{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T20:28:29Z","timestamp":1785529709159,"version":"3.56.0"},"reference-count":41,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2023,8,21]],"date-time":"2023-08-21T00:00:00Z","timestamp":1692576000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Australian Pork Limited (APL)","award":["2016\/081"],"award-info":[{"award-number":["2016\/081"]}]},{"name":"Australian Pork Limited (APL)","award":["2018\/0076"],"award-info":[{"award-number":["2018\/0076"]}]},{"name":"Vietnam International Education Cooperation Department (VIED)","award":["2016\/081"],"award-info":[{"award-number":["2016\/081"]}]},{"name":"Vietnam International Education Cooperation Department (VIED)","award":["2018\/0076"],"award-info":[{"award-number":["2018\/0076"]}]},{"name":"The University of Melbourne","award":["2016\/081"],"award-info":[{"award-number":["2016\/081"]}]},{"name":"The University of Melbourne","award":["2018\/0076"],"award-info":[{"award-number":["2018\/0076"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Climate change is associated with an increased frequency and intensity of heat waves, posing a threat of heat stress to pig production. Heat stress compromises the efficiency of pig production partly due to causing oxidative stress, intestinal dysfunction, and inflammatory responses. Superoxide dismutase is an antioxidant enzyme reported to reduce oxidative stress and inflammation. Therefore, this experiment aimed to investigate whether recombinant superoxide dismutase (rSOD) could ameliorate oxidative stress and inflammatory responses in heat-stressed grower pigs. Sixty-four female pigs (Large White \u00d7 Landrace, 27.8 \u00b1 1.65 kg, mean \u00b1 SD) were randomly allocated to a control diet (standard grower feed, CON) or the control diet supplemented with 50 IU recombinant superoxide dismutase (rSOD) for 14 days. After acclimation to the diet, pigs were then housed under thermoneutral (TN, 20 \u00b0C, 35\u201350% relative humidity) or cyclic heat stress conditions (CHS, at 35 \u00b0C: 9 a.m. to 5 p.m. and 28 \u00b0C: 5 p.m. to 9 a.m., 35\u201350% relative humidity) for 3 days. Heat stress increased respiration rate (RR), skin and rectal temperature (RR and RT) (p &lt; 0.001 for all), and reduced plasma thyroid hormone concentration (p &lt; 0.001). The amount of oxidized glutathione (GSH:GSSG) was increased in the jejunum and ileum of CHS pigs. In the jejunum, rSOD also increased the amount of oxidized glutathione in both TN and CHS pigs, without any change in endogenous SOD activity. In the ileum, rSOD prevented increases in oxidized glutathione formation in the CHS pigs only. Taken together, this may reflect increased oxidative stress in both the jejunum and ileum in CHS pigs. Alternatively, rSOD increased the conversion of reduced to oxidized glutathione independently of CHS, possibly reflecting an increased overall SOD activity due to the addition of exogenous SOD. In conclusion, the use of in-feed SOD enzymes at a dose of 50 IU\/kg may be a useful strategy for preventing oxidative stress in pigs.<\/jats:p>","DOI":"10.3390\/ani13162681","type":"journal-article","created":{"date-parts":[[2023,8,21]],"date-time":"2023-08-21T01:38:31Z","timestamp":1692581911000},"page":"2681","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Using Recombinant Superoxide Dismutase to Control Oxidative Stress in the Gastrointestinal Tract of Cyclic Heat-Stressed Pigs"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8649-6892","authenticated-orcid":false,"given":"Hieu Huu","family":"Le","sequence":"first","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"Faculty of Animal Sciences, Vietnam National University of Agriculture, Trau Quy, Gia Lam, Hanoi 12406, Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3055-6275","authenticated-orcid":false,"given":"Weicheng","family":"Zhao","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"School of Animal and Comparative Biomedical Sciences, The University of Arizona, Tucson, AZ 85719, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0219-3438","authenticated-orcid":false,"given":"John Barton","family":"Furness","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Neuroscience, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"Florey Institute of Neuroscience and Mental Health, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1857-2133","authenticated-orcid":false,"given":"Majid","family":"Shakeri","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"U.S. National