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Impacts of heat stress on immune responses and oxidative stress in farm animals and nutritional strategies for amelioration

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Abstract

Heat stress is one of the greatest challenges for the global livestock industries as increased environmental temperature and humidity compromises animal production during summer leading to devastating economic consequences. Over the last 30 years, significant developments have been achieved in cooling and provision of shade and shelter to mitigate heat stress reducing some of the losses associated with heat stress in farm animals. However, the recent increase in the incidence of heat waves which are also becoming more severe and lasting longer, due to climate change, further accentuates the problem of heat stress. Economic losses associated with heat stress are both direct due to loss in production and animal life, and indirect due to poorer quality products as a result of poor animal health and welfare. Animal health is affected due to impaired immune responses and increased reactive oxygen species production and/or deficiency of antioxidants during heat stress leading to an imbalance between oxidant and antioxidants and resultant oxidative stress. Research over the last 20 years has achieved partial success in understanding the intricacies of heat stress impacts on oxidative stress and immune responses and developing interventions to ameliorate impacts of heat stress, improving immune responses and farm animal health. This paper reviews the body of knowledge on heat stress impacts on immune response in farm animals. The impacts of heat stress on both cell-mediated and humoral immune responses have been discussed identifying the shift in immune response from cell-mediated towards humoral response, thereby weakening the immune status of the animal. Both species and breed differences have been identified as influencing how heat stress impacts the immune status of farm animals. In addition, crosstalk signaling between the immune system and oxidative stress has been considered and the role of antioxidants as potential nutritional strategies to mitigate heat stress has been discussed.

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References

  • Abraham SM, Lawrence T, Kleiman A, Warden P, Medghalchi M, Tuckermann J, Saklatvala J, Clark AR (2006) Anti-inflammatory effects of dexamethasone are partly dependent on induction of dual specificity phosphatase 1. J Exp Med 203(8):1883–1889. https://doi.org/10.1084/jem.20060336

    Article  CAS  Google Scholar 

  • Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 3:28. https://doi.org/10.1186/1477-7827-3-28

    Article  CAS  Google Scholar 

  • Aggarwal A, Upadhyay R (2012) Heat stress and immune function. Heat Stress Anim Prod:113–136. https://doi.org/10.1007/978-81-322-0879-2_5

  • Ahmed BMS (2017) Elevated in utero temperature: a suppressor of fetal development ruminant fitness?. Ph.D. Dissertation. University of Florida

  • Al-Qudah KM (2011) Oxidant and antioxidant profile of hyperketonemic ewes affected by pregnancy toxemia. Vet Clin Pathol 40(1):60–65. https://doi.org/10.1111/j.1939-165X.2011.00284.x

    Article  Google Scholar 

  • Archana PR, Aleena J, Pragna P, Vidya MK, Niyas AP, Bagath M, Krishnan G, Manimaran A, Beena V, Kurien EK, Sejian V (2017) Role of heat shock proteins in livestock adaptation to heat stress. J Dairy Vet Anim Res 5(1):00127. https://doi.org/10.15406/jdvar.2017.05.00127

    Article  Google Scholar 

  • Armstrong DV (1994) Heat Stress Interaction with Shade and Cooling. J Dairy Sci 77(7):2044–2050. https://doi.org/10.3168/jds.S0022-0302(94)77149-6

    Article  CAS  Google Scholar 

  • Bagath M, Krishnan G, Devaraj C, Rashamol VP, Pragna P, Lees AM, Sejian V (2019) The impact of heat stress on the immune system in dairy cattle: a review. Res Vet Sci 126:94–102. https://doi.org/10.1016/j.rvsc.2019.08.011

    Article  CAS  Google Scholar 

  • Bartlett JR, Smith MO (2003) Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poult Sci 82(10):1580–1588. https://doi.org/10.1093/ps/82.10.1580

    Article  CAS  Google Scholar 

  • Baumgard LH, Rhoads JRP (2013) Effects of heat stress on postabsorptive metabolism and energetics. Annu Rev Anim Biosci 1(1):311–337. https://doi.org/10.1146/annurev-animal-031412-103644

    Article  CAS  Google Scholar 

  • Beede DK, Collier RJ (1986) Potential nutritional strategies for intensively managed cattle during thermal-stress. J Anim Sci 62(2):543–554

    Article  CAS  Google Scholar 

  • Bell AW (1995) Regulation of organic nutrient metabolism during transition form late pregnancy to early lactation. J Anim Sci 73(9):2804–2819

    Article  CAS  Google Scholar 

  • Berman A (2005) Estimates of heat stress relief needs for Holstein dairy cows. J Anim Sci 83(6):1377–1384

    Article  CAS  Google Scholar 

  • Berman A (2011) Invited review: Are adaptations present to support dairy cattle productivity in warm climates? J Dairy Sci 94(5):2147–2158. https://doi.org/10.3168/jds.2010-3962

    Article  CAS  Google Scholar 

  • Bernabucci U, Ronchi B, Lacetera N, Nardone A (2002) Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. J Dairy Sci 85(9):2173–2179

    Article  CAS  Google Scholar 

  • Bernabucci U, Ronchi B, Lacetera N, Nardone A (2005) Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci 88(6):2017–2026

    Article  CAS  Google Scholar 

  • Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4(7):1167–1183. https://doi.org/10.1017/s175173111000090x

    Article  CAS  Google Scholar 

  • Bernabucci U, Biffani S, Buggiotti L, Vitali A, Lacetera N, Nardone A (2014) The effects of heat stress in Italian Holstein dairy cattle. J Dairy Sci 97(1):471–486. https://doi.org/10.3168/jds.2013-6611

