Rev Colomb Cienc Pecu 2016; 29:159-168

Revista Colombiana de Ciencias Pecuarias

Original articles

159

Literature Review

Physiology, cell dynamics of small intestinal mucosa, and performance of broiler chickens under heat stress: a review¤

Fisiología, dinámica celular de la mucosa del intestino delgado y rendimiento de pollos de engorde sometidos a estrés calórico: revisión de literatura

Fisiologia, dinâmica celular da mucosa do intestino delgado e desempenho de frangos de corte submetidos ao estresse pelo calor: revisão de literatura

Cristiane FP Marchini1*, MV, PhD; Marcos B Café2, MV, PhD; Eugênio G Araújo2, MV, PhD; Mara RBM Nascimento3, MV, PhD.

1Curso de Medicina Veterinária, Universidade de Franca, Franca, Brasil.

2Escola de Veterinária e Zootecnia, Universidade Federal de Goiás, Goiânia, Brasil.

3Faculdade de Medicina Veterinária, Universidade Federal de Uberlândia, Uberlândia, Brasil.

(Received: August 5, 2015; accepted: March 22, 2016)

doi: 10.17533/udea.rccp.v29n3a01

¤ Tocitethisarticle:MarchiniCFP,CaféMB,AraùjoEG,NascimentoMRBM.Physiology,celldynamicsofsmallintestinalmucosa,andperformanceofbroilerchickensunderheatstress:areviewRevColombCiencPecu2016;29:159-168.

* Correspondingauthor:CristianeFerreiraPrazeresMarchini.CursodeMedicinaVeterinária,UniversidadedeFranca.RuaRioGrandedoSul,1795–VilaAparecida–Franca/SP,Brasil,CEP:14401-324.E-mail:cfprazeres@gmail.com

Summary

Highroomtemperaturereducesproductionefficiencyofbroilerchickens.Differentfactorscontributetothissituation:fastgrowth,physiologicalvariations,andchangesinthesmallintestinemucosa.Thisreviewaimstodefinetheconceptofheatstressanditseffectsonseveralphysiologicalaspectsrelatedtothedevelopmentofthesmallintestinemucosaandtheperformanceofbroilerchickens.Heatstresstriggersacorticosteroidincreaseandacirculatingtriiodothyroninehormone(T3)reduction,increasesrespiratoryfrequency,whichtriggersrespiratoryalkalosis,diminishesfoodintake,andleadstochangesinthecellulardynamicsofthesmallintestinemucosa.Thesechangesdependonanimalgenotype,intensity,anddurationofthestressor.Acuteheatstressleadstoareductioninenterocyteproliferationandalsotoadecreaseincryptdepth,withoutaffectingvillusheightorvillus/cryptratio.Ontheotherhand,chronicstressdiminishesvillusheightandjejunumweight.Thesechangesaffectthecapacityofbroilerstodigestandabsorbthenutrientsrequiredformaintenanceandproduction.

Keywords: corticosteroids, enterocyte proliferation, gastrointestinal tract, microscopic findings, morphological findings.

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Resumen

Unaaltatemperaturaambientedisminuyelaeficienciadelaproduccióndepollosdeengorde.Diversosfactorescontribuyenaestasituación:crecimientorápido,cambiosfisiológicos,yanomalíasdelamucosadelintestinodelgado.Elobjetivodelapresenterevisiónfuedefinirelconceptodeestréscalóricoysusefectossobrealgunosaspectosdelafisiología,eneldesarrollodelamucosadelintestinodelgado,yenelrendimientodepollosdeengorde.Elestréscalóricodesencadenaunaumentodelosnivelesdecorticosteroides,reduccióndelahormonatriyodotironina(T3)circulante,aumentoenlafrecuenciarespiratoriaqueresultaenalcalosisrespiratoria,disminuyelaingestadealimentosyprovocacambiosenladinámicacelulardelamucosadelintestinodelgado.Estoscambiosdependendelgenotipodelanimalydelaintensidadyduracióndelaaccióndelfactorestresante.Elestréscalóricoagudocausaunadisminuciónenlaproliferacióndeenterocitos,reduccióndelaprofundidaddelascriptassincambioenlaalturadelasvellosidadesyenlarelaciónvellosidades/cripta.Yaelestréscrónicodisminuyelaalturadelasvellosidadesyelpesodelyeyuno.Estoscambiosafectanlacapacidaddelpollodeengordeparadigeriryabsorberlosnutrientesparasumantenimientoyproducción.