Poultry Research Center, USDA-ARS, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6590-3513","authenticated-orcid":false,"given":"Kristy","family":"DiGiacomo","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9073-9946","authenticated-orcid":false,"given":"Eugeni","family":"Roura","sequence":"additional","affiliation":[{"name":"Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD 4072, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Renaudeau","sequence":"additional","affiliation":[{"name":"PEGASE, INRAE, Agrocampus Ouest, 16 Le Clos Domaine de la Prise, 35590 Saint-Gilles, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas Kurt","family":"Gabler","sequence":"additional","affiliation":[{"name":"Department of Animal Science, Iowa State University, Ames, IA 50011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9173-2730","authenticated-orcid":false,"given":"Brian Joseph","family":"Leury","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3998-1240","authenticated-orcid":false,"given":"Frank Rowland","family":"Dunshea","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"Faculty of Biological Sciences, The University of Leeds, Leeds LS2 9JT, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gene","family":"Wijffels","sequence":"additional","affiliation":[{"name":"CSIRO Agriculture and Food, St. Lucia, QLD 4067, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1899-2090","authenticated-orcid":false,"given":"Jeremy James","family":"Cottrell","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.2527\/2005.8361385x","article-title":"Effects of increasing temperatures on physiological changes in pigs at different relative humidities","volume":"83","author":"Huynh","year":"2005","journal-title":"J. Anim. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.2527\/jas.2007-0801","article-title":"Effects of temperature stress on growth performance and bacon quality in grow-finish pigs housed at two densities","volume":"86","author":"White","year":"2008","journal-title":"J. Anim. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"627","DOI":"10.4314\/sajas.v48i4.4","article-title":"Effects of air temperature on physiology and productive performance of pigs during growing and finishing phases","volume":"48","author":"Oliveira","year":"2018","journal-title":"S. Afr. J. Anim. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"H509","DOI":"10.1152\/ajpheart.2001.280.2.H509","article-title":"Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia","volume":"280","author":"Hall","year":"2001","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"249","DOI":"10.3389\/fvets.2020.00249","article-title":"Intestinal Barrier Integrity in Heat-Stressed Modern Broilers and Their Ancestor Wild Jungle Fowl","volume":"7","author":"Tabler","year":"2020","journal-title":"Front. Vet. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1113\/EP085746","article-title":"Selenium and vitamin E together improve intestinal epithelial barrier function and alleviate oxidative stress in heat-stressed pigs","volume":"101","author":"Liu","year":"2016","journal-title":"Exp. Physiol."},{"key":"ref_7","unstructured":"Dziubla, T., and Butterfield, D.A. (2016). Oxidative Stress and Biomaterials, Academic Press."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.immuni.2005.05.002","article-title":"Phagocytosis: Elegant complexity","volume":"22","author":"Stuart","year":"2005","journal-title":"Immunity"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1071\/AN20667","article-title":"Recent advances in the use of phytochemicals to manage gastrointestinal oxidative stress in poultry and pigs","volume":"62","author":"Cottrell","year":"2022","journal-title":"Anim. Prod. Sci."},{"key":"ref_10","first-page":"287","article-title":"First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid","volume":"54","author":"Ighodaro","year":"2018","journal-title":"Alex. J. Med."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Elgendey, F., Al Wakeel, R.A., Hemeda, S.A., Elshwash, A.M., Fadl, S.E., Abdelazim, A.M., Alhujaily, M., and Khalifa, O.A. (2022). Selenium and\/or vitamin E upregulate the antioxidant gene expression and parameters in broilers. BMC Vet. Res., 18.","DOI":"10.1186\/s12917-022-03411-4"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"101858","DOI":"10.1016\/j.psj.2022.101858","article-title":"Influence of dietary vitamin E and selenium supplementation on broilers subjected to heat stress, Part II: Oxidative stress, immune response, gut integrity, and intestinal microbiota","volume":"101","author":"Calik","year":"2022","journal-title":"Poult. