Climate Change Impact on Immune Response in Sheep

  • Mariangela CaropreseEmail author
  • Maria Giovanna Ciliberti
  • Marzia Albenzio
  • Agostino Sevi


Sheep are considered one of the most resistant species with respect to climate change and high environmental temperatures. Most studies have focused on the effects of heat stress on the physiological mechanisms of adaptation in dairy cows; few studies have dealt with dairy sheep physiology and, above all, with sheep immunological responses. This chapter will focus on the complex network of mechanisms activated by heat stress as affecting immune responses in sheep. In particular, heat stress will be discussed as an attempt to animals’ homeostasis, thus affecting immune system and inducing activation of inflammatory processes. In particular, it will present a synopsis of the knowledge of the sheep immune system, and the changes induced by heat stress on both innate and adaptive immunity. Recent data suggesting a role of heat stress on perturbation of oxidative balance and the consequent effects on the immune system will be discussed. Finally, a discussion on the effects of heat stress on sheep mammary immunity will be presented.


Sheep Heat stress Immune responses Heat shock proteins Oxidative stress 


  1. Albenzio M, Caroprese M, Santillo A, Marino R, Taibi L, Sevi A (2004) Effects of somatic cell count and stage of lactation on the plasmin activity and cheese-making properties of ewe milk. J Dairy Sci 87:533–542PubMedCrossRefGoogle Scholar
  2. Albenzio M, Santillo A, Caroprese M, Marino R, Centoducati P, Sevi A (2005) Effect of different ventilation regimes on ewe milk and canestrato pugliese cheese quality in summer. J Dairy Res 72:447–455PubMedCrossRefGoogle Scholar
  3. Albenzio A, Santillo A, Caroprese M, Ruggieri D, Ciliberti M, Sevi A (2012) Immune competence of the mammary gland as affected by somatic cell and pathogenic bacteria in ewes with subclinical mastitis. J Dairy Sci 95:3877–3887PubMedCrossRefGoogle Scholar
  4. Albenzio M, Santillo A, Caroprese M, Ciliberti MG, Marino R, Sevi A (2016) Effect of stage of lactation on the immune competence of goat mammary gland. J Dairy Sci 99:3889–3895PubMedCrossRefGoogle Scholar
  5. Alhidary IA, Abdelrahman MM (2016) Effect of narginin supplementation on productive performance, antioxidant status and immune response in heat-stressed lambs. Small Rumin Res 138:31–36CrossRefGoogle Scholar
  6. Angelini DJ, Hasday JD, Goldblum SE, Bannerman DD (2005) Tumor necrosis factor-α-mediated pulmonary endothelial barrier dysfunction. Curr Respir Med Rev 1:233–246CrossRefGoogle Scholar
  7. Asadullah K, Sterry W, Volk HD (2003) Interleukin-10 therapy-review of a new approach. Pharmacol Rev 55:241–269PubMedCrossRefGoogle Scholar
  8. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E (2004) Involvement of reactive oxygen species in toll like receptor 4-dependent activation of NF-𝜅𝜅B. J Immunol 172:2522–2529PubMedCrossRefGoogle Scholar
  9. Baggiolini M, Clark-Lewis I (1992) Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 307:97–101PubMedCrossRefGoogle Scholar
  10. Bannerman DD (2009) Pathogen-dependent induction of cytokines and other soluble inflammatory mediators during intramammary infection of dairy cows. J Anim Sci 87:10–25PubMedCrossRefGoogle Scholar
  11. Barksby HE, Lea SR, Preshaw PM, Taylor JJ (2007) The expanding family of interleukin-1 cytokines and their role in destructive inflammatory disorders. Clin Exp Immunol 149:217–225PubMedPubMedCentralCrossRefGoogle Scholar