Palabras clave: corticoesteroides, hallazgos microscópicos, hallazgos morfológicos, proliferación de enterocitos, tracto gastrointestinal.

Resumo

Atemperaturaambienteelevadadiminuiaeficiênciaprodutivadefrangosdecorte.Diferentesfatorescontribuemparaestasituação:crescimentorápido,mudançasfisiológicasealteraçõesnamucosadointestinodelgado.Nestarevisão,oobjetivofoidefiniroconceitodeestressepelocaloreseusefeitossobrealgunosaspectosdafisiologia,nodesenvolvimentodamucosadointestinodelgadoeodesempenhodefrangosdecorte.O estresse pelo calor desencadeia aumento nos níveis de corticosteroides e reduçãodo hormôniotriiodotironina(T3)circulante,aumentaafrequênciarespiratória,resultandoemalcaloserespiratória,diminuiaingestãodealimentosedesencadeiaalteraçõesnadinâmicacelulardamucosadointestinodelgado.Essasalteraçõesdependemdogenótipodoanimaledaintensidadeeduraçãodaaçãodoagenteestressor.Oestressepelocaloragudopromovediminuiçãonaproliferaçãodosenterócitos,reduçãonaprofundidadedascriptassemalteraçãonaalturadasvilosidadesenarelaçãovilo/cripta.Jáoestressecrônicodiminuiaalturadasvilosidadesepesodojejuno.Estasalteraçõesafetamacapacidadedofrangodecortededigerireabsorvernutrientesparasuamanutençãoeprodução.

Palavras chave:achados microscópicos, achados morfológicos, corticosteroide, proliferação de enterócitos, trato gastrointestinal.

Introduction

Thegeneticselectionforfastgrowthandweightgain that broiler chickens have been subjected toin the last fewdecadeshas caused thesebreeds tobecome very vulnerable to environmental factorsthatare typicalof tropical regions, suchas intensesolarradiation, temperature,andhighairhumidity.Together, these factors cause stress in birds and,consequently,discomfort.

Theconceptofstress,oftenpoorlyunderstood,canbedefinedas“aforceofanykindthatactsinthebodycausingastrainstate”(Silva,2000).Therefore,a strain state in living beings results from stressand depends on the physiological characteristicsof each organism (Silva, 2000).When differentenvironmental factors act alone or together on a

livingbeing, theybecomestress factors thatmaycausetensiononthebody(Silva,2008).Therefore,thesymptomspresentedbyanimalssufferingfromtheactionofenvironmentalfactorsshowthattheyareunderstrainortension(SilvaandMaia,2012).Whenbirdsareinastateofstrain,neuroendocrineaswellasphysiologicalandbehavioralresponsesoccur that enable the birds to acclimate to theadverse environmental conditions they are beingraised in, in order tomaintain homeostasis (VanBorelli,1995).

Thestraingeneratedbyheatstressmayalsotriggerchanges in intestinal development by reducing thesmall intestineweight, thenumberofvilli,andtheproliferation rateof enterocytes (Uniet al., 2001).It directly affects the bird capacity to digest andabsorb the nutrients required formaintenance and

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production(Quintero-Filhoet al.,2010).Thestraincausedbyheatstressmayreducegrowthrate,foodintake,finalbodyweight,andweightgain,aswellasfeedconversionratio.Thus,performanceofbirdssubjectedtoheatstressiscompromisedbydeficientintestinaldevelopmentanddiminishedfoodintake.Furthermore, the strain caused by heat stressmayaffectbroilermetabolism,causeoxidativestress,andincreasesuperoxideproductionandmalondialdehydelevels(Azadet al.,2010).