    Article  CAS  Google Scholar 

  • Bharati J, Dangi SS, Mishra SR, Chouhan VS, Verma V, Shankar O, Bharti MK, Paul A, Mahato DK, Rajesh G, Singh G (2017) Expression analysis of toll like receptors and interleukins in Tharparkar cattle during acclimation to heat stress exposure. J Therm Biol 65:48–56. https://doi.org/10.1016/j.jtherbio.2017.02.002

    Article  CAS  Google Scholar 

  • Blackshaw JK, Blackshaw AW (1994) Heat-stress in cattle and the effect of shade on production and behavior. Aus J Exp Agricul 34(2):285–295

    Article  Google Scholar 

  • Brozos CN, Kiossis E, Georgiadis MP, Piperelis S, Boscos C (2009) The effect of chloride ammonium, vitamin E and Se supplementation throughout the dry period on the prevention of retained fetal membranes, reproductive performance and milk yield of dairy cows. Livest Sci 124(1-3):210–215. https://doi.org/10.1016/j.livsci.2009.01.018

    Article  Google Scholar 

  • Buffington DE, Collier RJ, Canton GH (1983) Shade management-systems to reduce heat-stress for dairy-cows in hot, humid climates. T ASABE 26(6):1798–1802

    Article  Google Scholar 

  • Calif. Dep. Food Agric. Hot topics affecting California Agriculture (2006) . An update from Sec. Kawamura. Sacramento: Calif Dep Food Agric (2006). http://www.cdfa.ca.gov/exec/Public_Affairs/pdf/AGOnAg080306.pdf.

  • Caroprese M, Ciliberti MG, Annicchiarico G, Albenzio M, Muscio A, Sevi A (2014) Hypothalamic-pituitary-adrenal axis activation and immune regulation in heat-stressed sheep after supplementation with polyunsaturated fatty acids. J Dairy Sci 97(7):4247–4258. https://doi.org/10.3168/jds.2013-7696

    Article  CAS  Google Scholar 

  • Caroprese M, Ciliberti MG, De Palo P, Santillo A, Sevi A, Albenzio M (2018) Glucocorticoid effects on sheep peripheral blood mononuclear cell proliferation and cytokine production under in vitro hyperthermia. J Dairy Sci 101(9):8544–8551. https://doi.org/10.3168/jds.2018-14471

    Article  CAS  Google Scholar 

  • Castillo C, Hernandez J, Lopez-Alonso M, Miranda M, Benedito JL (2001) A different point of view of glutathione peroxidase: its relationship to the metabolic changes associate with nutritional management is Assaf ovine breed. Arch Tierzucht 44(3):305–312

    CAS  Google Scholar 

  • Castillo C, Hernandez J, Bravo A, Lopez-Alonso M, Pereira V, Benedito JL (2005) Oxidative status during late pregnancy and early lactation in dairy cows. Vet J 169(2):286–292. https://doi.org/10.1016/j.tvjl.2004.02.001

    Article  CAS  Google Scholar 

  • Castillo C, Hernandez J, Valverde I, Pereira V, Sotillo J, Alonso ML (2006) Plasma malonaldehyde (MDA) and total antioxidant status (TAS) during lactation in dairy cows. Res Vet Sci 80(2):133–139. https://doi.org/10.1016/j.rvsc.2005.06.003

    Article  CAS  Google Scholar 

  • Celi P, Di Trana A, Claps S (2010) Effects of plane of nutrition on oxidative stress in goats during the peripartum period. Vet J 184:95–99. https://doi.org/10.1016/j.tvjl.2009.01.014

    Article  CAS  Google Scholar 

  • Chauhan SS, Celi P, Fahri FT, Leury BJ, Dunshea FR (2014a) Dietary antioxidants at supranutritional doses modulate skeletal muscle heat shock protein and inflammatory gene expression in sheep exposed to heat stress. J Anim Sci 92(11):4897–4908. https://doi.org/10.2527/jas.2014-8047

    Article  CAS  Google Scholar 

  • Chauhan SS, Celi P, Leury BJ, Clarke IJ, Dunshea FR (2014b) Dietary antioxidants at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep. J Anim Sci 92(8):3364–3374. https://doi.org/10.2527/jas.2014-7714

    Article  CAS  Google Scholar 

  • Chauhan SS, Celi P, Ponnampalam EN, Leury BJ, Liu F, Dunshea FR (2014c) Antioxidant dynamics in the live animal and implications for ruminant health and product (meat/milk) quality: role of vitamin E and selenium. Anim Prod Sci 54(10):1525–1536. https://doi.org/10.1071/AN14334

    Article  CAS  Google Scholar 

  • Chauhan SS, Ponnampalam EN, Celi P, Hopkins DL, Leury BJ, Dunshea FR (2016) High dietary vitamin E and selenium improves feed intake and weight gain of finisher lambs and maintains redox homeostasis under hot conditions. Small Rumin Res 137:17–23. https://doi.org/10.1016/j.smallrumres.2016.02.011

    Article  Google Scholar 

  • Chen H, Wu Y, Zhang Y, Jin L, Luo L, Xue B, Lu C, Zhang X, Yin Z (2006) Hsp70 inhibits lipopolysaccharide-induced NF-κB activation by interacting with TRAF6 and inhibiting its ubiquitination. FEBS Lett 580(13):3145–3152. https://doi.org/10.1016/j.febslet.2006.04.066

    Article  CAS  Google Scholar 

  • Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L (2018a) Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 9(6):7204–7218. https://doi.org/10.18632/oncotarget.23208

    Article  Google Scholar 

  • Chen S, Wang J, Peng D, Li G, Chen J, Gu X (2018b) Exposure to heat-stress environment affects the physiology, circulation levels of cytokines, and microbiome in dairy cows. Sci Rep 8(1):1–11

    Google Scholar 

  • Chu GM, Song YM (2018) Growth performance, blood characteristics and immune responses of fattening pigs in different seasons. Asian J Anim Vet Adv 8(5):691–702. https://doi.org/10.3923/ajava.2013.691.702

