Effect of a synbiotic supplement as an antibiotic alternative on broiler skeletal, physiological, and oxidative parameters under heat stress

Abdelqader, 2020, Probiotic bacteria maintain normal growth mechanisms of heat stressed broiler chickens, J. Therm. Biol., 92, 10.1016/j.jtherbio.2020.102654 Akbarian, 2016, Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals, J. Anim. Sci. Biotechnol., 7, 37, 10.1186/s40104-016-0097-5 Alhenaky, 2017, The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds, J. Therm. Biol., 70, 9, 10.1016/j.jtherbio.2017.10.015 Altan, 2003, Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers, Br. Poult. Sci., 44, 545, 10.1080/00071660310001618334 An, 2008, Growth performance and antibody response of broiler chicks fed yeast derived β-glucan and single-strain probiotics, Asian-Australas. J. Anim. Sci., 21, 1027, 10.5713/ajas.2008.70571 Aslam, 2018, Antibiotic resistance: a rundown of a global crisis, Infect. Drug Resist, 11, 1645, 10.2147/IDR.S173867 Aviagen, 2018. Ross broiler management handbook. https://en.aviagen.com/assets/Tech_Center/Ross_Broiler/Ross-BroilerHandbook2018-EN.pdf. Accessed Jan. 2022. Awad, 2009, Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens, Poult. Sci., 88, 49, 10.3382/ps.2008-00244 Azad, 2018, Immunomodulatory effects of probiotics on cytokine profiles, Biomed. Res. Int., 2018, 8063647, 10.1155/2018/8063647 Bae, 2019, Editorial: Stress and immunity, Front. Immunol., 10, 1, 10.3389/fimmu.2019.00245 Bagath, 2019, The impact of heat stress on the immune system in dairy cattle: a review, Res. Vet. Sci., 126, 94, 10.1016/j.rvsc.2019.08.011 Baxter, 2020, Water amino acid-chelated trace mineral supplementation decreases circulating and intestinal HSP70 and proinflammatory cytokine gene expression in heat-stressed broiler chickens, J. Anim. Sci., 98, 1, 10.1093/jas/skaa049 Castanon, 2007, History of the use of antibiotic as growth promoters in European poultry feeds, Poult. Sci., 86, 2466, 10.3382/ps.2007-00249 Cervantes, 2015, Antibiotic-free poultry production: is it sustainable?, J. Appl. Poult. Res., 24, 91, 10.3382/japr/pfv006 Chen, 2018, Dietary synbiotic incorporation as an alternative to antibiotic improves growth performance, intestinal morphology, immunity and antioxidant capacity of broilers, J. Sci. Food Agric., 98, 3343, 10.1002/jsfa.8838 Christakos, 2010, Vitamin D: metabolism, Endocrinol. Metab. Clin. North Am., 39, 243, 10.1016/j.ecl.2010.02.002 Colles, 2008, Campylobacter infection of broiler chickens in a free-range environment, Environ. Microbiol., 10, 2042, 10.1111/j.1462-2920.2008.01623.x De Boever, 2008, The influence of age and repeated lipopolysaccharide administration on body temperature and the concentration of interleukin-6 and IgM antibodies against lipopolysaccharide in broiler chickens, Avian Pathol., 37, 39, 10.1080/03079450701784875 De Oliveira, 2019, Bacillus amyloliquefaciens CECT 5940 alone or in combination with antibiotic growth promoters improves performance in broilers under enteric pathogen challenge, Poult. Sci., 98, 4391, 10.3382/ps/pez223 Engberg, 2000, Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers, Poult. Sci., 79, 1311, 10.1093/ps/79.9.1311 Feder, 1999, Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology, Annu. Rev. Physiol., 61, 243, 10.1146/annurev.physiol.61.1.243 Ghareeb, 2012, Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens, Poult. Sci., 91, 1825, 10.3382/ps.2012-02168 Ghosh, 2018, 45 Grunwald, 2014, The oxidation of HSP70 is associated with functional impairment and lack of stimulatory capacity, Cell Stress Chaperones., 19, 913, 10.1007/s12192-014-0516-5 Gyawali, 2019, 151 Hassanpour, 2013, Effects of synbiotic on the intestinal morphology and humoral immune response in broiler chickens, Livest. Sci., 153, 116, 10.1016/j.livsci.2013.02.004 Honda, 2015, Effects of heat stress on peripheral T and B lymphocyte profiles and IgG and IgM serum levels in broiler chickens vaccinated for Newcastle disease virus, Poult. Sci., 94, 2375, 10.3382/ps/pev192 Huang, 2019, Effects of the dietary probiotic, enterococcus faecium NCIMB11181, on the intestinal barrier and system immune status in Escherichia coli O78-challenged broiler chickens, Probiotics Antimicrob. Proteins., 11, 946, 10.1007/s12602-018-9434-7 