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0021-5198(19)31433-7","article-title":"Effect of lecithinized-superoxide dismutase on the rat colitis model induced by dextran sulfate sodium","volume":"74","author":"Hori","year":"1997","journal-title":"Jpn. J. Pharmacol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1111\/j.1463-1318.2008.01487.x","article-title":"A lecithinized superoxide dismutase (PC-SOD) improves ulcerative colitis","volume":"10","author":"Suzuki","year":"2008","journal-title":"Color. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.nut.2010.02.005","article-title":"A melon pulp concentrate rich in superoxide dismutase reduces stress proteins along the gastrointestinal tract of pigs","volume":"27","author":"Lalles","year":"2011","journal-title":"Nutrition"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1017\/S1751731118001234","article-title":"The effects of superoxide dismutase-rich melon pulp concentrate on inflammation, antioxidant status and growth performance of challenged post-weaning piglets","volume":"13","author":"Ahasan","year":"2019","journal-title":"Animal"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"431","DOI":"10.3389\/fphar.2017.00431","article-title":"Postnatal Maturation of the Glomerular Filtration Rate in Conventional Growing Piglets as Potential Juvenile Animal Model for Preclinical Pharmaceutical Research","volume":"8","author":"Gasthuys","year":"2017","journal-title":"Front. Pharmacol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1007\/s00484-023-02464-w","article-title":"Comparing the responses of grain fed feedlot cattle under moderate heat load and during subsequent recovery with those of feed restricted thermoneutral counterparts: Metabolic hormones","volume":"67","author":"Wijffels","year":"2023","journal-title":"Int. J. Biometeorol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Cottrell, J.J., Furness, J.B., Wijesiriwardana, U.A., Ringuet, M., Liu, F., DiGiacomo, K., Leury, B.J., Clarke, I.J., and Dunshea, F.R. (2020). The Effect of Heat Stress on Respiratory Alkalosis and Insulin Sensitivity in Cinnamon Supplemented Pigs. Animals, 10.","DOI":"10.3390\/ani10040690"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1530\/JME-15-0161","article-title":"Proteomic changes of the porcine small intestine in response to chronic heat stress","volume":"55","author":"Cui","year":"2015","journal-title":"J. Mol. Endocrinol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Le, H.H., Shakeri, M., Suleria, H.A.R., Zhao, W., McQuade, R.M., Phillips, D.J., Vidacs, E., Furness, J.B., Dunshea, F.R., and Artuso-Ponte, V. (2020). Betaine and Isoquinoline Alkaloids Protect against Heat Stress and Colonic Permeability in Growing Pigs. Antioxidants, 9.","DOI":"10.3390\/antiox9101024"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.aninu.2021.05.012","article-title":"Heat stress-induced mucosal barrier dysfunction is potentially associated with gut microbiota dysbiosis in pigs","volume":"8","author":"Xia","year":"2022","journal-title":"Anim. Nutr."},{"key":"ref_23","first-page":"1672","article-title":"Lecithinized superoxide dismutase enhances its pharmacologic potency by increasing its cell membrane affinity","volume":"271","author":"Igarashi","year":"1994","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1898","DOI":"10.3382\/ps\/pew120","article-title":"Diet supplementation with a specific melon concentrate improves oviduct antioxidant defenses and egg characteristics in laying hens","volume":"95","author":"Carillon","year":"2016","journal-title":"Poult. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.1111\/jam.12461","article-title":"Superoxide dismutase recombinant Lactobacillus fermentum ameliorates intestinal oxidative stress through inhibiting NF-\u03baB activation in a trinitrobenzene sulphonic acid-induced colitis mouse model","volume":"116","author":"Hou","year":"2014","journal-title":"J. Appl. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1186\/s12934-015-0241-5","article-title":"Detoxifying Escherichia coli for endotoxin-free production of recombinant proteins","volume":"14","author":"Mamat","year":"2015","journal-title":"Microb. Cell Factories"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"103857","DOI":"10.1016\/j.livsci.2019.103857","article-title":"Effects of long-term heat exposure on cholesterol metabolism and immune responses in growing pigs","volume":"230","author":"Wen","year":"2019","journal-title":"Livest. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e12315","DOI":"10.14814\/phy2.12315","article-title":"Effects of heat stress on carbohydrate and lipid metabolism in growing pigs","volume":"3","author":"Johnson","year":"2015","journal-title":"Physiol. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3695","DOI":"10.3382\/ps\/pez056","article-title":"Increased fat synthesis and limited apolipoprotein B cause lipid accumulation in the liver of broiler chickens exposed to chronic heat stress","volume":"98","author":"Lu","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1884","DOI":"10.2527\/jas.2015-0084","article-title":"Heat stress in pigs is accompanied by adipose tissue-specific responses that favor increased triglyceride storage","volume":"94","author":"Qu","year":"2016","journal-title":"J. Anim. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1002\/oby.21348","article-title":"Nanoformulated copper\/zinc superoxide dismutase reduces adipose inflammation in obesity","volume":"24","author":"Adi","year":"2016","journal-title":"Obesity"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.alcohol.2018.12.005","article-title":"Effect of nanoformulated copper\/zinc superoxide dismutase on chronic ethanol-induced alterations in liver and adipose tissue","volume":"79","author":"Natarajan","year":"2019","journal-title":"Alcohol"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1186\/s12944-020-01303-w","article-title":"Triglyceride is independently correlated with insulin resistance and islet beta cell function: A study in population with different glucose and lipid metabolism states","volume":"19","author":"Ma","year":"2020","journal-title":"Lipids Health Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/S0002-9149(99)00211-8","article-title":"Hypertriglyceridemia, insulin resistance, and the metabolic syndrome","volume":"83","author":"Grundy","year":"1999","journal-title":"Am. J. Cardiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1016\/j.jsams.2018.05.003","article-title":"Renal stress and kidney injury biomarkers in response to endurance cycling in the heat with and without ibuprofen","volume":"21","author":"McDermott","year":"2018","journal-title":"J. Sci. Med. Sport"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1053\/j.ajkd.2017.01.045","article-title":"Kidney Injury and Repair Biomarkers in Marathon Runners","volume":"70","author":"Mansour","year":"2017","journal-title":"Am. J. Kidney Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/S0749-3797(99)00025-2","article-title":"Excess hospital admissions during the July 1995 heat wave in Chicago","volume":"16","author":"Semenza","year":"1999","journal-title":"Am. J. Prev. Med."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/BF00586547","article-title":"Effects of exposure to hot environments on the regional distribution of blood flow and on cardiorespiratory function in sheep","volume":"344","author":"Hales","year":"1973","journal-title":"Pfl\u00fcgers Archiv."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0306-4565(00)00017-6","article-title":"Effect of nitric oxide synthase inhibition on regional blood flow during hyperthermia","volume":"26","author":"Sils","year":"2001","journal-title":"J. Therm. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Shakeri, M., Cottrell, J.J., Wilkinson, S., Zhao, W., Le, H.H., McQuade, R., Furness, J.B., and Dunshea, F.R. (2020). Dietary Betaine Improves Intestinal Barrier Function and Ameliorates the Impact of Heat Stress in Multiple Vital Organs as Measured by Evans Blue Dye in Broiler Chickens. Animals, 10.","DOI":"10.3390\/ani10010038"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1093\/jas\/skz122.315","article-title":"PSIV-8 Effect of selenium and superoxide dismutase supplementation on heat stressed pigs","volume":"97","author":"Le","year":"2019","journal-title":"J. Anim. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/16\/2681\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:38:13Z","timestamp":1760128693000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/16\/2681"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,21]]},"references-count":41,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ani13162681"],"URL":"https:\/\/doi.org\/10.3390\/ani13162681","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,21]]}}}