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RESEARCH ARTICLE

Resveratrol alleviates heat stress-induced impairment of intestinal morphology, barrier integrity and inflammation in yellow-feather broilers

Shaoping He https://orcid.org/0000-0003-0373-8265 A B , Liang Chen C , Yujia He D , Fu Chen A , Yujing Ma A , Dingfu Xiao A and Jianhua He A E
+ Author Affiliations
- Author Affiliations

A College of Animal Science and Technology, Hunan Agricultural University, No.1 Nongda Road, Furong District, Changsha 410128, China.

B Key Laboratory of Microecological Resources and Utilisation in Breeding Industry, Ministry of Agriculture and Rural Affairs, Haid Central Research Institute, Animal Husbandry and Fisheries Research Center of Guangdong Haid Group Co., No. 5, 8th Street, Fuping Road, Panyu District, Guangzhou, 511400, China.

C Huaihua Institute of Agricultural Sciences, No.140 Yingfeng East Road, Hecheng District, Huaihua, 418000, China.

D College of Veterinary Science, Hunan Agricultural University, No.1 Nongda Road, Furong District, Changsha 410128, China.

E Corresponding author. Email: jianhuahy@hunau.net

Animal Production Science 60(12) 1547-1556 https://doi.org/10.1071/AN19218
Submitted: 18 April 2019  Accepted: 17 January 2020   Published: 30 March 2020

Abstract

Context: Heat stress is one of the problems commonly found in broiler industry in tropic and subtropic regions that results in impairment of intestinal integrity, leading to inflammation and poor performance.

Aims: This study aimed to investigate the effect of dietary resveratrol supplementation on growth performance, intestinal morphology and barrier integrity, and inflammation response of yellow-feather broilers under heat stress.

Methods: In total, 288 birds (28-day-old) were randomly allotted to three treatment groups, with six replicates. A thermo-neutral group (24 ± 2°C) received a basal diet and two heat-stressed groups (37 ± 2°C for 8 h/day and 24 ± 2°C for the remaining time) were fed the basal diet (HT) or basal diet supplemented with 500 mg/kg resveratrol for 14 consecutive days.

Key results: Compared with the thermo-neutral group, birds in the HT group had a decreased (P < 0.05) average daily feed intake, average daily gain, villus height, villus height to crypt depth ratio, mRNA concentrations of mucin-2, secreted immunoglobulin A (sIgA), claudin-1,zona occludens-1 and serum concentrations of interferon γ, and increased (P < 0.05) feed to gain ratio, crypt depth, mRNA levels of expression of heat-shock protein (HSP) 70, HSP90, nuclear factor kappa B, mucin-4, claudin-2 and serum concentrations of endotoxin, interleukin (IL)-1β, IL-4, IL-6 and tumour necrosis factor (TNF)-α on Day 3 and Day 14, except for claudin-1 on Day 14 and TNF-α on Day 3 (P > 0.05). Compared with HT group, birds in HT supplemented with resveratrol group decreased (P < 0.05) crypt depth (in jejunum on Day 3, ileum on Day 14), mRNA levels of expression of HSP70, HSP90, nuclear factor kappa B, mucin-4, claudin-2 and serum concentrations of endotoxin, IL-1β, IL-4, IL-6 and TNF-α, and increased (P < 0.05) average daily feed intake (+11%), average daily gain (+22%) and villus height, villus height to crypt depth ratio, mRNA levels of expression of mucin-2, sIgA, claudin-1,zona occludens-1 and serum concentrations of interferon γ, although with few fluctuations between Day 3 and Day 14.

Conclusions: Dietary supplementation of resveratrol was effective in partially alleviating the adverse effects of heat stress on growth performance and intestinal barrier function in yellow-feather broilers, by restoring the impaired villus-crypt structure, altering the mRNA expression of intestinal HSPs, mucins, sIgA and tight junction-related gene, and inhibiting secretion of pro-inflammation cytokines.

Implications: Dietary resveratrol supplementation is a considerable nutritional strategy to anti-stress in animal production.

Additional keywords: resveratrol, growth performance, stress, intestinal barrier, inflammation.