Humam, 2021, Supplementation of postbiotic RI11 improves antioxidant enzyme activity, upregulated gut barrier genes, and reduced cytokine, acute phase protein, and heat shock protein 70 gene expression levels in heat-stressed broilers, Poult. Sci., 100, 10.1016/j.psj.2020.12.011 Humphrey, 2014, Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare, MBio, 5, 1, 10.1128/mBio.01364-14 Ikwegbue, 2018, Roles of heat shock proteins in apoptosis, oxidative stress, human inflammatory diseases, and cancer, Pharmaceuticals, 11, 1 Jee, 2016, Size dependent classification of heat shock proteins: a mini-review, J. Exerc. Rehabil., 12, 255, 10.12965/jer.1632642.321 Khan, 2019, Selenium-enriched probiotics improve hepatic protection by regulating pro-inflammatory cytokines and antioxidant capacity in broilers under heat stress conditions, J. Adv. Vet. Anim. Res., 6, 355, 10.5455/javar.2019.f354 Kirchhelle, 2020, Setting the standard: multidisciplinary hallmarks for structural, equitable and tracked antibiotic policy, BMJ Glob. Heal., 5, 1 Kjaer, 2006, Foot pad dermatitis and hock burn in broiler chickens and degree of inheritance, Poult. Sci., 85, 1342, 10.1093/ps/85.8.1342 Koltes, 2017, Effects of bacitracin methylene disalicylate and diet change on gastrointestinal integrity and endotoxin permeability in the duodenum of broiler chicken, BMC Res. Notes., 10, 8, 10.1186/s13104-017-2781-8 Konstantinidis, 2020, Effects of antibiotics upon the gut microbiome: a review of the literature, Biomedicines., 8, 1, 10.3390/biomedicines8110502 Kuehn, 2014, FDA moves to curb antibiotic use in livestock, JAMA - J. Am. Med. Assoc., 311, 347, 10.1001/jama.2013.285704 Lara, 2013, Impact of heat stress on poultry production, Animals., 3, 356, 10.3390/ani3020356 Li, 2020, Probiotics, prebiotics, and synbiotics regulate the intestinal microbiota differentially and restore the relative abundance of specific gut microorganisms, J. Dairy Sci., 103, 5816, 10.3168/jds.2019-18003 Liu, 2020, Heat stress impacts on broiler performance: a systematic review and meta-analysis, Poult. Sci., 99, 6205, 10.1016/j.psj.2020.08.019 Liu, 2016, Real-time investigation of antibiotics-induced oxidative stress and superoxide release in bacteria using an electrochemical biosensor, Free Radic. Biol. Med., 91, 25, 10.1016/j.freeradbiomed.2015.12.001 Mazmanian, 2005, An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system, Cell., 122, 107, 10.1016/j.cell.2005.05.007 Millet, 2011, The European ban on antibiotic growth promoters in animal feed: from challenges to opportunities, Vet. J., 187, 143, 10.1016/j.tvjl.2010.05.001 Min, 2016, Effects of dietary supplementation of synbiotics on growth performance, intestinal morphology, sIgA content and antioxidant capacities of broilers, J. Anim. Physiol. Anim. Nutr. (Berl)., 100, 1073, 10.1111/jpn.12479 Mohammed, 2018, Effect of dietary syn-biotic supplement on behavioral patterns and growth performance of broiler chickens reared under heat stress, Poult. Sci., 97, 1101, 10.3382/ps/pex421 Montilla, 2014, Heat stress causes oxidative stress but not inflammatory signaling in porcine skeletal muscle, Temperature., 1, 42, 10.4161/temp.28844 Nadeem, 2020, Antimicrobial resistance: more than 70 years of war between humans and bacteria, Crit. Rev. Microbiol., 46, 578, 10.1080/1040841X.2020.1813687 Petruk, 2004, Broiler breeder egg production and quality are affected by timing of increased dietary Ca relative to photostimulation, Can. J. Anim. Sci., 85, 411, 10.4141/A03-030 Redweik, 2020, Live bacterial prophylactics in modern poultry, Front. Vet. Sci., 7, 1, 10.3389/fvets.2020.592312 Rehman, 2020, Dietary effect of probiotics and prebiotics on broiler performance, carcass, and immunity, Poult. Sci., 99, 6946, 10.1016/j.psj.2020.09.043 Richter, 2010, The heat shock response: life on the verge of death, Mol. Cell., 40, 253, 10.1016/j.molcel.2010.10.006 Romagnani, 1997, The Th1/Th2 paradigm, Immunol. Today., 18, 263, 10.1016/S0167-5699(97)80019-9 Ruff, 2021, Evaluation of three formulations of essential oils in broiler chickens under cyclic heat stress, Animals., 11, 1, 10.3390/ani11041084 Saleh, 2012, Feeding Aspergillus awamori reduces skeletal muscle protein breakdown and stimulates growth in broilers, Anim. Sci. J., 83, 594, 