This review aims to define the concept of heatstressanditsconsequencesonseveralphysiologicalaspects of the development of the small intestinemucosaandtheperformanceofbroilerchickens.

Heat stress

The glossary of the International Union ofPhysiologicalScience(IUPS)ThermalCommission(2001)defines“thermalcomfortzone”as“therangeofambienttemperatures,associatedwithspecifiedmeanradiant temperature, humidity, and airmovement,withinwhichahumaninspecifiedclothingexpressesindifference to the thermal environment for anindefiniteperiod.”

Abirdmaintainsitsbodytemperatureinthethermalcomfortzonewithminimaluseofthermoregulatorymechanisms; i.e., themetabolic rate isminimum,constant,andindependentoftheroomtemperature(Abreuet al.,1998).Homeothermyismaintainedwithlowerenergyexpenditureundertheseconditionsandthebirdisabletoexpressitsmaximumproductionpotential(Furlan,2006).

According to the IUPSThermalCommission(2001),“thermalstressisanychangeinthethermalrelationship between a temperature regulatorymechanism and the environment which, if notcompensated,willresultinhyper-orhypothermia.”

Theeffectsofheatstressonbirdperformancewereextensivelystudiedinpastdecades(GrossandSiegel,1981;Arjonaet al.,1988;Donkoh,1989;CooperandWashburn,1998),ata timewhenmostshedswereopenandthustherewaslittleclimaticcontrolintheproductionenvironment.

In recent years, there has been a considerableincreaseinthenumberofstudiesonheatstressanditseffectsonanimalproduction,bothforeconomicreasonsandforanimalwelfare(Quintero-Filhoet al.,2010),andbecauseheatstressisanimportantproblemaffectingthepoultryindustryintropicalandsubtropicalregions(Sabahet al.,2008).

Organismsreacttoastressorwithphysiologicalor behavioral adjustments that allow them tobetter manage an adverse environment. Theseadjustmentsareanattempttomaintainhomeostasis,i.e., the relative constancy of chemical-physicalproperties in an organism internal environmentthat is maintained by regulatory mechanisms(IUPSThermalCommission,2001).TheThermalCommission (2001) considered such facts asevidencethatanimalsdevelopresponsemechanismswhentheirhomeostasisisthreatened.

It is necessary to emphasize that an animalresponsestostressorsdependmostlyonthegenotype(Havensteinet al.,2003a),intensityanddurationofthestressor(MitchellandLemme,2008).Thestressoreffectsonphysiologicalfunctionsmaybesufficientlyintensetocompromisethecapacityofbirdstogrow,reproduceandproduceefficiently(Medeiroset al., 2005;Silvaet al.,2007).

Heat stressmaybeacuteorchronic.Acutestressreferstosuddenandshortperiodsofhightemperatureforlessthansevendays,whereaschronicstressreferstoprolongedperiodsofhightemperatureformorethansevendays(Gonzalez-EsquerraandLeeson,2006).

Physiological changes induced by heat stress in broilers

Birdsarehomoeothermicanimalsthatmaintaina relatively constant internal body temperatureunderawiderangeofroomtemperatures(DawsonandWhittow, 1998). The body temperature ofadultdomesticatedbroilers isapproximately41.1°C(Marchiniet al.,2007).Whenairtemperatureandhumidity exceed the thermal comfort range, theability to dissipate heat is reduced and animalssuffer the effects of heat stress (Dawson andWhittow,1998).