    Article  CAS  Google Scholar 

  • Colaco CA, Bailey CR, Walker KB, Keeble J (2013) Heat shock proteins: stimulators of innate and acquired immunity. Biomed Res Int 2013:1–11. https://doi.org/10.1155/2013/461230

    Article  CAS  Google Scholar 

  • Collier RJ, Dahl GE, VanBaale MJ (2006) Major advances associated with environmental effects on dairy cattle. J Dairy Sci 89(4):1244–1253

    Article  CAS  Google Scholar 

  • Collier RJ, Collier JL, Rhoads RP, Baumgard LH (2008) Invited review: genes involved in the bovine heat stress response. J Dairy Sci 91(2):445–454. https://doi.org/10.3168/jds.2007-0540

    Article  CAS  Google Scholar 

  • Collier RJ, Eley RM, Sharma AK, Pereira RM, Buffington DE (1981) Smanagement in sub-tropical environment for milk-yield and composition in holstein and jersey cows. J Dairy Sci 64(5):844–849

    Article  Google Scholar 

  • Correa-Calderon A, Armstrong D, Ray D, DeNise S, Enns M, Howison C (2004) Thermoregulatory responses of Holstein and Brown Swiss Heat-Stressed dairy cows to two different cooling systems. Int J Biometeorol 48(3):142–148. https://doi.org/10.1007/s00484-003-0194-y

    Article  Google Scholar 

  • Cottrell JJ, Liu F, Hung AT, DiGiacomo K, Chauhan SS, Leury BJ, Furness JB, Celi P, Dunshea FR (2015) Nutritional strategies to alleviate heat stress in pigs. Anim Prod Sci 55(12):1391–1402. https://doi.org/10.1071/an15255

    Article  CAS  Google Scholar 

  • Cronje P (2005) Heat stress in livestock - the role of the gut in its aetiology and a potential role for betaine in its alleviation. Recent Adv Anim Nutrin Aust 15:107–122

    Google Scholar 

  • Cui Y, Hao Y, Li J, Bao W, Li G, Gao Y, Gu X (2016) Chronic heat stress induces immune response, oxidative stress response, and apoptosis of finishing pig liver: a proteomic approach. Int J Mol Sci 17(5):393. https://doi.org/10.3390/ijms17050393

    Article  CAS  Google Scholar 

  • Dado-Senn B, Skibiel AL, Fabris TF, Zhang Y, Dahl GE, Peñagaricano F, Laporta J (2018) RNA-Seq reveals novel genes and pathways involved in bovine mammary involution during the dry period and under environmental heat stress. Sci Rep 8(1):11096. https://doi.org/10.1038/s41598-018-29420-8

    Article  CAS  Google Scholar 

  • Dahl GE, Collier RJ (2017) Heat stress effect on immune function in dairy cattle. Cornell Nutrition Conference for Feed Manufacturers. DOI: http://ansci.cals.cornell.edu/extension-outreach/adult-extension/dairy-management/order-proceedings-resources

  • Dahl GE, Tao S, Laporta J (2020) Heat stress impacts immune status in cows across the life cycle. Front Vet Sci 7:116. https://doi.org/10.3389/fvets.2020.00116

    Article  Google Scholar 

  • Davies KJA (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50(4-5):279–289

    Article  CAS  Google Scholar 

  • Di Trana A, Celi P, Claps S, Fedele V, Rubino R (2006) The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation. Anim Sci 82(5):717–722. https://doi.org/10.1079/as200672

    Article  Google Scholar 

  • DiGiacomo K, Warner RD, Leury BJ, Gaughan JB, Dunshea FR (2014) Dietary betaine supplementation has energy- sparing effects in feedlot cattle during summer, particularly in those without access to shade. Anim Prod Sci 54(4):450–458. https://doi.org/10.1071/an13418

    Article  CAS  Google Scholar 

  • DiGiacomo K, Simpson S, Leury BJ, Dunshea FR (2016) Dietary betaine impacts the physiological responses to moderate heat conditions in a dose dependent manner in sheep. Anim 6(9):51. https://doi.org/10.3390/ani6090051

    Article  Google Scholar 

  • Do Amaral BC, Connor EE, Tao S, Hayen J, Bubolz J, Dahl GE (2009) Heat-stress abatement during the dry period: does cooling improve transition into lactation? J Dairy Sci 92(12):5988–5999. https://doi.org/10.3168/jds.2009-234

    Article  Google Scholar 

  • Drovers Cattle Netw. Heat wave kills as many as 4,000 cattle last week in Iowa. (2011). http://www.cattlenetwork.com/cattle-resources/hot-topics/Heat-wave-kills-as-many-as-4000-cattle-last-week-inIowa-126763608.html

  • Dunshea FR, Leury BJ, Fahri F, DiGiacomo K, Hung A, Chauhan S, Clarke IJ, Collier R, Little S, Baumgard L, Gaughan JB (2013) Amelioration of thermal stress impacts in dairy cows. Anim Prod Sci 53(9):965–975. https://doi.org/10.1071/an12384

    Article  Google Scholar 

  • Dunshea FR, Oluboyede K, DiGiacomo K, Leury BJ, Cottrell JJ (2019) Betaine improves milk yield in grazing dairy cows supplemented with concentrates at high temperatures. Anim 9(2):57

    Article  Google Scholar 

  • Eklund M, Bauer E, Wamatu J, Mosenthin R (2005) Potential nutritional and physiological functions of betaine in livestock. Nutr Res Rev 18(1):31–48. https://doi.org/10.1079/NRR200493

    Article  CAS  Google Scholar 

  • Elvinger F, Natzke RP, Hansen PJ (1992) Interactions of heat stress and bovine somatotropin affecting physiology and immunology of lactating cows. J Dairy Sci 75(2):449–462. https://doi.org/10.3168/jds.S0022-0302(92)77781-9