10.1111/j.1740-0929.2011.00999.x Sannasimuthu, 2020, Intracellular oxidative damage due to antibiotics on gut bacteria reduced by glutathione oxidoreductase-derived antioxidant molecule GM15, Arch. Microbiol., 202, 1127, 10.1007/s00203-020-01825-y Scanes, 2020, Avian physiology: are birds simply feathered mammals?, Front. Physiol., 11, 1, 10.3389/fphys.2020.542466 Scholz-Ahrens, 2007, Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure, J. Nutr., 137, 10.1093/jn/137.3.838S Shahir, 2014, Effects of dietary inclusion of probiotic or prebiotic on growth performance, organ weight, blood parameters and antibody titers against influenza and newcastle in broiler chickens, Int. J. Poult. Sci., 13, 70, 10.3923/ijps.2014.70.75 Shepherd, 2010, Footpad dermatitis in poultry, Poult. Sci., 89, 2043, 10.3382/ps.2010-00770 Shin, 2020, Absolute configuration and antibiotic activity of piceamycin, J. Nat. Prod., 83, 277, 10.1021/acs.jnatprod.9b00678 Shini, 2020, Probiotic Bacillus amyloliquefaciens H57 ameliorates subclinical necrotic enteritis in broiler chicks by maintaining intestinal mucosal integrity and improving feed efficiency, Poult. Sci., 99, 4278, 10.1016/j.psj.2020.05.034 Siddiqui, 2020, Chronic heat stress regulates the relation between heat shock protein and immunity in broiler small intestine, Sci. Rep., 10, 1, 10.1038/s41598-020-75885-x Singh, 2008, Effect of supplementation of diets with BMD and Virginiamycin on the growth performance, carcass characteristics and bacterial population in broiler chickens, Vet. World., 1, 141 Slimen, 2014, Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review, Int. J. Hyperth., 30, 513, 10.3109/02656736.2014.971446 Song, 2011, Effects of feeding diets containing bacitracin methylene disalicylate to heat-stressed finishing pigs, J. Anim. Sci., 89, 1830, 10.2527/jas.2010-3218 Strzępa, 2017, Broad spectrum antibiotic enrofloxacin modulates contact sensitivity through gut microbiota in a murine model, J. Allergy Clin. Immunol., 140, 121, 10.1016/j.jaci.2016.11.052 Swiatkiewicz, 2017, The nutrition of poultry as a factor affecting litter quality and foot pad dermatitis - an updated review, J Anim Physiol Anim Nutr (Berl), 101, e14, 10.1111/jpn.12630 Tanaka, 2014, IL-6 in inflammation, immunity, and disease, Cold Spring Harb Perspect Biol, 6, a016295, 10.1101/cshperspect.a016295 Tanaka, 2014, IL-6 in inflammation, immunity, and disease, Cold Spring Harb. Perspect. Biol., 6, 10.1101/cshperspect.a016295 Tang, 2018, Rosemary reduces heat stress by inducing CRYAB and HSP70 expression in broiler chickens, Oxid. Med. Cell. Longev., 2018, 7014126, 10.1155/2018/7014126 Toppel, 2019, Effect of pH-lowering litter amendment on animal-based welfare indicators and litter quality in a European commercial broiler husbandry, Poult. Sci., 98, 1181, 10.3382/ps/pey489 Tu, 2021, The microbiota-gut-bone axis and bone health, J. Leukoc. Biol, 110, 525, 10.1002/JLB.3MR0321-755R Tuo, 2018, Screening probiotics from Lactobacillus strains according to their abilities to inhibit pathogen adhesion and induction of pro-inflammatory cytokine IL-8, J. Dairy Sci., 101, 4822, 10.3168/jds.2017-13654 Ubeda, 2012, Antibiotics, microbiota, and immune defense, Trends Immunol., 33, 459, 10.1016/j.it.2012.05.003 Wang, 2018, Supplementation of Bacillus subtilis-based probiotic reduces heat stress-related behaviors and inflammatory response in broiler chickens, J. Anim. Sci., 96, 1654, 10.1093/jas/sky092 Webster, 2008, Validation of a three-point gait-scoring system for field assessment of walking ability of commercial broilers, J. Appl. Poult. Res., 17, 529, 10.3382/japr.2008-00013 Wideman, 2016, Bacterial chondronecrosis with osteomyelitis and lameness in broilers: a review, Poult. Sci., 95, 325, 10.3382/ps/pev320 Wideman, 2012, Dexamethasone triggers lameness associated with necrosis of the proximal tibial head and proximal femoral head in broilers, Poult. Sci., 91, 2464, 10.3382/ps.2012-02386 Wideman, 2012, A wire-flooring model1 for inducing lameness in broilers: evaluation of probiotics as a prophylactic treatment, Poult. Sci., 91, 870, 10.3382/ps.2011-01907 Yan, 2019, Effects of a dietary synbiotic inclusion on bone health in broilers subjected to cyclic heat stress episodes, Poult. Sci., 98, 1083, 10.3382/ps/pey508