  12. Beckman KB, Ames BN (1998) The free radical theory of ageing matures. Physiol Rev 78:547–581PubMedGoogle Scholar
  13. Bernabucci U (2012) Impact of hot environment on nutrient requirements. In: Collier RJ, Collier JL (eds) Environmental physiology of livestock. Wiley, Ames, pp 101–128CrossRefGoogle Scholar
  14. Bernabucci U, Lacetera N, Danieli PP, Bani P, Nardone A, Ronchi B (2009) Influence of different periods of exposure to hot environment on rumen function and diet digestibility in sheep. Int J Biometeorol 53:387–395PubMedCrossRefGoogle Scholar
  15. Bertoni G, Bernabucci U, Balestra F (1991) Heat-stress effects on some blood parameters of sheep. In: Ronchi B (ed) Animal husbandry in warm climates, vol 55. Pudoc, Wageningen, pp 98–102Google Scholar
  16. Biffl WL, Moore EE, Moore FA, Peterson VM (1996) Interleukin-6 in the injured patient. Marker of injury or mediator of inflammation? Ann Surg 224:647–664PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bradford BJ (2012) Nutrition and immunity. In: Proceedings of the 21st tri-state dairy nutrition conference, Fort Wayne, IN, 24–25 April 2012, pp 5–15Google Scholar
  18. Brouckaert P, Fiers W (1996) Tumor necrosis factor and the systemic inflammatory response syndrome. Curr Top Microbiol Immunol 216:167–187PubMedGoogle Scholar
  19. Burvenich C, Detilleux J, Paape MJ, Massart-Leën AM (2000) Physiological and genetic factors that influence the cow resistance to mastitis, especially during early lactation. In: Zecconi A (ed) Proceedings of the international symposium on immunology of ruminant mammary gland, Stresa, Italy, pp 9–20Google Scholar
  20. Caroprese M, Albenzio M, Annicchiarico G, Sevi A (2006) Changes occurring in immune responsiveness of single- and twin bearing Comisana ewes during the transition period. J Dairy Sci 89:562–568PubMedCrossRefGoogle Scholar
  21. Caroprese M, Albenzio M, Marzano A, Schena L, Annicchiarico G, Sevi A (2010) Relationship between cortisol response to stress and behavior, immune profile, and production performance of dairy ewes. J Dairy Sci 93:2395–2403PubMedCrossRefGoogle Scholar
  22. Caroprese M, Albenzio M, Bruno A, Fedele V, Santillo A, Sevi A (2011) Effect of solar radiation and flaxseed supplementation on milk production and fatty acid profile of lactating ewes under high ambient temperature. J Dairy Sci 94:3856–3867PubMedCrossRefGoogle Scholar
  23. Caroprese M, Albenzio M, Bruno A, Annichiarico G, Marino R, Sevi A (2012) Effects of shade and flaxseed supplementation on welfare of lactating ewes under high ambient temperatures. Small Rumin Res 102:177–185CrossRefGoogle Scholar
  24. 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 97:4247–4258PubMedCrossRefGoogle Scholar
  25. Caroprese M, Ciliberti MG, Albenzio M, Annicchiarico G, Sevi A (2015) Dietary polyunsaturated fatty acids from flaxseed affect immune responses of dairy sheep around parturition. Vet Immunol Immunopathol 168:56–60PubMedCrossRefGoogle Scholar
  26. Celi P (2010) The role of oxidative stress in small ruminants’ health and production. Rev Bras Zootec 39:348–363CrossRefGoogle Scholar
  27. Celi P, Merlo M, Da Dalt L, Stefani A, Barbato O, Gabai G (2011) Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows. Reprod Fertil Dev 23:527–533PubMedCrossRefGoogle Scholar
  28. Chauahan SS, Celi P, Leury BJ, Clarke IJ, Dunshea FR (2014) Dietary antioxidant at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep. J Anim Sci 92:3364–3374CrossRefGoogle Scholar