    Article  CAS  Google Scholar 

  • Finch JM, Turner RJ (1996) Effects of selenium and vitamin E on the immune responses of domestic animals. Res Vet Sci 60(2):97–106

    Article  CAS  Google Scholar 

  • Gabler NK, Frouel S, Awati A, Owusu-Asiedu A, Amerah AM, Patridge GG, Dunshea FR (2013) Betaine mitigates intestinal permeability in growing pigs induced by heat stress. In ‘Manipulating pig production XIV’. In: Pluske JR, Pluske JM (eds) . (Australasian Pig Science Association (Inc.), Melbourne, p 85

    Google Scholar 

  • Gabler NK, Koltes D, Schaumberger S, Murugesan GR, Reisinger N (2018) Diurnal heat stress reduces pig intestinal integrity and increases endotoxin translocation. Translat Anim Sci 2:1–0. https://doi.org/10.1093/tas/txx003

    Article  CAS  Google Scholar 

  • Ganesan S, Reynolds C, Hollinger K, Pearce SC, Gabler NK, Baumgard LH, Rhoads RP, Selsby JT (2018) Twelve hours of heat stress induces inflammatory signaling in porcine skeletal muscle. Am J Phys Regul Integr Comp Phys 310(11):R1288–R1296. https://doi.org/10.1152/ajpregu.00494.2015

    Article  Google Scholar 

  • Gomes da Silva R, Paranhos da Costa MJR, Silva Sobrinho AG (1992) Influence of hot environments on some blood variables of sheep. Int J Biometeorol 36(4):223–225. https://doi.org/10.1007/BF02726402

    Article  Google Scholar 

  • Gonzalez-Rivas PA, Chauhan SS, Ha M, Fegan N, Dunshea FR, Warner RD (2020) Effects of heat stress on animal physiology, metabolism, and meat quality: a review. Meat Sci 162:108025. https://doi.org/10.1016/j.meatsci.2019.108025

    Article  CAS  Google Scholar 

  • Gross WB (1992) Effect of short-term exposure of chickens to corticosterone on resistance to challenge exposure with Escherichia coli and antibody response to sheep erythrocytes. Am J Vet Res 53(3):291–293

    CAS  Google Scholar 

  • Gupta S, Gupta HK, Soni J (2005) Effect of Vitamin E and selenium supplementation on concentrations of plasma cortisol and erythrocyte lipid peroxides and the incidence of retained fetal membranes in crossbred dairy cattle. Theriogenology 64(6):1273–1286. https://doi.org/10.1016/j.theriogenology.2005.03.008

    Article  CAS  Google Scholar 

  • Hall RA, Gow NA (2013) Mannosylation in C andida albicans: role in cell wall function and immune recognition. Mol Microbial 90(6):1147–1161

    Article  CAS  Google Scholar 

  • Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150

    Article  CAS  Google Scholar 

  • Hefnawy AE, Tortora-Perez JL (2010) The importance of selenium and the effects of its deficiency in animal health. Small Rumin Res 89(2-3):185–192. https://doi.org/10.1016/j.smallrumres.2009.12.042

    Article  Google Scholar 

  • Hemsworth PH, Barnett JL, Beveridge L, Matthews LR (1995) The welfare of extensively managed dairy-cattle - A Review. Appl Anim Behav Sci 42(3):161–182

    Article  Google Scholar 

  • Hirakawa R, Nurjanah S, Furukawa K, Murai A, Kikusato M, Nochi T, Toyomizu M (2020) Heat stress causes immune abnormalities via massive damage to effect proliferation and differentiation of lymphocytes in broiler chickens. Front Vet Sci 7:46. https://doi.org/10.3389/fvets.2020.00046

    Article  Google Scholar 

  • Hogan JS, Weiss WP, Smith KL (1993) Role of vitamin-e and selenium in host-defense against mastitis. J Dairy Sci 76(9):2795–2803

    Article  CAS  Google Scholar 

  • Huo C, Xiao C, She R, Liu T, Tian J, Dong H, Tian H, Hu Y (2019) Chronic heat stress negatively affects the immune functions of both spleens and intestinal mucosal system in pigs through the inhibition of apoptosis. Microb Pathog 136:103672. https://doi.org/10.1016/j.micpath.2019.103672

    Article  CAS  Google Scholar 

  • IPCC (2014) Summary for policymakers. In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Climate change 2014: mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York

    Google Scholar 

  • Jamme I, Petit E, Divoux D, Gerbi A, Maixent JM, Nouvelot A (1995) Modulation of mouse cerebral Na+,K+-ATPase activity by oxygen free radicals. Neuroreport 7(1):333–337

    CAS  Google Scholar 

  • Joy A, Dunshea FR, Leury BJ, Clarke IJ, DiGiacomo K, Chauhan SS (2020) Resilience of small ruminants to climate change and increased environmental temperature: a review. Anim 10:867

    Article  Google Scholar 

  • Ju X-H, Yong Y-H, Xu H-J, An L-L, Xu Y (2011) Impacts of heat stress on baseline immune measures and a subset of T cells in Bama miniature pigs. Livest Sci 135(2):289–292. https://doi.org/10.1016/j.livsci.2010.07.009

    Article  Google Scholar 

  • Ju XH, Xu HJ, Yong YH, An LL, Jiao PR, Liao M (2014) Heat stress upregulation of Toll-like receptors 2/4 and acute inflammatory cytokines in peripheral blood mononuclear cell (PBMC) of Bama miniature pigs: an in vivo and in vitro study. Anim 8(9):1462–1468. https://doi.org/10.1017/S1751731114001268