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Theresponsetostressoragentsinvolvesaseriesofneuroendocrineandbehavioralresponsesthatseektomaintainthebalanceofvitalfunctions(BarnettandHemsworth,1990;VanBorelli,1995)byactivatingthehypothalamic-pituitary-adrenal(HPA)axis.ThestressoragentcausesanervestimulationthatreachesthehypothalamusandactivatestheHPAaxis,resultingintheproductionofcorticotropin-releasinghormone(CRH).Thishormoneactsontheadenohypophysis,whichwillproduceandsecreteadrenocorticotropichormone (ACTH) andβ-endorphins.Blood-streamtransportedACTHstimulatesglucocorticoidsecretionin the adrenal cortex as well as adrenalin andnoradrenalinreleaseinthesympatheticnerveendingsand in the adrenalmedulla (Dukes, 2004).Plasmacorticosteroidlevelsrapidlyincreaseasaconsequenceofsevereheatstressandreachapeakafteronehourofheatexposure(Siegel,1980).

Whenthestressoractionpersistsonananimal,there is prolonged secretion of hormones such ascatecholaminesandcorticosteroids.Numerousharmfulconsequenceswill be triggered if corticosteronelevelsremainhigh(Ribeiroet al.,2008),includingredistribution of body reserves—including energyand proteins—thus leading to reduced growth,reproduction, and health (Braude et al., 1999;Oliveiraet al., 2006)becausecorticosterone is theglucocorticoidresponsibleforglucoseformationfrombodyreservesofcarbohydrates,lipids,andproteins(Freeman,1987).

HPAregulationisaccomplishedbythenegativefeedbackmechanismof corticosterone,which actson thehypothalamusby inhibitingCRHrelease intheadenohypophysis,andtherebyinhibitingACTHsecretion(Dukes,2004).

Thyrotropin releasinghormone (TRH),producedin the hypothalamus, acts as a thyroid stimulatinghormone (TSH) stimulator.TSHacts in the thyroidglandtoproducethyroxin(T4),whichistransformedinto triiodothyronine (T3).SerumT3concentration is reducedasheatstresspersists(Yahavet al.,1995;Yahav,1999). Thyroidhormonesynthesis andsecretionareregulatedbythethyroidhormonesthemselvesinaself-regulatorymanner.Theseeventsdemonstratethatthereis“interaxial”hypothalamiccontrolofTSHreleaseinthechicken(Debonneet al.,2008).

Furthermore,heatstresscausesimportantchangesintheelectrolyticbalanceofbroilers(Borgeset al., 2004).The respiratory frequencyofbirds increasesin order to reduce body temperature during heatstress(Marchiniet al.,2007),andpantingresultsinchangesof theacid-basebalanceand inrespiratoryalkalosisfromgreatereliminationofCO2andfrompCO2reduction in the blood.The body respondswithmetabolic acidosis, anH+ excretiondecrease,and anHCO3

- excretion increase by the kidneysto compensate for this disturbance, and thus suchchangescontributetobloodacidification(Borgeset al.,2004).Energyreservereductiontakesplaceandthehomeostaticefficiencybalanceofthebodydiminishesastheacclimatizationmechanismsbegintofail.

Different physiological responsesmay occurduringheatstressandtheydependontheintensity,severity, and duration of heat stress (Azad et al., 2010), thereby causing higher or lower levels ofglucocorticoid release (Gonzalez-Esquerra andLeeson, 2006).Thesephysiological responses are:changes in the functional integrityof the intestinalmucosa(Hornet al.,2009),bodytemperatureincrease(Marchiniet al.,2007;MitchellandLemme,2008),muscledegradation(Zuoet al.,2015),andincreaseinmortalityrate(Estrada-Parejaet al.,2007)whenhighenvironmental temperaturescoincidewith theagetomarket(Arjonaet al.,1988).

Effects of heat stress on cell dynamics of broiler chicken small intestinal mucosa

Small intestinemucosadevelopment results fromtwoassociatedcytologicalevents:cellrenewal—dueto proliferation and differentiation of columnarcells in the crypt and along the villi (Uni et al., 1998)—andthenaturallossofcellsbyextrusionatthevillousapices(Pelicanoet al.,2003)after theyhave undergone apoptosis (Renehan et al., 2001).Enterocyte proliferation in broiler chicken smallintestineoccursinthecryptandalongthevilli(Uniet al.,1998).Atfourdaysofage,thesecellsmigratetotheduodenumandjejunum(Geyraet al.,2001).