  29. Chung DR, Kasper DL, Panzo RJ, Chitnis T, Grusby MJ, Sayegh MH, Tzianabos AO (2003) CD4+ T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J Immunol 170:1958–1963PubMedCrossRefGoogle Scholar
  30. Ciliberti MG, Albenzio M, Annicchiarico G, Marino R, Santillo A, Sevi A, Caroprese M (2016) Role of different sources of dietary PUFA supplementation on sheep welfare under high ambient temperature. Small Rumin Res 135:32–38CrossRefGoogle Scholar
  31. Collier RJ, Collier JL, Rhoads RP, Baumgard LH (2008) Invited review: genes involved in the Bovine heat stress response. J Dairy Sci 91:445–454PubMedCrossRefGoogle Scholar
  32. Conti P, Kempuraj D, Kandere K, Di Gioacchino M, Barbacane RC, Castellani ML, Felaco M, Boucher W, Letourneau R, Theoharides TC (2003) IL-10, an inflammatory/inhibitory cytokine, but not always. Immunol Lett 86:123–129PubMedCrossRefGoogle Scholar
  33. Cox SS, Speaker KJ, Beninson LA, Craig WC, Paton MM, Fleshner M (2014) Adrenergic and glucocorticoid modulation of the sterile inflammatory response. Brain Behav Immun 36:183–192PubMedCrossRefGoogle Scholar
  34. D’Rourke O (2009) Nutrition and udder health in dairy cows: a review. Ir Vet J 62:S15–S20CrossRefGoogle Scholar
  35. De Waal Malefyt R, Figdor C, Huijbens R, Mohan-Peterson S, Bennett B, Culpepper J, Dang W, Zurawski G, de Vries J (1993) Effects of IL-13 on phenotype, cytokine production and cytotoxic function of human monocytes. J Immunol 151:6370–6381PubMedGoogle Scholar
  36. Doherty M, Kastelein K, Menon S, Andrade S, Coffman R (1993) Modulation of murine macrophage function by IL-13. J Immunol 151:7151–7160PubMedGoogle Scholar
  37. Elenkov IJ, Chrousos GP (1999) Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab 10:359–368PubMedCrossRefGoogle Scholar
  38. Elhmouzi-Younes J, Boysen P, Pende D, Storset AK, Le Vern Y, Laurent F, Drouet F (2010) Ovine CD16+/CD14 blood lymphocytes present all the major characteristics of natural killer cells. Vet Res 41:04–15CrossRefGoogle Scholar
  39. Ellis TN, Beaman BL (2004) Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology 112:2–12PubMedPubMedCentralCrossRefGoogle Scholar
  40. Entrican G, Wattegedera SR, Griffiths DJ (2015) Exploiting ovine immunology to improve the relevance of biomedical models. Mol Immunol 66:68–77PubMedPubMedCentralCrossRefGoogle Scholar
  41. Estes DM, Hirano A, Heussler VT, Dobbelaere DAE, Brown WC (1995) Expression and biological activities of bovine interleukin-4: effects of recombinant bovine interleukin-4 on T cell proliferation and B cell differentiation and proliferation in vitro. Cell Immunol 163:268–279PubMedCrossRefGoogle Scholar
  42. Fajardo-Lira CE, Nielsen SS (1998) Effect of psychrotrophic microorganisms on the plasmin system in milk. J Dairy Sci 81:901–908PubMedCrossRefGoogle Scholar
  43. Fleshner M (2013) Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav Immun 27:1–7PubMedCrossRefGoogle Scholar
  44. Gately MK, Renzetti LM, Magram J, Stern AS, Adorini L, Gubler U, Presky DH (1998) The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 16:495–521PubMedCrossRefGoogle Scholar
  45. Gloire G, Legrand-Poels S, Piette J (2006) NF-𝜅B activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 72:1493–1505PubMedCrossRefGoogle Scholar
  46. Gouwy M, Struyf S, Proost P, Van Damme J (2005) Synergy in cytokine and chemokine networks amplifies the inflammatory response. Cytokine Growth Factor Rev 16:561–580PubMedCrossRefGoogle Scholar
