Abstract
While fever is known to occur in invertebrates and vertebrates, the mechanisms of fever in animals other than mammals have received scant attention. We look initially at the recognition, by the avian immune system, of pathogen associated molecular patterns and the likely role of toll-like receptors in signaling the presence of bacteria and viruses. Several mediators of fever are subsequently released by immune cells, including interleukin-6 and interleukin-1β, that eventually reach the brain and alter thermoregulatory function. As is the case in mammals, prostaglandins appear to be the ultimate mediators of fever in birds, since the febrile response is attenuated when prostaglandin synthesis is inhibited. Ambient temperature modulates the fever response, with larger fevers at higher, and smaller fevers at lower ambient temperatures. Glucocorticoid levels are increased during fever and seem to play an important role by modulating the extent of fever generation, possibly playing a role in the attenuation of fever after repeated exposure to a pathogen in a process termed tolerance, suggesting that the fever process can be phenotypically adapted to likely future conditions. While fever has an ancient phylogenetic history and many of the underling mechanisms in birds appear similar to mammals, there are several important differences that suggest fever has evolved quite differently in these two homeothermic classes.
Similar content being viewed by others
Abbreviations
- LPS:
-
Lipopolysaccharide
- PAMP:
-
Pathogen-associated molecular pattern
- MDP:
-
Muramyl dipeptide
- TLR:
-
Toll-like receptor
- EE:
-
Energy expenditure
- PG:
-
Prostaglandin
- NO:
-
Nitric oxide
- AA:
-
Arachidonic acid
- COX:
-
Cyclo-oxygenase
- l-NAME:
-
l-Nitro-arginine methyl ester
- IL:
-
Interleukin
- TRI:
-
Thermal response index
- AVT:
-
Arginine vasotocin
- TNZ:
-
Thermoneutral zone
- TNF:
-
Tumour necrosis factor
- HPA:
-
Hypothalamic–pituitary–adrenal
References
Akarsu E, House R, Cohceani F (1998) Formation of interleukin-6 in the brain of the febrile cat: relationship to interleukin-1. Brain Res 803:137–143
Ardawi M, Newsholme E (1985) Metabolism in lymphocytes and its importance in the immune response. Essays Biochem 21:1–44
Baert K, Duchateau L, Boever SD, Cherlet M, Backer PD (2005) Antipyretic effect of oral sodium salicylate after an intravenous E. coli LPS injection in broiler chickens. Br Poult Sci 46:137–143
Banet M (1981) Fever and survival in the rat. Metabolic versus temperature response. Cell Mol Life Sci 37:1302–1304
Banet M (1986) Fever in mammals: is it beneficial? Yale J Biol Med 59:117–124
Barr D, Russell L, DuBois E (1922) Clinical calorimetry XXXII: temperature regulation after the intravenous injection of protease and typhoid vaccine. Arch Intern Med 29:608–634
Barton G, Medzhitov R (2002) Toll-like receptors and their ligands. Curr Top Microbiol Immunol 270:81–92
Beisel W (1975) Metabolic response to infection. Annu Rev Med 26:9–20
Beishuizen A, Thijs L (2003) Review: endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J Endotoxin Res 9:3–24
Bilbo SD, Nelson RJ (2002) Melatonin regulates energy balance and attenuates fever in Siberian hamsters. Endocrinology 143:2527–2533
Blatteis CM (2003) Fever: pathological or physiological, injurious or beneficial? J Therm Biol 28:1–13
Blatteis CM (2004) The cytokine-prostaglandin cascade in fever production: fact of fancy? J Therm Biol 29:359–368
Blatteis CM, Sehic E, Li S (2000) Pyrogen sensing and signalling: old views and new concepts. Clin Infect Dis 31:S168–S177
Boorstein SM, Ewald PW (1987) Costs and benefits of behavioral fever in Melanoplus sanguinipes infected by Nosema acridophagus. Physiol Zool 60:586–595
Boulant J (2000) Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clin Infect Dis Clin 31:S157–S161