    Article  CAS  Google Scholar 

  • Kapila N, Sharma A, Kishore A, Sodhi M, Tripathi PK, Mohanty AK, Mukesh M (2016) Impact of heat stress on cellular and transcriptional adaptation of mammary epithelial cells in riverine buffalo (Bubalus bubalis). PLoS One 11:e0157237. https://doi.org/10.1371/journal.pone.0157237

    Article  CAS  Google Scholar 

  • Kendall PE, Nielsen PP, Webster JR, Verkerk GA, Littlejohn RP, Matthews LR (2006) The effects of providing shade to lactating dairy cows in a temperate climate. Livest Sci 103(1–2):148–157. https://doi.org/10.1016/j.livsci.2006.02.004

    Article  Google Scholar 

  • Key N, Sneeringer S (2014) Potential effects of climate change on productivity of U.S. dairies. Am J Agric Econ 96:1136–1156

    Article  Google Scholar 

  • Khongdee S, Sripoon S, Chousawai S, Hinch G, Chaiyabutr N, Markvichitr K, Vajrabukka C (2010) The effect of modified roofing on the milk yield and reproductive performance of heat-stressed dairy cows under hot-humid conditions. Anim Sci J 81(5):606–611. https://doi.org/10.1111/j.1740-0929.2010.00771.x

    Article  CAS  Google Scholar 

  • Knapp DM, Grummer RR (1991) Response of lactating dairy cows to fat supplementation during heat stress. J Dairy Sci 74(8):2573–2579. https://doi.org/10.3168/jds.S0022-0302(91)78435-X

    Article  CAS  Google Scholar 

  • Koch F, Thom U, Albrecht E, Weikard R, Nolte W, Kuhla B, Kuehn C (2019) Heat stress directly impairs gut integrity and recruits distinct immune cell populations into the bovine intestine. Proc Natl Acad Sci U S A 116(21):10333–10338. https://doi.org/10.1073/pnas.1820130116

    Article  CAS  Google Scholar 

  • Lacetera N (2018) Impact of climate change on animal health and welfare. Anim Front 9(1):26–31. https://doi.org/10.1093/af/vfy030

    Article  Google Scholar 

  • Lacetera N, Bernabucci U, Ronchi B, Nardone A (1996) Effects of selenium and vitamin E administration during a late stage of pregnancy on colostrum and milk production in dairy cows, and on passive immunity and growth of their offspring. Am J Vet Res 57:1776–1780

    CAS  Google Scholar 

  • Lacetera N, Bernabucci U, Scalia D, Basiricò L, Morera P, Nardone A (2006) Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J Dairy Sci 89(12):4606–4612. https://doi.org/10.3168/jds.S0022-0302(06)72510-3

    Article  CAS  Google Scholar 

  • Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci 87(14):E101–E108. https://doi.org/10.2527/jas.2008-1339

    Article  CAS  Google Scholar 

  • Lean IJ, Van Saun R, DeGaris PJ (2013) Mineral and antioxidant management of transition dairy cows. Vet Clin North Am Food Anim Pract 29(2):367–36+. https://doi.org/10.1016/j.cvfa.2013.03.004

    Article  Google Scholar 

  • Liao X, Lu L, Li S, Liu S, Zhang L, Wang G, Li A, Luo X (2012) Effects of selenium source and level on growth performance, tissue selenium concentrations, antioxidation, and immune functions of heat-stressed broilers. Biol Trace Elem Res 150(1-3):158–165. https://doi.org/10.1007/s12011-012-9517-3

    Article  CAS  Google Scholar 

  • Liu F, Cottrell JJ, Furness JB, Rivera LR, Kelly FW, Wijesiriwardana U (2016) Selenium and vitamin E together improve intestinal epithelial barrier function and alleviate oxidative stress in heat-stressed pigs. Exp Physiol 101(7):801–810. https://doi.org/10.1113/EP085746

    Article  CAS  Google Scholar 

  • Lu Z, Chu M, Li Q, Jin M, Fei X, Ma L, Zhang L, Wei C (2019) Transcriptomic analysis provides novel insights into heat stress responses in sheep. Anim 9:387

    Article  Google Scholar 

  • Lykkesfeldt J, Svendsen O (2007) Oxidants and antioxidants in disease: oxidative stress in farm animals. Vet J 173(3):502–511. https://doi.org/10.1016/j.tvjl.2006.06.005

    Article  CAS  Google Scholar 

  • Madhusoodan AP, Sejian V, Afsal A, Bagath M, Krishnan G, Savitha ST, Rashamol VP, Devaraj C, Bhatta R (2019) Differential expression patterns of candidate genes pertaining to productive and immune functions in hepatic tissue of heat-stressed Salem Black goats. Biol Rhythm Res 2:1–2. https://doi.org/10.1080/09291016.2019.1607213

    Article  CAS  Google Scholar 

  • Mashaly MM, Hendricks GL 3rd, Kalama MA, Gehad AE, Abbas AO, Patterson PH (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci 83(6):889–894. https://doi.org/10.1093/ps/83.6.889.10.3390/ani9060387

    Article  CAS  Google Scholar 

  • Mates JM, Perez-Gomez C, De Castro IN (1999) Antioxidant enzymes and human diseases. Clin Biochem 32(8):595–603

    Article  CAS  Google Scholar 

  • Mayorga EJ, Ross JW, Keating AF, Rhoads RP, Baumgard LH (2020) Biology of heat stress; the nexus between intestinal hyperpermeability and swine reproduction. Theriogenology 154:73–83. https://doi.org/10.1016/j.theriogenology.2020.05.023

    Article  CAS  Google Scholar 

  • McDaniel CD, Hood JE, Parker HM (2004) An attempt at alleviating heat stress infertility in male broiler breeder chickens with dietary ascorbic acid. Int J Poult Sci 3(9):593–602. https://doi.org/10.3923/ijps.2004.593.602