  47. Guerriero V Jr, Raynes DA (1990) Synthesis of heat stress proteins in lymphocytes from livestock. J Anim Sci 68:2779–2783PubMedCrossRefGoogle Scholar
  48. Gyorffy EJ, Glogauer M, Kennedy L, Reynolds JD (1992) T-cell receptor-γδ association with lymphocyte populations in sheep intestinal mucosa. Immunology 77:25–30PubMedPubMedCentralGoogle Scholar
  49. Habeeb AAM, Marai IFM, Kamal TH (1992) Heat stress. In: Phillips C, Piggins D (eds) Farm animals and environment. CAB International, Wallingford, pp 27–47Google Scholar
  50. Hall DJ, Brownlee C, Stiles CD (1989) Interleukin-1 is a potent regulator of JE and KC gene expression in quiescent BALB/c fibroblasts. J Cell Physiol 141:154–159PubMedCrossRefGoogle Scholar
  51. Happel KI, Dubin PJ, Zheng M, Ghilardi N, Lockhart C, Quinton LJ, Odden AR, Shellito JE, Bagby GJ, Nelson S, Kolls JK (2005) Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J Exp Med 202:761–769PubMedPubMedCentralCrossRefGoogle Scholar
  52. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K (1994) Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56:559–564PubMedGoogle Scholar
  53. Hein WR, Griebel PJ (2003) A road less travelled: large animal models in immunological research. Nat Rev Immunol 3:79–84PubMedCrossRefGoogle Scholar
  54. Hein WR, Mackay CR (1991) Prominence of γδ T cells in the ruminant immune system. Immunol Today 12:30–34PubMedCrossRefGoogle Scholar
  55. Hein WR, Peterhans E (1998) Handbook of vertebrate immunology. Pastoret PP, Griebel P, Bazin H, Govaerts A (eds). Academic, San Diego, p 502Google Scholar
  56. Huang W, Na L, Fidel PL, Schwarzenberger P (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190:624–631PubMedCrossRefGoogle Scholar
  57. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5:987–995PubMedCrossRefGoogle Scholar
  58. Jabrane-Ferrat N, Siewiera J (2014) The up side of decidual natural killer cells: new developments in immunology of pregnancy. Immunology 141:490–497PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kehrli E Jr, Lee AH, Ackermann MR (2000) Acute phase response of the bovine mammary gland to Escherichia coli. In: Zecconi A (ed) Proceedings of the international symposium on immunology of ruminant mammary gland, Stresa, Italy, pp 21–29Google Scholar
  60. Keller ET, Wanagat J, Ershler WB (1996) Molecular and cellular biology of interleukin-6 and its receptor. Front Biosci 1:d340–d357PubMedCrossRefGoogle Scholar
  61. King IL, Mohrs M (2009) IL-4–producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J Exp Med 206:1001–1007PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kobayashi Y (2008) The role of chemokines in neutrophil biology. Front Biosci 13:2400–2407PubMedCrossRefGoogle Scholar
  63. Lacetera N, Bernabucci U, Scalia D, Ronchi B, Kuzminsky G, Nardone A (2005) Lymphocyte functions in dairy cows in hot environment. Int J Biometeorol 50:105–110PubMedCrossRefGoogle Scholar
  64. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, Cua DJ (2004) IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 202:96–105PubMedCrossRefGoogle Scholar
  65. Lund BT, Evans CW, Davis WC, McConnell I, Bujdoso R (1993) Expression of T19 (WC1) molecules by ovine lymphocytes. Vet Immunol Immunopathol 39:145–153PubMedCrossRefGoogle Scholar
  66. Makay CR, Beya M-F, Matzinger P (1989) γ/δ T cells express a unique surface molecule appearing late during thymic development. Eur J Immunol 19:1477–1483CrossRefGoogle Scholar
  67. Marai IFM, El-Darawany AA, Fadiel A, Abdel-Hafez MAM (2007) Physiological traits as affected by heat stress in sheep – a review. Small Rumin Res 71:1–12CrossRefGoogle Scholar