Effective foodmetabolism is directly relatedtotheintegrityofthedigestivesystem,especiallythesmallintestine,andpartofthedigestiveprocess,

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aswellastheabsorptionofnutrients,occursintheenterocytes (Smith et al., 1990).The functionalintegrityoftheepithelialintestinalmucosadependsoncoordinatedprocesses,suchasmetabolicregulationofepithelialcellsandregulationofthemucuslayer.Theepitheliumofintestinalmucosaiscoveredbyamucuslayercomposedofglycoproteinssynthesizedbythegobletcells.Thismucusactsasaprotectionto helpmaintain epithelium integrity, lubrication,nutrient absorption (Gibson et al., 1996), andmoleculetransportbetweentheluminalcontentsandtheepithelialcellsduringdigestionandabsorptionofnutrientsfromthediet(Uniet al.,1998).Thus,mucusisthefirstbarrierthenutrientshavetointeractwith;theyhavetodiffuseintothemucustobeabsorbedandgainaccesstothecirculatorysystemandtheirtargetorgans (Bansil andTurner, 2006). Environmentalfactors able to induce changes in the dynamics ofmucins have the potential to affect viscosity andintegrityofthemucuslayerandnutrienttransportation(Horn et al., 2009). Therefore, interruption ofintestinalhomeostasisleadstochangesinthemucusbarrierthatprotectstheentericmucosa.Anincreasein the entericmucosa permeabilitymay result ininflammatoryprocessesandinjuriestomucosacells(Dharmaniet al.,2009).

Oneof themain features thatmake the broilerchicken so productive is the great capacity of itsintestinal epithelium to absorb nutrients (Oliveiraet al., 2000).According to Cera et al. (1988),the absorption capacity of the small intestine isproportionaltothenumberandsizeoftheintestinalvilli and the surface area available for absorption.Thus,adequateandfastweightgainisrelatedtothemorpho-functionalintegrityoftheintestinalmucosa,especiallyinthesmallintestine(Furlanet al.,2001).Suchintegrityiscrucialtoenablethebirdtoimproveitsdigestionandabsorptionprocessesand,therefore,itsperformancepotential.

Damagetointestinalmorphologyisoneofthefirstconsequencesofstress (Cosen-Binkeret al.,2004)anditdependsonthestressorintensityandduration.Acutestressreducesenterocyteproliferationinchicks(Uni et al., 2001) and reduces ileum crypt depthwithoutchangingvillusheightorthevillus/cryptratio(Burkholderet al.,2008).Nevertheless,Marchiniet al.(2011)foundnochangeinenterocyteproliferation

in broiler chickens subjected to daily cyclic heatstress(from12-13hat38°Cbetweenthe1standthe27thdayandat40ºCbetweenthe28thandthe42nd day).Chronicheatstressledtoa19%reductioninvillusheightand26%reductioninjejunumweight(MitchellandCarlisle,1992).However,nochangeswere observed in villus and crypt structureswhenbirdsweresubjectedtocyclicheatstress(36°Cfor12h,betweenthe35thandthe41stdayofage),afactthatcouldbeattributedtothefastre-epithelializationof intestinalmucosa (Quintero-Filhoet al., 2010).Actually,itdemonstratedthattheepithelialstructureisreplacedinlessthan36hafterthestressconditionisremoved(Burkholderet al.,2008).

Reductionoffeedintakeasaconsequenceofheatstress(Quintero-Filhoet al.,2010)isoneofthefactorsthatmaychangeintestinalmorphology,forinstance,byreducingvillusheightandcryptdepth(Burkholderet al.,2008)andbyreducingenterocyteproliferationinthesmallintestine,bothofwhichwoulddirectlyaffect the capacity to digest and absorb nutrientsnecessary formaintenance andproduction (Uniet al.,2001).AccordingtoSellet al.(1985),cryptdepthreductionalongwithincreasedmucussecretioncouldreduceabsorptioncapacityoftheintestine.