Bouverot P, Hildwein G, Le Goff D (1974) Evaporative water loss, respiratory pattern, gas exchange and acid–base balance during thermal panting in Pekin ducks exposed to moderate heat. Respir Physiol 21:255–269
Boyd A, Philbin VJ, Smith AL (2007) Conserved and distinct aspects of the avian Toll-like receptor (TLR) system: implications for transmission and control of bird-borne zoonoses. Biochem Soc Trans 35:1504–1507
Bronstein SM, Conner WE (1984) Endotoxin-induced behavioural fever in the Madagascar cockroach, Gromphadorhina portentosa. J Insect Physiol 30:327–330
Brownlie R, Allan B (2011) Avian toll-like receptors. Cell Tissue Res 343:121–130
Cabanac M, Guelte LL (1980) Temperature regulation and prostaglandin E1 fever in scorpions. J Physiol 303:365–370
Capua I, Marangon S (2000) The avian influenza epidemic in Italy, 1999–2000: a review. Avian Pathol 29:289–294
Cartmell T, Mitchell D (2005) The molecular basis of fever. In: Steckler T, Kahn NH, Reul JM (eds) Handbook of stress and the brain, vol 15. Elsevier, Amsterdam
Cartmell T, Poole S, Turnbull AV, Rothwell NJ, Luheshi GN (2000) Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J Physiol 526:653–661
Casterlin ME, Reynolds WW (1977) Behavioral fever in anuran amphibian larvae. Life Sci 20:593–596
Casterlin ME, Reynolds WW (1980) Fever and antipyresis in the crayfish Cambarus bartoni. J Physiol 303:417–421
Cavaillon J, Adib-Conquy M (2006) Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis. Crit Care 10:233
Chuang J, Lin M, Chan S, Won S (1990) Febrile effects of polyriboinosinic acid: polyribocytidylic acid and interferon: relationship to somatostatin in rat hypothalamus. Pflüg Arch Eur J Physiol 415:606–610
Coelho MM, Luheshi G, Hopkins SJ, Pela IR, Rothwell NJ (1995) Multiple mechanisms mediate antipyretic action of glucocorticoids. Am J Physiol Regul Integr Comp Physiol 269:R527–R535
Coon CAC, Warne RW, Martin LB (2011) Acute-phase responses vary with pathogen identity in house sparrows (Passer domesticus). Am J Physiol Regul Integr Comp Physiol 300:R1418–R1425
D’Alecy LG, Kluger M (1975) Avian febrile response. J Physiol 253:223–232
Dawson W (1982) Evaporative losses of water by birds. Comp Biochem Physiol A 71:95–509
DeBoever S, Beyaert R, Vandemaele F, Baert K, Duchateau L, Goddeeris B, Backer PD, Croubels S (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 37:39–44
Demas G, Chefer V, Talan M, Nelson R (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol 273:R1631–R1637
Denyer SP, Hodges NA, Gorman SP, Russel AD (2004) Hugo and Russell pharmaceutical microbiology. Blackwell, Oxford
Dijkhuizen A, Davies G (1995) Animal health and related problems in densely populated livestock areas of the community. In: Proceedings of a workshop of the European commission, agriculture, Brussels, Belgium
Dil N, Qureshi MA (2002) Involvement of lipopolysaccharide related receptors and nuclear factor kB in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds. Vet Immunol Immunopathol 88:149–161
Dinarello C, Cannon J, Mancilla J, Bishai I, Lees J, Coceani F (1991) Interleukin-6 as an endogenous pyrogen: induction of prostaglandin E2 in brain but not in peripheral blood mononuclear cells. Brain Res 562:199–206
Erf GF (2004) Cell-mediated immunity in poultry. Br Poult Sci 83:580–590
Fan H, Cook J (2004) Molecular mechanisms of endotoxin tolerance. J Endotoxin Res 10:71–84
Feder M, Hofmann G (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Feldberg W, Saxena P (1971) Fever produced by prostaglandin E1. J Physiol 217:547–556
Firth BT, Boardman TJ (1980) Independent effects of the pineal and a bacterial pyrogen in behavioural thermoregulation in lizards. Nature 285:399–400
