Effects of Heat Stress on Production Performance, Redox Status, Intestinal Morphology and Barrier-Related Gene Expression, Cecal Microbiome, and Metabolome in Indigenous Broiler Chickens

Abstract

This study was done to evaluate the effects of heat stress (HS) on production performance, redox status, small intestinal barrier-related parameters, cecal microbiota, and metabolome of indigenous broilers. A total of forty female indigenous broilers (56-day-old) were randomly and equally divided into normal treatment group (NT group, 21.3 ± 1.2°C, 24 h/day) and HS group (32.5 ± 1.4°C, 8 h/day) with five replicates of each for 4 weeks feeding trial. The results showed that the body weight gain (BWG) of broilers in HS group was lower than those in NT group during 3–4 weeks and 1–4 weeks (p < 0.05). The HS exposure increased the abdominal fat rate (p < 0.05) but decreased the thigh muscle rate (p < 0.01). Besides, broilers in HS group had higher drip loss of breast muscle than NT group (p < 0.01). Broilers exposed to HS had lower total antioxidant capacity (T-AOC) in serum and jejunum, activities of total superoxide dismutase (T-SOD) in the jejunum, glutathione peroxidase (GSH-Px) in the thigh muscle, duodenum, and jejunum; and catalase (CAT) in breast muscle, duodenum, and jejunum (p < 0.05). Whereas the malondialdehyde (MDA) contents in breast muscle, duodenum, and jejunum was elevated by HS exposure (p < 0.05). Moreover, the relative mRNA expression of Occludin and ZO-1 in the duodenum, Occludin, Claudin-1, Claudin-4, ZO-1, Mucin-2 in the jejunum, and the Claudin-4 and Mucin-2 in the ileum was down-regulated by HS exposure (p < 0.05). The 16S rRNA sequencing results showed that the HS group increased the relative abundance of Anaerovorax in the cecum at the genus level (p < 0.05). Cecal metabolomics analysis indicated 19 differential metabolites between the two groups (p < 0.10, VIP >1). The Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that the differential metabolites mainly enriched in 10 signaling pathways such as the Citrate cycle (TCA cycle) (p < 0.01). In summary, chronic HS exposure caused a decline of production performance, reduced antioxidant capacity, disrupted intestinal barrier function, and negatively affected cecal microbiota and metabolome in indigenous broilers.

Effects of brown seaweed products on growth performance, plasma biochemistry, immune response, and antioxidant capacity of broiler chickens challenged with heat stress

“…Exposure of broiler chicks to an acute temperature of 32°C for 6 h induced metabolic changes that triggered oxidative stress ( Lin et al, 2006 ). A recent study by Liu et al (2022a) further confirmed that chronic HS (32.5 ± 1.4°C for 8 h/d) for 4 wk induced oxidative stress in broilers evidenced by elevated MDA levels and reduced antioxidant enzymes activity in serum, muscles and small intestines. Enzymatic and non-enzymatic antioxidant defence systems can be internally synthesized or externally supplied in response to oxidative stress and increased due to defence mechanisms against heat-induced oxidative stress ( Akbarian et al, 2016 ; Surai et al, 2019 ).…”

A review of heat stress in chickens. Part I: Insights into physiology and gut health

“…Enteral inflammation has been shown to shorten the lifespan of enterocytes and cause crypt hyperplasia and villus atrophy (Smith et al, 2014). These alterations in intestinal epithelium morphology (microarchitecture), along with increased cell apoptosis and reduced cell proliferation, have recently been observed in broiler chickens exposed to HS (He et al, 2018a(He et al, , 2018bLiu et al, 2020Liu et al, , 2022Nanto-Hara et al, 2020). In their pair-feeding study with broilers, Nanto-Hara et al ( 2020) evidenced that intestinal morphological damage and increased intestinal permeability are direct consequences of HS rather than of feed intake reduction induced by HS itself.…”

“…For instance, data from several studies indicate that high ambient temperatures can dramatically shape the GI microbiota. Specifically, it has been demonstrated that HS perturbs the GI microbiota in rats ( Suzuki et al, 1983 , 1989 ), poultry ( Suzuki et al, 1983 , 1989 ; Lan et al, 2004 ; Burkholder et al, 2008 ; Song et al, 2014 ; Wang X. J. et al, 2018 ; He et al, 2019b ; Shi et al, 2019 ; Xing et al, 2019 ; Zhu et al, 2019 ; Liu et al, 2020 ; Wang et al, 2020 ; He et al, 2021 ; Liu et al, 2022 ), dairy cattle ( Chen et al, 2018 ), and pigs ( He et al, 2019a ; Le Sciellour et al, 2019 ; Xiong et al, 2020 ), pushing it to dysbiosis. Dysbiosis (dysbacteriosis) is an alteration in the gut microbiota with an overgrowth of harmful microorganisms, or a depletion of beneficial bacteria, which can weaken the fragile equilibrium between the host and its GI microbiota ( Walker, 2017 ; Ducatelle et al, 2018 ).…”

“…A dysbiotic state is often associated with depression in nutrient digestion, loss of intestinal barrier function, and GI inflammation ( Chen et al, 2015 ; Ducatelle et al, 2018 ), whereas eubiosis, referred to as a balanced microbial ecosystem ( Iebba et al, 2016 ), can enhance health, productivity, and ability of chickens to withstand environmental stressors ( Kogut, 2019 ). Although cutting-edge analytical techniques are currently available to study the GI microbiota ( Borda-Molina et al, 2018 ), the modifications in structure, composition, and functions of the GI microbiota of heat-stressed chickens are still to be fully understood ( He et al, 2021 ; Liu et al, 2022 ). However, changes in GI morphology, mucus quantity and composition, and attachment sites, coupled with an accumulation of poorly digested or even undigested feed components, are all plausible reasons for HS-caused dysbiosis.…”

“…Ducatelle et al (2018),He et al (2018a),He et al (2018b),Epstein and Yanovich (2019), Nanto-Hara et al (2020),Ruff et al (2020),Tabler et al (2020),Liu et al (2020),Liu et al (2022) ↑ paracellular permeability (↓ transepithelial electrical resistance and ↑ mucosa-to-serosa flux of markers) → "leaky gut"↓GI epithelium integrity LPS/endotoxins leakage → ↑ pro-inflammatory cytokines → GI inflammation and ↓ GI barrier ↓ liver health and functionality Endotoxemia → systemic inflammation, multi-organ failure, and septic shock "Bacterial translocation" → ↓ liver health and functionality bacterial chondronecrosis with osteomyelitis Upward arrow (↑), increase; downward arrow (↓), decrease; rightward arrow (→), consequence/degeneration. a Include studies on non-avian species that have exhibited comparable heat stress effects and responses to those observed in chickens.…”