    Article  Google Scholar 

  • McDowell LR, Williams SN, Hidiroglou N, Njeru CA, Hill GM, Ochoa L, Wilkinson NS (1996) Vitamin E supplementation for the ruminant. Anim Feed Sci Technol 60(3-4):273–296

    Article  CAS  Google Scholar 

  • Miller JK, Brzezinska-Slebodzinska E, Madsen FC (1993) Oxidative stress, antioxidants, and animal function. J Dairy Sci 76(9):2812–2823. https://doi.org/10.3168/jds.S0022-0302(93)77620-1

    Article  CAS  Google Scholar 

  • Mishra A, Hooda O, Singh G, Meur S (2011) Influence of induced heat stress on HSP70 in buffalo lymphocytes. J Anim Physiol Anim Nutr 95(4):540–544

    Article  CAS  Google Scholar 

  • Mitchell JB, Russo A (1983) Thiols, thiol depletion, and thermosensitivity. Radiat Res 95(3):471–485

    Article  CAS  Google Scholar 

  • MLA (Meat and Livestock Australia). Animal health survey of the Australian feedlot industry. (2010). file:///C:/Users/LENOVO/Downloads/P.PSH.0547_Final_Report.pdf

  • Moeini M, Karami H, Mikaeili E (2009) Effect of selenium and vitamin E supplementation during the late pregnancy on reproductive indices and milk production in heifers. Anim Reprod Sci 114(1-3):109–114

    Article  CAS  Google Scholar 

  • Morgante M, Beghelli D, Pauselli M, Dall’Ara P, Capuccella M, Ranucci S (1999) Effect of administration of vitamin E and selenium during the dry period on mammary health and milk cell counts in dairy ewes. J Dairy Sci 82(3):623–631

    Article  CAS  Google Scholar 

  • Morrow-Tesch JL, McGlone JJ, Salak-Johnson JL (1994) Heat and social stress effects on pig immune measures. J Anim Sci 72(10):2599–2609

    Article  CAS  Google Scholar 

  • Mujahid A, Yoshiki Y, Akiba Y, Toyomizu M (2005) Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poult Sci 84(2):307–314

    Article  CAS  Google Scholar 

  • Mukherjee J, Pandita S, Huozha R, Ashutosh M (2011) In vitro immune competence of buffaloes (Bubalus bubalis) of different production potential: effect of heat stress and cortisol. Vet Med Inter DOI 2011:1–5. https://doi.org/10.4061/2011/860252

    Article  Google Scholar 

  • Niu Z, Liu F, Yan Q, Li L (2009a) Effects of different levels of selenium on growth performance and immunocompetence of broilers under heat stress. Arch Anim Nutr 63(1):56–65

    Article  CAS  Google Scholar 

  • Niu Z, Liu F, Yan Q, Li W (2009b) Effects of different levels of vitamin E on growth performance and immune responses of broilers under heat stress. Poult Sci 88(10):2101–2107

    Article  CAS  Google Scholar 

  • Ohtsu H, Yamazaki M, Abe H, Murakami H, Toyomizu M (2015) Heat stress modulates cytokine gene expression in the spleen of broiler chickens. J Poult Sci 52:282–287

    Article  CAS  Google Scholar 

  • Osei-Amponsah R, Chauhan SS, Leury BJ, Cheng L, Cullen B, Clarke IJ, Dunshea FR (2019) Genetic selection for thermotolerance in ruminants. Animals (Basel) 9(11):948

    Article  Google Scholar 

  • Paul A, Dangi S, Gupta M, Singh J, Thakur N, Naskar S, Nanda P, Mohanty N, Das A, Bandopadhayay S (2015) Expression of TLR genes in Black Bengal goat (Capra hircus) during different seasons. Small Rumin Res 124:17–23

    Article  Google Scholar 

  • Pavlata L, Prasek J, Filipek J, Pechova A (2004) Influence of parenteral administration of selenium and vitamin E during pregnancy on selected metabolic parameters and colostrum quality in dairy cows at parturition. Vet Med 49:149–155

    Article  CAS  Google Scholar 

  • Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, Rhoads RP, Baumgard LH, Gabler NK (2013) Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8(8):e70215

    Article  CAS  Google Scholar 

  • Politis I, Hidiroglou M, Batra T, Gilmore J, Gorewit R, Scherf H (1995) Effects of vitamin E on immune function of dairy cows. Am J Vet Res 56(2):179–184

    CAS  Google Scholar 

  • Quinteiro-Filho WM, Calefi AS, Cruz D, Aloia TPA, Zager A, Astolfi-Ferreira CS, Ferreira JP, Sharif S, Palermo-Neto J (2017) Heat stress decreases expression of the cytokines, avian β-defensins 4 and 6 and Toll-like receptor 2 in broiler chickens infected with Salmonella Enteritidis. Vet Immunol Immunopathol 186:19–28

    Article  CAS  Google Scholar 

  • Rashamol V, Sejian V, Bagath M, Krishnan G, Beena V, Bhatta R (2019) Effect of heat stress on the quantitative expression patterns of different cytokine genes in Malabari goats. Int J Biometeorol 63(8):1005–1013

    Article  CAS  Google Scholar 

  • Renaudeau D, Collin A, Yahav S, De Basilio V, Gourdine J, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Anim 6(5):707–728

    Article  CAS  Google Scholar 

  • Rezapour A, Taghinejad-Roudbaneh M (2011) Effects of food restriction on oxidative stress indices in Ghezel ewes. J Anim Vet Adv 10(8):980–986

    Article  CAS  Google Scholar 

  • Rhoads M, Rhoads R, VanBaale M, Collier RJ, Sanders S, Weber WJ, Crooker BA, Baumgard L (2009) Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin. J Dairy Sci 92(5):1986–1997

    Article  CAS  Google Scholar 

  • Rhoads RP, Baumgard LH, Suagee JK, Sanders SR (2013) Nutritional interventions to alleviate the negative consequences of heat stress. Adv Nutr 4(3):267–276