Flohéa S, Fernándeza ED, Ackermann M, Hirsch T, Börgermann J, Schadeb F (1998) Endotoxin tolerance in rats: expression of TNF-a, IL-6, IL-10, VCAM-1 and HSP 70 in lung and liver during endotoxin shock. Cytokine 11:796–804
Fortier M-E, Kent S, Ashdown H, Poole S, Boksa P, Luheshi GN (2004) The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am J Physiol Regul Integr Comp Physiol 287:R759–R766
Fraifeld V, Blaicher-Kulick R, Degen AA, Kaplanski J (1995) Is hypothalamic prostaglandin E2 involved in avian fever? Life Sci 56:1343–1346
Fukui A, Inoue N, Matsumoto M, Nomura M, Yamada K, Matsudan Y, Toyoshima K, Tsukasa-Seya T (2001) Molecular cloning and functional characterization of chicken toll-like receptors: a single chicken toll covers multiple molecular patterns. J Biol Chem 276:47143–47149
Givalois LG, Dornand J, Mekaouche M, Solier MD, Bristow AF, Ixart G, Siaud P, Assenmacher I, Barbanel G (1994) Temporal cascade of plasma level surges in ACTH, corticosterone, and cytokines in endotoxin-challenged rats. Am J Physiol Regul Integr Comp Physiol 266:R164–R170
Gray DA, Ironside CS, Maloney SK (2000) Modulation of plasma antidiuretic hormone levels does not change the magnitude of the LPS-induced febrile response in Pekin ducks. J Comp Physiol B 170:315–320
Gray DA, Maloney SK, Kamerman PR (2005) Lipopolysaccharide- induced fever in Pekin ducks is mediated by prostaglandins and nitric oxide and modulated by adrenocortical hormones. Am J Physiol Regul Integr Comp Physiol 289:R1258–R1264
Gray DA, Maloney SK, Kamerman PR (2008) Restraint increases afebrile body temperature but attenuates fever in Pekin ducks (Anas platyrhynchos). Am J Physiol Regul Integr Comp Physiol 294:R1666–R1671
Guerreiro EN, Giachetto PF, Givisiez PEN, Ferro JA, Ferro MIT, Gabriel JE, Furlan RL, Macari M (2004) Brain and hepatic Hsp70 protein levels in heat-acclimated broiler chickens during heat stress. Rev Bras Cienc Avic 6:201–206
Hallman GM, Towner MC (1990) Effect of bacterial pyrogen on three lizard species. Comp Biochem Physiol A 96:383–386
Harden L, Plessis ID, Poole S, Laburn H (2006) Interleukin-6 and leptin mediate lipopolysaccharide-induced fever and sickness behaviour. Physiol Behav 89:146–155
Harden L, Plessis ID, Poole S, Laburn H (2008) Interleukin (IL)-6 and IL-1beta act synergistically within the brain to induce sickness behaviour and fever in rats. Brain Behav Immun 22:838–849
Hasday J, Fairchild K, Shanholtz C (2000) The role of fever in the infected host. Microb Infect 2:1891–1904
Houghton JT (1985) The global climate. Cambridge University Press, Cambridge
Houghton JT (2004) Global warming: the complete briefing. Cambridge University Press, Cambridge
Huang WT, Lin MT, Won SJ (1997) Mechanisms and sites of pyrogenic action exerted by staphylococcal enterotoxin A in rabbits. Neurosci Lett 236:53–56
WATT Executive Guide to World Poultry Trends (2007) In: 2007 Executive guide. Poultry International, USA
Janeway C, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216
Johnson RW, Curtis S, Dantzer R, Bahr J, Kelley KW (1993a) Sickness behavior in birds caused by peripheral or central injection of endotoxin. Physiol Behav 53:343–348
Johnson RW, Curtis SE, Dantzer R, Kelley KW (1993b) Central and peripheral prostaglandins are involved in sickness behaviour in birds. Physiol Behav 53:127–131
Kamerman PR, Laburn HP, Mitchell D (2003) Inhibitors of nitric oxide synthesis block cold-induced thermogenesis in rats. Can J Physiol Pharmacol 81:834–838
Kawasaki H, Moriyama M, Ohtani Y, Naitoh M, Nariuchi H, Tanaka A (1987) Restoration of normal febrile response to endotoxin in pyrogen-tolerant rabbits by injection with human beta interferon. Infect Immun 55:2574–2578
Klasing KC (1998) Avian macrophages: regulators of local and systemic immune response. Poult Sci 77:983–989
Klasing K, Korver D (1997) Leucocytic cytokines regulate growth rate and composition following activation of the immune system. J Anim Sci 75:58–67
