnan W & Zhao Z. 2020. Effects of dietary chitosan oligosaccharides on oxidative stress and inflammation response in liver and spleen of yellow-feather broilers exposed to high ambient temperature. Italian Journal of Animal Science. 19 (1): 1508–1517. DOI: 10.1080/1828051X.2020.1850215
Mansour MA, Ginawi OT, El-Hadiyah T, El-Khatib AS, Al-Shabanah OA & Al-Sawaf HA. 2001. Effects of volatile oil constituents of Nigella sativa on carbon tetrachloride-induced hepatotoxicity in mice: evidence for antioxidant effects of thymoquinone. Research Communications in Molecular Pathology and Pharmacology, 110: 239-251.
Mahmoud HS, Almallah AA, Gad EL‑Hak HN, Aldayel TS, Abdelrazek HMA & Khaled EH. 2021. The effect of dietary supplementation with Nigella sativa (black seeds) mediates immunological function in male Wistar rats. Scientific Reports, 11: 7542. DOI: 10.1038/s41598-021-86721-1
Mabrouk, GM, Moselhy SS, Zohny SF, Ali EM, Helal TE, Amin AA & Khalifa AA. 2002. Inhibition of methylnitrosourea (MNU) induced oxidative stress and carcinogenesis by orally administered bee honey and Nigella grains in Sprague Dawely rats. Journal of Experimental and Clinical Cancer Research, 21: 341-346.
Nourozi E, Danesyar M & Farhoomand P. 2013. Dietary supplementation effects of zinc acetate and magnesium sulfate on performance and antioxidant status of broilers under continuous heat stress. Spanish Journal of Agricultural Research, 11(1): 127–131. DOI: 10.5424/sjar/2013111-2874
Ozogurlu F, Sahin S, Idýz N, Akyol O, Ilhan A, Yigitoglu R & Isýk B. 2005. The effect of Nigella sativa oil against experimental allergic encephalomyelitis via nitric oxide and other oxidative stress parameters. Cellular and Molecular Biology, 51: 337-342.
Ojueromi OO, Ganiyu O & Ayokunle OA. 2022. Effect of black seeds (Nigella sativa) on inflammatory and immunomodulatory markers in Plasmodium berghei-infected mice. Journal of Food Biochemistry, 00: e14300. DOI: 10.1111/jfbc.14300
Ohtsu H, Yamazaki M, Abe H, Murakami H, Toyomizu M. 2015. Heat stress modulates cytokine gene expression in the spleen of broiler chickens. Japanese Poultry Science, 52(4): 282–287. DOI: 10.2141/jpsa.0150062
Pawar SS, Basavaraj S, Dhansing LV, Pandurang, KN, Sahebrao KA, Vitthal NA, Pandit BM & Kumar BS. 2016. Assessing and mitigating the impact of heat stress in poultry. Advances in Animal and Veterinary Sciences, 4: 332–341. DOI: 10.14737/journal.aavs/ 2016/4.6.332.341
Rahman MM & Kim SJ. 2016. Effects of dietary Nigella sativa seed supplementation on broiler productive performance, oxidative status and qualitative characteristics of thighs meat. Italian Journal of Animal Science, 15(2): 241–247. DOI: 10.1080/1828051X.2016.1159925
Rhoads RP, Baumgard LH & Suagee JK. 2013. 2011 and 2012 early careers achievement awards: metabolic priorities during heat stress with an emphasis on skeletal muscle. Journal of Animal Science, 91: 2492–2503. DOI: 10.2527/jas2012- 6120
Saki A, Kalantar M, Nejad ER & Ghatabar FM. 2014. Health characteristics and performance of broiler chicks in response to Trigonella Foenum Graenaecium and Foeniculum vulgare. Iranian Journal of Applied Animal Science, 1: 387–391.
Salam S, Sunarti D & Isroli I. 2013. Physiological responses of blood and immune organs of broiler chicken fed dietary black seed powder (Nigella sativa) during dry seasons. Journal of the Indonesian Tropical Animal Agriculture, 38: 185–191. DOI: 10.14710/jitaa.38.3.185-191
Shuaib M, Nasrullah Hafeez M, Alhidary I, Abdelrahman M & Khan RU. 2021.
Effect of dietary supplementation of wild Cumin (Bunium persicum) seeds on
performance, nutrient digestibility and circulating metabolites in broiler chicks
during the finisher phase. Animal Biotechnology, DOI: 10.1080/10495398.2020.1844222
Song Z, Cheng K, Zhang L & Wang T. 2017. Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat stressed broilers. Journal of Thermal Biology, 69: 184–190. DOI: 10.1016/j.jtherbio.2017.07.015
Surai PF. 2014. Polyphenol compounds in the chicken/animal diet: from the past to the future. The Journal of Animal Physiology and Animal Nutrition, 98 (1): 19–31. DOI: 10.1111/jpn.12070.
Uyanga VA, Jingpeng Z, Xiaojuan W, Hongchao J, Okanlawon M & Onagbesan Hai Lin. 2022. Effects of dietary L-citrulline supplementation on nitric oxide synthesis, immune responses and mitochondrial energetics of broilers during heat stress. Journal of Thermal Biology, 105: 103227. DOI: 10.1016/j.jtherbio.2022.103227
Wang W, Yan F, Hu J, Amen O & Cheng H. 2018. Supplementation of Bacillus subtilis-based probiotic reduces heat stress-related behaviors and inflammatory response in broiler chickens. Journal of Animal Science, 96(5): 1654–1666.DOI: 10.1093/jas/sky092
Weinbrenner T, Fito M, Torre RD, Saez GT, Rijken P & Tormos C. 2004. Olive oils high in phenolic compounds modulate oxidative/antioxidative status in men. Journal of Nutrition, 134: 2314-2321. DOI: 10.1093/jn/134.9.2314
Xia F, Wang C, Jin Y, Liu Q, Meng Q, Liu K & Sun H. 2014. Luteolin protects HUVECs from TNF-a-induced oxidative stress and inflammation via its effects on the Nox4/ROSNF- jB and MAPK pathways. Journal of Atherosclerosis and Thrombosis, 21(8): 768-83. DOI: 10.5551/jat.23697
Yi D, Hou YQ, Tan LL, Liao M, Xie JQ, Wang L, Ding BY, Yang Y & Gong J. 2016. N-acetylcysteine improves the growth performance and intestinal function in the heat-stressed broilers. Animal Feed Science and Technology, 220: 83–92. DOI: 10.1016/j.anifeedsci.2016.07.014
Zhang C, Chen K, Zhao X & Geng Z. 2018. Protective effects of resveratrol against high ambient temperature-induced spleen dysplasia in broilers through modulating splenic redox status and apoptosis. Journal of the Science of Food and Agriculture, 98(14): 5409–5417. DOI: 10.1002/jsfa.9084