It is important to highlight that feed intakereductionisnottheonlycauseofgrowthratedecreasein broilers reared under high room temperature.Geraert et al. (1996) subjected broilers to heatstressandfedotherbirds,keptunderthermoneutralconditions,withthesamefeedintakeasthoserearedunder heat stress.They concluded that feed intakereductionbybroilerskeptunderhigh temperatureswas responsible for approximately 50%of growthreduction.Theseauthorsalsoreportedthatbroilersreared under high temperature showed changes inproteinmetabolism(adecreaseinproteinsynthesisoranincreaseinitscatabolicrate),whichcanalsocontributetoareductionofthegrowthrate.

Withregard to lowerenterocyteproliferation inbroilers rearedunderhigh temperatures,Gaoet al. (2013)reportedthatheatstressinducesprogrammedcelldeath(apoptosis) in thesmall intestineofrats,andthisismediatedbytheAKTsignallingpathway.TheAKTisaserine-threoninekinasefirstdescribedas an oncogenewithin themouse leukaemia virus

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(Bellacosa et al., 1991) and it is implied in cellgrowthandsurvival(Frankeet al.,2008).Itinhibitsthepro-apoptosiseffect(Dasariet al.,2008)inducedbyheat stress andpromotescell survival (Dattaet al., 1997). It represses apoptosis by inhibiting theactivitiesofpro-apoptoticproteins(Gaoet al.,2013).Gao et al.(2013)reportedthatduringheat-inducedapoptosis,moreAKTswere activated, showingincreasedphosphorylation.Theseauthorsobservedthat two hours after heat exposure there was ahigher level ofAKTphosphorylation in rat IEC-6cell linethatcoincidedwithamarkedreductionofapoptosis.TheauthorsalsosuggestedaneffectofAKTonsuppressingapoptosistriggeredbyheatstressandthereforeprotectsvilliepithelialcellsfromapoptosisatcertainpointsintheapoptoticprocess,promotingcellsurvival.Whentheyreplicatedtheirstudyin vitro, theresultsweresimilartothein vivo ones.Therefore,theauthorsconcludedthathightemperatureinducesintestinalcelldamageregardlessoffeedintake.

Redirection of blood flow takes place duringexposure to heat stress.Heat stress significantlyreducesdigestivesystemcapillarybloodflowtoinnerorganssuchastheupperrespiratorytract,tothebrainof layinghens (Wolfensonet al., 1981)and to theskin(Cronje,2007).ItcanresultingutischemiaandincreasedROSproductionduetoinsufficientoxygensupply(Cronje,2007),whichmayinduceexcessiveepithelial cell apoptosis, shedding of intestinalepithelialcells(Gaoet al.,2013),andreducednutrientabsorption(Kohnet al.,1993).

It has also been demonstrated that heat stressincreases lipid peroxidation.Bagchi et al. (1999)reported that acute and chronic stress exposureincreasesmucosal lipidperoxidation, cytochromecreduction, and hydroxyl radical production in ratintestinalmucosa.Suchresultsindicatethatoxygenfree radicals, including superoxide anions andhydroxylradicals,areinvolvedinthepathogenesisofacuteandchronicstress-inducedgastrointestinalinjury,andcanresultinlipidperoxidation.

Highbodytemperatureduetoheatstress(Marchiniet al.,2007)caninducemetabolicchangesinvolvedwithoxidativestressinduction.AccordingtoIsmailet al. (2013),heat stress increases lipidperoxidation—highvaluesofmalondialdehyde (MDA)—and

depletesthebirdantioxidantcapacity,asevidencedbydecreasedcatalase(CAT),glutathione-S-transferase(GST), and superoxide dismutase (SOD) activityinbroilers.Altanet al. (2003) concluded thatheatstressincreasedlipidperoxidationduetoincreasedfreeradicalgeneration,asindicatedbytheincreasedMDAconcentrationinbroilersexposedtoheatstress.AccordingtoAltanet al.(2000),oxidativestresscanbeconsideredpartofthebroilerchickenresponsetoheatexposure.