    Article  CAS  Google Scholar 

  • Rimbach G, Minihane AM, Majewicz J, Fischer A, Pallauf J, Virgli F, Weinberg PD (2002) Regulation of cell signalling by vitamin E. Proc Nutr Soc 61(4):415–425

    Article  CAS  Google Scholar 

  • Rooke J, Robinson J, Arthur J (2004) Effects of vitamin E and selenium on the performance and immune status of ewes and lambs. J Agric Sci 142(3):253–262

    Article  CAS  Google Scholar 

  • Rostagno MH (2020) Effects of heat stress on the gut health of poultry. J Anim Sci 98(4):skaa090

    Article  Google Scholar 

  • Rotruck JT, Pope AL, Ganther HE, Swanson A, Hafeman DG, Hoekstra W (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179(4073):588–590

    Article  CAS  Google Scholar 

  • Safa S, Kargar S, Moghaddam GA, Ciliberti MG, Caroprese M (2019) Heat stress abatement during the postpartum period: effects on whole lactation milk yield, indicators of metabolic status, inflammatory cytokines, and biomarkers of the oxidative stress. J Anim Sci 97(1):122–132

    Article  Google Scholar 

  • Sahin N, Onderci M, Sahin K, Kucuk O (2008) Supplementation with organic or inorganic selenium in heat-distressed quail. Biol Trace Elem Res 122(3):229–237

    Article  CAS  Google Scholar 

  • Sathya A, Prabhakar S, Sangha S, Ghuman S (2007) Vitamin E and selenium supplementation reduces plasma cortisol and oxidative stress in dystocia-affected buffaloes. Vet Res Commun 31(7):809–818

    Article  CAS  Google Scholar 

  • Savitha S, Girish Kumar V, Amitha J, Sejian V, Bagath M, Krishnan G, Devaraj C (2019) Bhatta R (2019) Comparative assessment of thermo-tolerance between indigenous Osmanabadi and Salem black goat breeds based on expression patterns of different intracellular toll-like receptor genes during exposure to summer heat stress. Biol Rhythm Res 22:1–9. https://doi.org/10.1080/09291016.2019.1592350

    Article  CAS  Google Scholar 

  • Schütz K, Rogers A, Cox N, Webster J, Tucker C (2011) Dairy cattle prefer shade over sprinklers: Effects on behavior and physiology. J Dairy Sci 94(1):273–283

    Article  CAS  Google Scholar 

  • Schütz K, Cox N, Tucker C (2014) A field study of the behavioral and physiological effects of varying amounts of shade for lactating cows at pasture. J Dairy Sci 97(6):3599–3605

    Article  CAS  Google Scholar 

  • Shah AM, Ma J, Wang Z, Zou H, Hu R, Peng Q (2020) Betaine supplementation improves the production performance, rumen fermentation, and antioxidant profile of dairy cows in heat stress. Anim 10(4):634

    Article  Google Scholar 

  • Shakeri M, Cottrell JJ, Wilkinson S, Le HH, Suleria HA, Warner RD, Dunshea FR (2019) Growth performance and characterization of meat quality of broiler chickens supplemented with betaine and antioxidants under cyclic heat stress. Antioxidants 8(9):336

    Article  CAS  Google Scholar 

  • Shakeri M, Cottrell JJ, Wilkinson S, Zhao W, Le HH, McQuade R, Furness JB, Dunshea FR (2020a) 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. Anim 10(1):38

    Article  Google Scholar 

  • Sharma N, Singh N, Singh O, Pandey V, Verma P (2011) Oxidative stress and antioxidant status during transition period in dairy cows. Asian-Australas J Anim Sci 24(4):479–484

    Article  CAS  Google Scholar 

  • Sheikh AA, Aggarwal A, Aarif O (2016) Effect of in vitro zinc supplementation on HSPs expression and Interleukin 10 production in heat treated peripheral blood mononuclear cells of transition Sahiwal and Karan Fries cows. J Therm Biol 56:68–76

    Article  CAS  Google Scholar 

  • Sivakumar AVN, Singh G, Varshney VP (2010) Antioxidants Supplementation on Acid Base Balance during Heat Stress in Goats. Asian-Australasian J Anim Sci 23(11):1462–1468

    Article  CAS  Google Scholar 

  • Smith KL, Hogan J, Weiss W (1997) Dietary vitamin E and selenium affect mastitis and milk quality. J Anim Sci 75(6):1659–1665

    Article  CAS  Google Scholar 

  • Smith TR, Chapa A, Willard S, Herndon C, Williams RJ, Crouch J, Riley T, Pogue D (2006) Evaporative tunnel cooling of dairy cows in the southeast. II: Impact on lactation performance. J Dairy Sci 89(10):3915–3923

    Article  CAS  Google Scholar 

  • Sophia I, Sejian V, Bagath M, Bhatta R (2016) Quantitative expression of hepatic toll-like receptors 1–10 mRNA in Osmanabadi goats during different climatic stresses. Small Rumin Res 141:11–16

    Article  Google Scholar 

  • Sophia I, Sejian V, Bagath M, Bhatta R (2017) Influence of different environmental stresses on various spleen toll like receptor genes expression in Osmanabadi goats. Asian J Biol Sci 10(1):9–16. https://doi.org/10.3923/ajbs.2017.9.16

    Article  Google Scholar 

  • Sordillo LM, Aitken SL (2009) Impact of oxidative stress on the health and immune function of dairy cattle. Vet Immunol Immunopathol 128(1-3):104–109

    Article  CAS  Google Scholar 

  • Sordillo L, Mavangira V (2014) The nexus between nutrient metabolism, oxidative stress and inflammation in transition cows. Anim Prod Sci 54(9):1204–1214