References

Abdelqader AM, Abuajamieh M, Hammad HM, Al-Fataftah ARA (2017) Effects of dietary butyrate supplementation on intestinal integrity of heat-stressed cockerels. Journal of Animal Physiology and Animal Nutrition 101, 1115–1121.
Effects of dietary butyrate supplementation on intestinal integrity of heat-stressed cockerels.Crossref | GoogleScholarGoogle Scholar | 28063242PubMed |

Alarcón de la Lastra C, Villegas I (2005) Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Molecular Nutrition & Food Research 49, 405–430.
Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications.Crossref | GoogleScholarGoogle Scholar |

Alhenaky A, Abdelqader A, Abuajamieh M, Al-Fataftah A (2017) The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. Journal of Thermal Biology 70, 9–14.
The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds.Crossref | GoogleScholarGoogle Scholar | 29108563PubMed |

Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, Usman MM, Ijaz S, Rehman H (2013) Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. Journal of Animal Physiology and Animal Nutrition 97, 68–73.
Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress.Crossref | GoogleScholarGoogle Scholar | 23639019PubMed |

Berman AY, Motechin RA, Wiesenfeld MY, Holz MK (2017) The therapeutic potential of resveratrol: a review of clinical trials. NPJ Precision Oncology 1, 35–51.
The therapeutic potential of resveratrol: a review of clinical trials.Crossref | GoogleScholarGoogle Scholar | 28989978PubMed |

Bitterman JL, Chung JH (2015) Metabolic effects of resveratrol: addressing the controversies. Cellular and Molecular Life Sciences 72, 1473–1488.
Metabolic effects of resveratrol: addressing the controversies.Crossref | GoogleScholarGoogle Scholar | 25548801PubMed |

Borges SC, Ferreira P, Da SL, de Paula WM, Irache JM, Cavalcanti OA, Buttow NC (2018) Evaluation of the treatment with resveratrol-loaded nanoparticles in intestinal injury model caused by ischemia and reperfusion. Toxicology 396–397, 13–22.
Evaluation of the treatment with resveratrol-loaded nanoparticles in intestinal injury model caused by ischemia and reperfusion.Crossref | GoogleScholarGoogle Scholar | 29427784PubMed |

Camilleri M, Madsen K, Spiller R, Van Meerveld BG, Verne GN (2012) Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterology and Motility 24, 503–512.
Intestinal barrier function in health and gastrointestinal disease.Crossref | GoogleScholarGoogle Scholar | 22583600PubMed |

Deng W, Dong XF, Tong JM, Zhang Q (2012) The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poultry Science 91, 575–582.
The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens.Crossref | GoogleScholarGoogle Scholar | 22334732PubMed |

Ganesan S, Volodina O, Pearce SC, Gabler NK, Baumgard LH, Rhoads RP, Selsby JT (2017) Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle. Physiological Reports 5, 13397
Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle.Crossref | GoogleScholarGoogle Scholar |

Groschwitz KR, Hogan SP (2009) Intestinal barrier function: molecular regulation and disease pathogenesis. The Journal of Allergy and Clinical Immunology 124, 3–20.
Intestinal barrier function: molecular regulation and disease pathogenesis.Crossref | GoogleScholarGoogle Scholar | 19560575PubMed |

He SP, Arowolo MA, Medrano RF, Li S, Yu QF, Chen JY, He JH (2018) Impact of heat stress and nutritional interventions on poultry production. World’s Poultry Science Journal 74, 647–664.
Impact of heat stress and nutritional interventions on poultry production.Crossref | GoogleScholarGoogle Scholar |

Heled Y, Fleischmann C, Epstein Y (2013) Cytokines and their role in hyperthermia and heat stroke. Journal of Basic and Clinical Physiology and Pharmacology 24, 85–96.
Cytokines and their role in hyperthermia and heat stroke.Crossref | GoogleScholarGoogle Scholar | 23509213PubMed |

Holmes-McNary M, Baldwin AJ (2000) Chemopreventive properties of trans-resveratrol are associated with inhibition of activation of the IkappaB kinase. Cancer Research 60, 3477–3483. doi.org/ content/60/13/3477

Jeurissen SH, Lewis F, van der Klis JD, Mroz Z, Rebel JM, ter Huurne AA (2002) Parameters and techniques to determine intestinal health of poultry as constituted by immunity, integrity, and functionality. Current Issues in Intestinal Microbiology 3, 1–14.