Effects of heat stress on broiler chicken performance

Between 1956 and 2000, selective breeding ofbroilerchickensforfastgrowthandmoreefficientfoodconversion resulted in significantproductivitygainsforthepoultryindustry.Themostremarkablechangesobservedinthemodernbroilerchickenwhencomparedtoitsancestorsarebettergrowthrates,heaviercarcassweight, andgreater yield of breastmeat. In 2000,broilerchickens reached1.82Kgbodyweightat32daysofage.In1966,achickenneededapproximately60daystoattainthesameweight,andittook84daysin1956(Havensteinet al.,2003a;2003b).Therefore,improvements in genetics, nutrition, and breedingmanagementover the last fewdecadeshave resultedinapproximatelyone-thirdofthetimeandthreetimeslessfoodforbroilerstoreach1.85Kg.Geneticincreasewasresponsiblefor85to90%increaseingrowthweight(Havensteinet al.,2003b).

However, fast growth comes along with adisproportionatedevelopmentof the cardiovascularandrespiratoryorgans(Havensteinet al.,2003a).Thisimpairstheabilitytodealwithheatstresschallenges(Yahavet al.,2005),sincebirdsselectedforhighgrowthratesalsopresenthighermetabolicratesandgeneratemoreendogenousheat(Thiruvenkadanet al.,2011).

The changes introduced by domestication andgeneticselection—toimprovebroilerresponsetoacuteheatstress(36°Cfor3hours)—weredescribedbySoleimaniet al.(2011).Thoseauthorsreportedagreatersusceptibilitytoheatstressinthefastgrowing,geneticallyimprovedCobbbreedwhencomparedtotheunimprovedRedJungleFowl(RJF)andVillageFowl (VF) breeds.They investigated birds of the

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sameage(30daysold)weighing150g(RJF),354g(VF)and1432g(Cobb),andalsobirdswiththesamebodyweight(930g)at150(RJF),90(VF),and22(Cobb) days of age.TheCobb chickens exhibitedgreater heterophil: lymphocyte ratio, greater bodytemperature, lowerHsp70 levels in the brain, andlowercorticosteroneconcentrations.Theyconcludedthat domestication and genetic improvement forgreaterweightgainandfasterdevelopmentresultedinphysiologicalchangesinthechickenbreedscurrentlyused in the poultry industry.These changes led tomoresusceptibleandlessresistantindividualswhencomparedwithunimprovedbreeds.

Duringheatstress,thereisblockageoftheappetitecenterlocatedinthehypothalamus.Consequently,thereisfeedconsumptionreduction(Akşitet al.,2006)andthebirdssufferdeficienciesinmany,ifnotall,nutrientsessentialtotheirperformance(Donkoh,1989).

Feedconsumptionreductionisachangeindietarybehavior associatedwith productionmechanismsandheatloss.Thechangeisnecessarytodissipatetheheatgeneratedbydigestionandenergymetabolism(Veldkampet al.,2005).Thus,feedconsumptionofchickenssubjectedtoheatstressbetween21 and40daysofagewasinverselyproportionaltotheincreaseintheroomtemperatureasthetemperaturewasraisedfrom25to31°C(Estrada-Parejaet al.,2007).

Asthestressperiodpersists,itsnegativeimpacton feed intake getsworse.Birds raised at a roomtemperatureof32°Chadafeedintakedecreaseof14.7%between1and21daysofage,andadecreaseof22%between1and49days.Therefore,thereis2.2%decreaseinfeedintakeperdegreecentigradeincrease in room temperature above the thermalcomfortzone(Oliveiraet al.,2006).