    Article  Google Scholar 

  • Sordillo JE, Alwis UK, Hoffman E, Gold DR, Milton DK (2011) Home characteristics as predictors of bacterial and fungal microbial biomarkers in house dust. Environ Health Perspect 119(2):189–195

    Article  CAS  Google Scholar 

  • Spears JW, Weiss WP (2008) Role of antioxidants and trace elements in health and immunity of transition dairy cows. Vet J 176(1):70–76

    Article  CAS  Google Scholar 

  • Srikanth K, Kwon A, Lee E, Chung H (2017) Characterization of genes and pathways that respond to heat stress in Holstein calves through transcriptome analysis. Cell Stress Chaperones 22(1):29–42

    Article  CAS  Google Scholar 

  • Steele M (2016) Does heat stress affect immune function in dairy cows? Vet Evidence 1(3). https://doi.org/10.18849/ve.v1i3.39

  • St-Pierre N, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci 86:E52–E77

    Article  Google Scholar 

  • Sun Y, Liu J, Ye G, Gan F, Hamid M, Liao S, Huang K (2018) Protective effects of zymosan on heat stress-induced immunosuppression and apoptosis in dairy cows and peripheral blood mononuclear cells. Cell Stress Chaperones 23(5):1069–1078

    Article  CAS  Google Scholar 

  • Tao S, Connor E, Bubolz J, Thompson I, Do Amaral B, Hayen M, Dahl G (2013) Effect of heat stress during the dry period on gene expression in mammary tissue and peripheral blood mononuclear cells. J Dairy Sci 96(1):378–383

    Article  CAS  Google Scholar 

  • Thaxton P, Sadler C, Glick B (1968) Immune response of chickens following heat exposure or injections with ACTH. Poult Sci 47(1):264–266

    Article  CAS  Google Scholar 

  • Thompson I, Tao S, Monteiro A, Jeong K, Dahl G (2014) Effect of cooling during the dry period on immune response after Streptococcus uberis intramammary infection challenge of dairy cows. J Dairy Sci 97(12):7426–7436

    Article  CAS  Google Scholar 

  • Tirawattanawanich C, Chantakru S, Nimitsantiwong W, Tongyai S (2011) The effects of tropical environmental conditions on the stress and immune responses of commercial broilers, Thai indigenous chickens, and crossbred chickens. J Appl Poult Res 20(4):409–420

    Article  Google Scholar 

  • Tirumurugaan K, Dhanasekaran S, Raj GD, Raja A, Kumanan K, Ramaswamy V (2010) Differential expression of toll-like receptor mRNA in selected tissues of goat (Capra hircus). Vet Immunol Immunopathol 133(2-4):296–301

    Article  CAS  Google Scholar 

  • Tucker CB, Rogers AR, Schutz KE (2008) Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasturebased system. Appl Anim Behav Sci 109(2–4):141–154. https://doi.org/10.1016/j.applanim.2007.03.015

    Article  Google Scholar 

  • Vandana G, Bagath M, Sejian V, Krishnan G, Beena V, Bhatta R (2019) Summer season induced heat stress impact on the expression patterns of different toll-like receptor genes in Malabari goats. Biol Rhythm Res 50(3):466–482

    Article  CAS  Google Scholar 

  • Waller KP, Sandgren CH, Emanuelson U, Jensen SK (2007) Supplementation of RRR-α-tocopheryl acetate to periparturient dairy cows in commercial herds with high mastitis incidence. J Dairy Sci 90(8):3640–3646

    Article  CAS  Google Scholar 

  • Watson RR (1998) Vitamin E and the immune system. In: Peter JD (ed) Encyclopedia of ommunology, 2nd edn. Elsevier, Oxford, pp 2500–2501

    Chapter  Google Scholar 

  • Williams CM (2000) Dietary fatty acids and human health. Ann Zootech 49:165–180

    Article  CAS  Google Scholar 

  • Wojtas K, Cwynar P, Kołacz R (2014) Effect of thermal stress on physiological and blood parameters in merino sheep. Bull Vet Inst Pulawy 58(2):283–288

    Article  Google Scholar 

  • Zhang F, Weng X, Wang J, Zhou D, Zhang W, Zhai C, Hou Y, Zhu Y (2014) Effects of temperature–humidity index and chromium supplementation on antioxidant capacity, heat shock protein 72, and cytokine responses of lactating cows. J Anim Sci 92(7):3026–3034

    Article  CAS  Google Scholar 

  • Zhang M, Dunshea FR, Warner RD, DiGiacomo K, Osei-Amponsah R, Chauhan SS (2020) Impacts of heat stress on meat quality and strategies for amelioration: a review. Int J Biometeorol 64:1613–1628. https://doi.org/10.1007/s00484-020-01929-6

    Article  Google Scholar 

  • Zininga T, Ramatsui L, Shonhai A (2018) Heat shock proteins as immunomodulants. Molecules 23(11):2846

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Agriculture and Food, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, VIC, 3010, Australia

    Surinder S. Chauhan & Frank R. Dunshea

  2. ICAR National Institute of Animal Nutrition and Physiology, Bangalore, India

    V. P. Rashamol, M. Bagath & Veerasamy Sejian

  3. Faculty of Biological Sciences, The University of Leeds, Leeds, LS2 9JT, UK

    Frank R. Dunshea

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  1. Surinder S. Chauhan
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  2. V. P. Rashamol
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  3. M. Bagath
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  5. Frank R. Dunshea
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All authors SSC, VPR, VS, MB, and FRD have contributed equally and made substantial, direct, and intellectual contributions to the work, and approved it for publication.

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Chauhan, S.S., Rashamol, V.P., Bagath, M. et al. Impacts of heat stress on immune responses and oxidative stress in farm animals and nutritional strategies for amelioration. Int J Biometeorol 65, 1231–1244 (2021). https://doi.org/10.1007/s00484-021-02083-3

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