  68. Martin CA, Kurkowski DL, Valentino AM, Schwarz FS (2009) Increased intracellular, cell surface, and secreted inducible heat shock protein 70 responses are triggered during the monocyte to dendritic cell (DC) transition by cytokines independently of heat stress and infection and may positively regulate DC growth. J Immunol 183:388–399PubMedPubMedCentralCrossRefGoogle Scholar
  69. Matsukawa A, Hogaboam CM, Lukacs NW, Kunkel SL (2000) Chemokines and innate immunity. Rev Immunogenet 2:339–358PubMedGoogle Scholar
  70. Matteri RL, Carroll JA, Dyer CJ (2000) Neuroendocrine responses to stress. In: Sejrsen K, Hvelplund T, Nielsen MO (eds) The biology of animal stress. CABI-Publishing, Wallingford, pp 43–76Google Scholar
  71. McKenzie GJ, Emson CL, Bell SE, Anderson S, Fallon P, Zurawski G, Murray R, McKenzie ANJ (1998) Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9:423–432PubMedCrossRefGoogle Scholar
  72. Miller JK, Brzezinskaslebodzinska E, Madsen FC (1993) Oxidative stress, antioxidants, and animal function. J Dairy Sci 76:2812–2823PubMedCrossRefGoogle Scholar
  73. Miossec P, Kolls JK (2012) Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov 11:763–776PubMedCrossRefGoogle Scholar
  74. Mocellin S, Marincola F, Rossi CR, Nitti D, Lise M (2004) The multifaceted relationship between IL-10 and adaptive immunity: putting together the pieces of a puzzle. Cytokine Growth Factor Rev 15:61–76PubMedCrossRefGoogle Scholar
  75. Moore KW, de Waal MR, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765PubMedCrossRefGoogle Scholar
  76. Mujahid A, Yoshiki Y, Akiba Y, Toyomizu M (2005) Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poult Sci 84:307–314PubMedCrossRefGoogle Scholar
  77. Mukaida N (2003) Pathophysiological roles of interleukin-8/CXCL8 in pulmonary diseases. Am J Phys Lung Cell Mol Phys 284:L566–L577Google Scholar
  78. Murzenok PP, Netukova NI, Zhytkevitch TI (1997) Ultrastructure and functional state of rabbit lymphoid cells after repeated exposure to lipopolysaccharide and external heating. Arch Immunol Ther Exp 45:301–305Google Scholar
  79. Nalubamba KS, Gossner AG, Dalziel RG, Hopkins J (2007) Differential expression of pattern recognition receptors in sheep tissues and leukocyte subsets. Vet Immunol Immunopathol 118:252–262PubMedCrossRefGoogle Scholar
  80. Noack M, Miossec P (2014) Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun Rev 13:668–677PubMedCrossRefGoogle Scholar
  81. Oosterveld FG, Rasker JJ (1994) Effect of local heat and cold treatment on surface and articular temperature of arthritic knees. Arthritis Rheum 37:1578–1582PubMedCrossRefGoogle Scholar
  82. Oviedo-Boyso J, Valdez-Alarcón JJ, Cajero-Juárez M, OchoaZarzosa A, López-Meza JE, Bravo-Patiño A, Baizabal-Aguirre VM (2007) Innate immune response of bovine mammary gland to pathogenic bacteria responsible for mastitis. J Infect 54:399–409PubMedCrossRefGoogle Scholar
  83. Park HG, Han SI, Oh SY, Kang HS (2005) Cellular responses to mild heat stress. Cell Mol Life Sci 62:10–23PubMedCrossRefGoogle Scholar
  84. Punnonen J, Aversa G, Cocks BG, McKenzie ANJ, Menon S, Zurawski G, De Waal Malefyt R, De Vries JE (1993) Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc Natl Acad Sci 90:3730–3734PubMedPubMedCentralCrossRefGoogle Scholar
  85. Rhoads RP, Baumgard LH, Suagee JK, Sanders SR (2013) Nutritional interventions to alleviate the negative consequences of heat stress. Adv Nutr 4:267–276PubMedPubMedCentralCrossRefGoogle Scholar