Klasing KC, Laurin D, Peng R, Fry D (1987) Immunologically mediated growth depression in chicks: influence of feed intake, corticosterone and interleukin-1. J Nutr 117:1629–1637
Kluger MJ, Rothenburg B (1979) Fever and reduced iron: their interaction as a host defence response to bacterial infection. Science 203:374–376
Kluger MJ, Vaughn L (1978) Fever and survival in rabbits infected with Pasteurella multocida. J Physiol 282:243–251
Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1996) The adaptive value of fever. Infect Dis Clin N Am 10:1–20
Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1998) Role of fever in disease. Ann N Y Acad Sci 856:224–233
Kogut MH, Iqbal M, He H, Philbin V, Kaiser P, Smith A (2005) Expression and function of toll-like receptors in chicken heterophils. Dev Comp Immunol 29:791–807
Koutsos EA, Klasing KC (2001a) The acute phase response in Japanese quail (Coturnix coturnix japonica). Comp Biochem Phys C 128:255–263
Koutsos EA, Klasing KC (2001b) Modulation of nutritional states by the immune response. In: Proceedings 28th Annual Caroline poultry nutrition conference, Sheraton Imperial Hotel, Raleigh, NC, 14–15 November, pp 1–6
Kozak WKJ, Conn CA, Kluger MJ (1997) Attenuation of lipopolysaccharide fever in rats by protein kinase C inhibitors. Am J Physiol Regul Integr Comp Physiol 273:R873–R879
Lee D (1948) Heat and cold. Annu Rev Physiol 10:365–386
Leshchinsky TV, Klasing KC (2001) Divergence of the inflammatory response in two types of chickens. Dev Comp Immunol 25:629–638
Liu E, Lewis K, Al-Saffar H, Krall CM, Singh A, Kulchitsky VA, Corrigan JJ, Simons CT, Peterson SR, Musteata FM, Bakshi CS, Romanovsky AA, Sellati TJ, Steiner AA (2012) Naturally occurring hypothermia is more advantageous than fever in severe forms of lipopolysaccharide- and Escherichia coli-induced systemic inflammation. Am J Physiol Regul Integr Comp Physiol 302:R1372–R1383
Luker F, Mitchell D, Laburn H (2000) Fever and motor activity in rats following day and night injection of Staphylococcus aureus cell walls. Am J Physiol Regul Integr Comp Physiol 279:R610–R616
Macari M, Furlan RL, Gregorut FP, Secato ER, Guerreiro JR (1993) Effects of endotoxin, interleukin 1-beta and prostaglandin injections on fever response in broilers. Br Poult Sci 34:1035–1042
Mackowiak P (1994) Fever: blessing or curse? A unifying hypothesis. Ann Intern Med 120:1037–1040
Mackowiak P, Boulant J (1996) Fever’s glass ceiling. Clin Infect Dis 22:525–536
Mahmoud KZ, Edens FW, Eisen EJ, Havenstein GB (2003) Effect of ascorbic acid and acute heat exposure on heat shock protein 70 expression by young white Leghorn chickens. Comp Biochem Phys C 136:329–335
Maloney SK, Gray DA (1998) Characteristics of the febrile response in Pekin ducks. J Comp Physiol B 168:177–182
Maloney SK, Bonomelli JM, DeSouza J (2003) Scrotal heating stimulates panting and reduces body temperature similarly in febrile and non-febrile rams (Ovis aries). Comp Biochem Physiol A 135:565–573
Marais M, Gray DA (2009) A role for natriuretic peptide in lipopolysaccharide-induced fever in Pekin ducks (Anas platyrhynchos): is natriuretic peptide an endogenous antipyretic in birds? J Comp Physiol B 179:125–132
Marais M, Gugushe N, Maloney SK, Gray DA (2011a) Body temperature responses of Pekin ducks exposed to different pathogens. Poult Sci 90:1234–1238
Marais M, Maloney SK, Gray DA (2011b) The metabolic cost of fever in Pekin ducks. J Therm Biol 36:116–120
Marais M, Maloney SK, Gray DA (2011c) Brain IL-6 and prostaglandin-dependent actions of IL-1β and lipopolysaccharide in avian fever. Am J Physiol Regul Integr Comp Physiol 301:R791–R800
Marais M, Maloney SK, Gray DA (2011d) Ambient temperature modulates the magnitude of LPS-induced fevers in Pekin ducks. J Therm Biol 36:121–127