Joly A, Wettstein G, Mignot G, Ghiringhelli F, Garrido C (2010) Dual role of heat shock proteins as regulators of apoptosis and innate immunity. Journal of Innate Immunity 2, 238–247.
Dual role of heat shock proteins as regulators of apoptosis and innate immunity.Crossref | GoogleScholarGoogle Scholar | 20375559PubMed |

Lara L, Rostagno M (2013) Impact of heat stress on poultry production. Animals 3, 356–369.
Impact of heat stress on poultry production.Crossref | GoogleScholarGoogle Scholar | 26487407PubMed |

Li J, Liu Y, Duan P, Yu R, Gu Z, Li L, Liu Z, Su L (2018) NFkappaB regulates HSF1 and cJun activation in heat stress induced intestinal epithelial cell apoptosis. Molecular Medicine Reports 17, 3388–3396.
NFkappaB regulates HSF1 and cJun activation in heat stress induced intestinal epithelial cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 29257252PubMed |

Liu LL, He JH, Xie HB, Yang YS, Li JC, Zou Y (2014) Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poultry Science 93, 54–62.
Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens.Crossref | GoogleScholarGoogle Scholar | 24570423PubMed |

Liu L, Fu C, Yan M, Xie H, Li S, Yu Q, He S, He J (2016) Resveratrol modulates intestinal morphology and HSP70/90, NF-kappaB and EGF expression in the jejunal mucosa of black-boned chickens on exposure to circular heat stress. Food & Function 7, 1329–1338.
Resveratrol modulates intestinal morphology and HSP70/90, NF-kappaB and EGF expression in the jejunal mucosa of black-boned chickens on exposure to circular heat stress.Crossref | GoogleScholarGoogle Scholar |

Muralidharan S, Mandrekar P (2013) Cellular stress response and innate immune signaling: integrating pathways in host defense and inflammation. Journal of Leukocyte Biology 94, 1167–1184.
Cellular stress response and innate immune signaling: integrating pathways in host defense and inflammation.Crossref | GoogleScholarGoogle Scholar | 23990626PubMed |

Narinç D, Erdoğan S, Tahtabiçen E, Aksoy T (2016) Effects of thermal manipulations during embryogenesis of broiler chickens on developmental stability, hatchability and chick quality. Animal 10, 1328–1335.
Effects of thermal manipulations during embryogenesis of broiler chickens on developmental stability, hatchability and chick quality.Crossref | GoogleScholarGoogle Scholar | 26932726PubMed |

NRC (1994) ‘Nutrient requirements of poultry.’ 9th edn. (National Academies Press: Washington, DC)

Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sakai M, Sa LR, Ferreira AJ, Palermo-Neto J (2010) Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poultry Science 89, 1905–1914.
Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 20709975PubMed |

Quinteiro-Filho WM, Rodrigues MV, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sa LR, Ferreira AJ, Palermo-Neto J (2012) Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation. Journal of Animal Science 90, 1986–1994.
Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation.Crossref | GoogleScholarGoogle Scholar | 22228037PubMed |

Sahin K, Orhan C, Akdemir F, Tuzcu M, Iben C, Sahin N (2012) Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. Journal of Animal Physiology and Animal Nutrition 96, 66–74.
Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins.Crossref | GoogleScholarGoogle Scholar | 21244525PubMed |

Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, Shi B, Zou XT (2014) Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poultry Science 93, 581–588.
Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress.Crossref | GoogleScholarGoogle Scholar | 24604851PubMed |

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.
Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat-stressed broilers.Crossref | GoogleScholarGoogle Scholar | 29037381PubMed |

Sun X, Zhang H, Sheikhahmadi A, Wang Y, Jiao H, Lin H, Song Z (2015) Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). International Journal of Biometeorology 59, 127–135.
Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus).Crossref | GoogleScholarGoogle Scholar | 24736810PubMed |