  86. Rock KL, Latz E, Ontiveros F, Kono H (2010) The sterile inflammatory response. Annu Rev Immunol 28:321–342PubMedPubMedCentralCrossRefGoogle Scholar
  87. Romero RD, Pardo AM, Montaldo HH, Rodríguez AD, Romero JHC (2013) Differences in body temperature, cell viability, and HSP-70 concentrations between Pelibuey and Suffolk sheep under heat stress. Trop Anim Health Prod 45:1691–1696PubMedCrossRefGoogle Scholar
  88. Rosen O, Pedersen BK, Øritsland TR, Bahr R, Kjeldsen-Kragh J (2001) Leukocyte counts and lymphocyte responsiveness associated with repeated bouts of strenuous endurance exercise. J Appl Physiol 91:425–434Google Scholar
  89. Saker KE, Fike JH, Veit H, Ward DL (2004) Brown seaweed-(Tasco™) treated conserved forage enhances antioxidant status and immune function in heat-stressed wether lambs. J Anim Physiol Anim Nutr 88:122–130CrossRefGoogle Scholar
  90. Salces-Ortiz J, Gonzáez C, Moreno-Sánchez N, Calvo JH, Pérez-Guzmán M, Serrano MM (2013) Ovine HSP90AA1 expression rate is affected by several SNPs at the promoter under both basal and heat stress conditions. PLoS One 8:e66641PubMedPubMedCentralCrossRefGoogle Scholar
  91. Schoenborn JR, Wilson CB (2007) Regulation of interferon-γ during innate and adaptive immune responses. Adv Immunol 96:41–101PubMedCrossRefGoogle Scholar
  92. Schroder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-γ: an overview of signals, mechanisms and functions. J Leukoc Biol 75:163–189PubMedCrossRefGoogle Scholar
  93. Sejian V, Maurya VP, Naqvi SMK (2010) Adaptive capability as indicated by endocrine and biochemical responses of Malpura ewes subjected to combined stresses (thermal and nutritional) in a semi-arid tropical environment. Int J Biometeorol 54:653–661PubMedCrossRefGoogle Scholar
  94. Sevi A, Massa S, Annicchiarico G, Dell’Aquila S, Muscio A (1999) Effect of stocking density on ewes milk yield, udder health and micro-environment. J Dairy Res 66:489–499PubMedCrossRefGoogle Scholar
  95. Sevi A, Annicchiarico G, Albenzio M, Taibi L, Muscio A, Dell’Aquila S (2001) Effects of solar radiation and feeding time on behavior, immune response and production of lactating ewes under high ambient temperature. J Dairy Sci 84:629–640PubMedCrossRefGoogle Scholar
  96. Sevi A, Albenzio M, Annicchiarico G, Caroprese M, Marino R, Taibi L (2002) Effects of ventilation regimen on the welfare and performance of lactating ewes in summer. J Anim Sci 80:2349–2361PubMedCrossRefGoogle Scholar
  97. Sevi A, Taibi L, Albenzio M, Annicchiarico G, Marino R, Caroprese M (2003) Influence of ventilation regimen on micro-environment and on ewe welfare and milk yield in summer. Ital J Anim Sci 2:197–212CrossRefGoogle Scholar
  98. Sevi A, Albenzio M, Annicchiarico G, Caroprese M, Marino R, Santillo A (2006) Effects of dietary protein level on ewe milk yield and nitrogen utilization, and on air quality under different ventilation rates. J Dairy Sci 73:197–206Google Scholar
  99. Sgorlon S, Colitti M, Asquini E, Ferrarini A, Pallavicini A, Stefanon B (2012) Administration of botanicals with the diet regulates gene expression in peripheral blood cells of Sarda sheep during ACTH challenge. Domest Anim Endocrinol 43:213–226PubMedCrossRefGoogle Scholar
  100. Silanikove N (2000) Effects of heat stress on the welfare of extensively managed domestic ruminants. Livest Prod Sci 67:1–18CrossRefGoogle Scholar