Marais M, Maloney SK, Gray DA (2011e) The development of endotoxin tolerance, and the role of hypothalamic–pituitary–adrenal function and glucocorticoids in Pekin ducks. J Exp Biol 214:3378–3385
Mazzi CM, Ferro MIT, Coelho AAD, Savino VJM, Macari M, Ferro JA, Givivisiez PEN, Giachetto PF, Silva MM, Dionello NJL (2002) Effect of heat exposure on the thermoregulatory responses of selected naked neck chickens. Arq Bras Med Vet Zootec 54:35–41
McKechnie A, Wolf B (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett 6:253–256
Medzhitov R, Janeway CJ Jr (2000) Innate immune recognition: mechanisms and pathways. Immunol Rev 173:89–97
Monagas WR, Gatten RJ (1983) Behavioural fever in the turtles Terrapene carolina and Chrysemys picta. J Therm Biol 8:285–288
Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168
Muchlinski AE, Hogan JM (1989) Fever response in laboratory-maintained and free-ranging chuckwallas (Sauromalus obesus). Am J Physiol Regul Integr Comp Physiol 257:R150–R155
Nomoto S (1996) Diurnal variations in fever induced by intravenous LPS injection in pigeons. Pflugers Arch 431:987–989
Nomoto S (2003) Role of prostaglandin E2 and indomethacin in the febrile response of pigeons. Jpn J Physiol 53:253–258
Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K et al (2000) Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 164:3476–3479
Oka Y, Ibuki T, Matsumura K, Namba M, Yamazaki Y, Poole S, Tanaka Y, Kobayashi S (2007) Interleukin-6 is a candidate molecule that transmits inflammatory information to the CNS. Neuroscience 145:530–538
Palmes E, Park C (1965) The regulation of body temperature during fever. Arch Environ Health 11:749–759
Parry M, Canziani O, Palutikof J, Van der Linden P, Hanson C (2007) Change 2007: impacts, adaptation and vulnerability. In: Contribution of working group 2 to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK
Philippe A, Pierre C (2004) Impacts du changement climatique et modalisation intagrae, la part de l’arbitraire. Natures Sciences Sociétés 12(4):375–386
Pichlmair A, Sousa CRE (2007) Innate recognition of viruses. Immunity 27:370–383
Pittman QJ, Cockeram AW, Cooper KE (1976) Changes in body temperature produced by prostaglandins and pyrogens in the chicken. Am J Physiol 230:1284–1287
Prinzingera R, Pressmara A, Schleuchera E (1991) Body temperature in birds. Comp Biochem Physiol A 99:499–506
Reynolds WW, Casterlin ME, Covert JB (1976) Behavioural fever in teleost fishes. Nature 259:41–42
Roe C, Kinney J (1965) The caloric equivalent of fever II. Influence of major trauma. Ann Surg 161:140–147
Romanovsky AA, Almeida M, Aronoff DM, Ivanov AI, Konsman JP, Steiner AA, Turek VF (2005) Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci 10:2193–2216
Roth J (2006) Endogenous antipyretics. Clin Chim Acta 371:13–24
Roth J, De Souza G (2001) Fever induction pathways: evidence from responses to systemic and local cytokine formation. Braz J Med Biol Res 34:301–314
Roth J, McClellan JL, Kluger MJ, Zeisberger E (1994) Attenuation of fever and release of cytokines after repeated injections of lipopolysaccharide in guinea-pigs. J Physiol 477:177–185
Roth J, Aslan T, Storr B, Zeisberger E (1997) Lack of cross tolerance between LPS and muramyl dipeptide in induction of circulation TNF-a and IL-6 in guinea pigs. Am J Physiol Regul Integr Comp Physiol 273:R1529–R1533
Roth J, Harre E, Rummel C, Gerstberger R, Hubschle T (2004) Signaling the brain in systemic inflammation: role of sensory circumventricular organs. Front Biosci 9:290–300
Rothwell NJ, Luheshi GN, Toulmond S (1996) Cytokines and their receptors in the central nervous system: physiology, pharmacology and pathology. Pharmacol Ther 69:85–95