Sun L, Zou LX, Wang J, Chen T, Han YC, Zhu DD, Zhuo SC (2018) Mucin 4 gene silencing reduces oxidative stress and calcium oxalate crystal formation in renal tubular epithelial cells through the extracellular signal-regulated kinase signaling pathway in nephrolithiasis rat model. Kidney & Blood Pressure Research 43, 820–835.
Mucin 4 gene silencing reduces oxidative stress and calcium oxalate crystal formation in renal tubular epithelial cells through the extracellular signal-regulated kinase signaling pathway in nephrolithiasis rat model.Crossref | GoogleScholarGoogle Scholar |

Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cellular and Molecular Life Sciences 70, 631–659.
Regulation of intestinal epithelial permeability by tight junctions.Crossref | GoogleScholarGoogle Scholar | 22782113PubMed |

Syafwan S, Kwakkel RP, Verstegen MWA (2011) Heat stress and feeding strategies in meat-type chickens. World’s Poultry Science Journal 67, 653–674.
Heat stress and feeding strategies in meat-type chickens.Crossref | GoogleScholarGoogle Scholar |

Tang S, Yin B, Xu J, Bao E (2018) Rosemary reduces heat stress by inducing CRYAB and HSP70 expression in broiler chickens. Oxidative Medicine and Cellular Longevity 2018, 7014126
Rosemary reduces heat stress by inducing CRYAB and HSP70 expression in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 30425783PubMed |

Wan X, Jiang L, Zhong H, Lu Y, Zhang L, Wang T (2017) Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress. Animal Science Journal 88, 1239–1246.
Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 28052518PubMed |

Wang H, Xue Y, Zhang H, Huang Y, Yang G, Du M, Zhu M (2013) Dietary grape seed extract ameliorates symptoms of inflammatory bowel disease in IL10-deficient mice. Molecular Nutrition & Food Research 57, 2253–2257.
Dietary grape seed extract ameliorates symptoms of inflammatory bowel disease in IL10-deficient mice.Crossref | GoogleScholarGoogle Scholar |

Xu D, Li W, Huang Y, He J, Tian Y (2014) The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on immune response in chicken spleen under heat stress. Biological Trace Element Research 160, 232–237.
The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on immune response in chicken spleen under heat stress.Crossref | GoogleScholarGoogle Scholar | 24965082PubMed |

Xu J, Tang S, Song E, Yin B, Wu D, Bao E (2017) Hsp70 expression induced by co-enzyme Q10 protected chicken myocardial cells from damage and apoptosis under in vitro heat stress. Poultry Science 96, 1426–1437.
Hsp70 expression induced by co-enzyme Q10 protected chicken myocardial cells from damage and apoptosis under in vitro heat stress.Crossref | GoogleScholarGoogle Scholar | 27794544PubMed |

Yang G, Wang H, Kang Y, Zhu MJ (2014) Grape seed extract improves epithelial structure and suppresses inflammation in ileum of IL-10-deficient mice. Food & Function 5, 2558–2563.
Grape seed extract improves epithelial structure and suppresses inflammation in ileum of IL-10-deficient mice.Crossref | GoogleScholarGoogle Scholar |

Yang G, Xue Y, Zhang H, Du M, Zhu MJ (2015) Favourable effects of grape seed extract on intestinal epithelial differentiation and barrier function in IL10-deficient mice. British Journal of Nutrition 114, 15–23.
Favourable effects of grape seed extract on intestinal epithelial differentiation and barrier function in IL10-deficient mice.Crossref | GoogleScholarGoogle Scholar | 25990915PubMed |

Yang G, Bibi S, Du M, Suzuki T, Zhu MJ (2017) Regulation of the intestinal tight junction by natural polyphenols: a mechanistic perspective. Kidney & Blood Pressure Research 57, 3830–3839.
Regulation of the intestinal tight junction by natural polyphenols: a mechanistic perspective.Crossref | GoogleScholarGoogle Scholar |

Zhang C, Zhao XH, Yang L, Chen XY, Jiang RS, Jin SH, Geng ZY (2017) Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poultry Science 96, 4325–4332.
Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers.Crossref | GoogleScholarGoogle Scholar | 29053872PubMed |