  101. Silanikove N, Shapiro F, Shinder D (2009) Acute heat stress brings down milk secretion in dairy cows by up-regulating the activity of the milk-borne negative feedback regulatory system. BCM Physiol 9:13Google Scholar
  102. Sordillo LM (2013) Selenium-dependent regulation of oxidative stress and immunity in periparturient dairy cattle. Vet Med Int 2:1–8CrossRefGoogle Scholar
  103. Sordillo LM, Raphael W (2013) Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Vet Clin N Am Food Anim Pract 29:267–278CrossRefGoogle Scholar
  104. Spears JW, Weiss WP (2008) Role of antioxidants and trace elements in health and immunity of transition dairy cows. Vet J 176:70–76PubMedCrossRefGoogle Scholar
  105. Szczęsna M, Kirsz K, Kmiotek M, Zieba DA (2015) Seasonal fluctuation in the steady-state mRNA levels of suppressor of cytokine signaling-3 (SOCS-3) in the mammary gland of lactating and non-lactating ewes. Small Rumin Res 124:101–104CrossRefGoogle Scholar
  106. Todini I (2007) Thyroid hormones in small ruminants: effects of the endogenous, environmental and nutritional factors. Animal 1:997–1008PubMedCrossRefGoogle Scholar
  107. Trinchieri G (1998) Proinflammatory and immunoregulatory functions of interleukin-12. Int Rev Immunol 16:365–396PubMedCrossRefGoogle Scholar
  108. Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133–146PubMedCrossRefGoogle Scholar
  109. van der Poll T, van Deventer SJ (1998) The role of interleukin 6 in endotoxin-induced inflammatory responses. Prog Clin Biol Res 397:365–377PubMedGoogle Scholar
  110. Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132:256–263PubMedCrossRefGoogle Scholar
  111. Wadekar SA, Li DP, Periyasamy S, Sanchez ER (2001) Inhibition of heat shock transcription factor by GR. Mol Endocrinol 15:1396–1410PubMedCrossRefGoogle Scholar
  112. Wahl SM, Hunt DA, Wong HL, Dougherty S, McCartney-Francis N, Wahl LM, Ellingsworth L, Schmidt JA, Hall G, Roberts AB, Sporn MB (1988) Transforming growth factor-beta is a potent immunosuppressive agent that inhibits IL-1-dependent lymphocyte proliferation. J Immunol 140:3026–3032PubMedGoogle Scholar
  113. Wattegedera S, Sills K, Howard CJ, Hope JC, McInnes CJ, Entrican G (2004) Variability in cytokine production and cell proliferation by mitogen-activate ovine peripheral blood mononuclear cells: modulation by interleukin (IL)-10 and IL-12. Vet Immunol Immunopathol 102:67–76PubMedCrossRefGoogle Scholar
  114. Wattegedera S, Rocchi M, Sales J, Howard CJ, Hope JC, Entrican G (2008) Antigen-specific peripheral immune responses are unaltered during normal pregnancy in sheep. J Reprod Immunol 77:171–178PubMedCrossRefGoogle Scholar
  115. Wattegedera S, Corripio-Miyar Y, Pang Y, Frew D, McNeilly TN, McInnes C, Hope J, Glass E, Entrican G (2015) Evaluation of methods and development of reagents for the detection of native bovine and ovine IL-17 A production. Book of abstract of 5th European Veterinary Immunology Workshop (EVIW), p 38Google Scholar
  116. Webster JJ, Tonelli L, Sternberg EM (2002) Neuroendocrine regulation of immunity. Annu Rev Immunol 20:125–163PubMedCrossRefGoogle Scholar
  117. Zurawski G, de Vries J (1994) Interleukin-13, and interleukin-4 like cytokine that acts on monocytes and B-cells but not on T-cells. Immunol Today 15:19–26PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Mariangela Caroprese
    • 1
    Email author
  • Maria Giovanna Ciliberti
    • 1
  • Marzia Albenzio
    • 1
  • Agostino Sevi
    • 1
  1. 1.Department of the Sciences of Agriculture, Food and Environment (SAFE)University of FoggiaFoggiaItaly

Personalised recommendations