Rudaya AY, Steiner AA, Robbins JR, Dragic AS, Romanovsky AA (2005) Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am J Physiol Regul Integr Comp Physiol 289:R1244–R1252
Schneider K, Klaas R, Kaspers B, Staeheli P (2001) Chicken interleukin-6 cDNA structure and biological properties. Eur J Biochem 268:4200–4206
Scott IM, Fertel RH, Boulant JA (1987) Leucocytic pyrogen effects on prostaglandins in hypothalamic tissue slices. Am J Physiol Regul Integr Comp Physiol 253:R71–R76
Shanks N, Windle R, Perks P, Harbuz M, Jessop D, Ingram D, Lightman S (2000) Early life exposure to endotoxin alters hypothalamic–pituitary–adrenal axis and pre-disposition to inflammation. Proc Natl Acad Sci USA 97:5645–5650
Sharp F, Hammel H (1972) The effects of fever on the salivation response in the resting and exercising dog. Am J Physiol 223:77–82
Sherman EBL, Fernandez G (1991) Fever and thermal tolerance in the toad Bufo marinus. J Therm Biol 16:297–301
Shoham S, Krueger J (1988) Muramyl dipeptide-induced sleep and fever: effects of ambient temperature and time of injections. Am J Physiol Regul Integr Comp Physiol 255:R157–R165
Simon-Opperman C, Simon E, Jessen C, Hammel H (1978) Hypothalamic thermosensitivity in conscious Pekin ducks. Am J Physiol Regul Integr Comp Physiol 235:R130–R140
Staeheli P, Puehler F, Schneider K, Gobel TW, Kaspers B (2001) Cytokines of birds: conserved functions—a largely different look. J Interferon Cytokine Res 21:993–1010
Steiner AA, Branco LGS (2001) Nitric oxide in the regulation of body temperature and fever. J Therm Biol 26:325–330
Steiner AA, Rudaya AY, Ivanov AI, Romanovsky AA (2004) Febrigenic signalling to the brain does not involve nitric oxide. Br J Pharmacol 141:1204–1213
Steiner AA, Ivanov AI, Serrats J, Hosokawa H, Phayre A, Robbins J, Roberts J, Kobayashi S, Matsumura K, Sawchenko P et al (2006) Cellular and molecular bases of the initiation of fever. PLoS Biol 4:1517–1524
Steiner AA, Hunter JC, Phipps SM, Nucci TB, Oliveira DL, Roberts JL, Scheck AC, Simmons DL, Romanovsky AA (2009) Cyclooxygenase-1 or -2 which one mediates lipopolysaccharide-induced hypothermia? Am J Physiol Regul Integr Comp Physiol 297:R485–R494
Stitt J (1973) Prostaglandin E1 fever induced in rabbits. J Physiol 232:163–179
Stitt J (1979) Fever versus hyperthermia. Fed Proc 38:39–43
Tanaka M, McKinley M, McAllen R (2009) Roles of two preoptic cell groups in tonic and febrile control of rat tail sympathetic fibers. Am J Physiol Regul Integr Comp Physiol 296:R1248–R1257
Tegowska E, Kadziela W, Narebski J (1986) Ambient thermal conditions and thermoregulatory mechanisms in fever in rabbits. Acta Physiol Pol 37:8–17
Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW (2008) Evolution of the chicken toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 1:62
vanKampen M (1971) Some aspects of thermoregulation White Leghorn fowl. Int J Biometeorol 15:244–246
Vasilache AM, Andersson J, Nilsberth C (2007) Expression of PGE2 EP3 receptor subtypes in the mouse preoptic region. Neurosci Lett 423:179–183
Voet D, Voet JG (2004) Biochemistry. Wiley International, NJ
West M, Heagy W (2002) Endotoxin tolerance: a review. Crit Care Med 30:S54–S73
Won S, Lin M (1988) Pyrogenicity of interferon and its inducer in rabbits. Am J Physiol 254:R499–R507
Xie W, Merrill JR, Bradshaw WS, Simmons DL (1992) Structural determination and promoter analysis of the chicken mitogen-inducible prostaglandin G/H synthase gene and genetic mapping of the murine homolog. Arch Biochem Biophys 300:247–252
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume.
Rights and permissions
About this article
Cite this article
Gray, D.A., Marais, M. & Maloney, S.K. A review of the physiology of fever in birds. J Comp Physiol B 183, 297–312 (2013). https://doi.org/10.1007/s00360-012-0718-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-012-0718-z