Inadditiontotheprolongedstressperiod,intensityof the high temperatures also affects feed intake.Al-Fataftah andAbu-Dieyeh (2007) subjectedbroilers daily to three constant temperatures: 25(thermoneutrality), 30, and 35 °C.According tothese authors, therewas 12.4% feed consumptionreductioninbirdskeptat30°Cand28%reductioninthosekeptat35°Cwhencomparedwithbirdskeptatthermoneutrality(25°C).Therefore,asbroilerswere

challengedbyhigherroomtemperatures,greaterfeedintakereductionwasobserved.

Temperatureincreaseandheatstressdurationmayalsocausenegativeresponsesinbodyweightgain,and these responses also dependon broiler breed.Weightgainlossesmayrangefrom13.9%inbroilerchickenskeptat32°Cfor24hbetween1andthe49daysofage(Oliveiraet al.,2006),to44%inIsaVedettechickenskeptat35°Cfor24hbetween28and56daysofage(Al-FataftahandAbu-Dieyeh,2007).Theseauthorsconcluded that lowerweightgainathightemperaturesresultfromfeedintakereduction,digestion inefficiency, and impairedmetabolism.Azadet al.(2010)alsoconcludedthateitherchronicorcyclicheatstresscouldreducebodyweightgainduetoreductionsinbothfeedconsumptionandfeedefficiency.

Reports about feed conversion andmortality inbirdssubjectedtoheatstressarecontroversial,andresponsesdependonstressorintensityandduration.Estrada-Parejaet al.(2007)foundnochangesinfeedconversionofbroilerchickenssubjectedtoheatstress(31°C)for24hbetween21and40daysofagewhencomparedtothoseraisedinthermoneutrality(25°C),despitea6.9%reductioninweightgain.However,Akşitet al.(2006)reportedpoorerfeedconversioninbroilerchickenskeptat34°Cand60%relativehumidityfrom21to49daysofage,whencomparedtothosekeptinthermoneutrality.CooperandWashburn(1998)reportedthatmortalitydidnotchangeinRossmalebroilers subjected to32°C for24hbetween28and49daysofage.However,whenAl-FataftahandAbu-Dieyeh (2007), evaluated performanceof broilers subjected to heat stress, they verifieda significant increase inmortality of IsaVedettechickensraisedat35°Cbetween4and8weeksoflife.LossesbymortalityinBrazilduetoexcessiveheatinchickenraisingshedscorrespondsto10%ofthetotalproductionthroughthehottestmonthsoftheyear(Aradaset al.,2005).

Exposure to high room temperature is a causedecline in broiler production efficiency andmeatyield.High environmental temperatures also harmbreast,thigh,anddrumstickmeatyield.Thisnegativeeffectisworsenbyanincreaseinrelativeairhumidity(Oliveira et al., 2006).These changes take place

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because heat stress can stimulate reactive oxygenspecies (ROS) production, particularly superoxideformationandoxidativedamage.Heat-inducedROSformationmaybethecauseofdamagesintheskeletalmuscle(Azadet al.,2010).Hightemperaturesalsocausechangesinenergy,protein,andfatretentioninthebody,andcausephysiologicalchangesinthedevelopmentoforgansandcarcass(Baldwinet al.,1980).

Final considerations

Ourcurrentunderstandingoftheeffectsofheatstress on broiler chicken performance shows thatproduction efficiency declines under heat stresswhen compared to production efficiency underthermoneutralconditions.

Accordingtotheexistingevidence,itisreasonableto assume that broilers under heat stress developan acid-base imbalance and increased plasmacorticosteroid levels. Furthermore, heat stress cangenerateoxidative stressandgutflow impairment,andcandamagetheintestinalepithelium.

Ourchallengeistodocumentthelinkbetweentheseconceptsandbroilerperformance.Understandingtheeffects of heat stress on the physiology of broilerchickens has been the purpose of recent studies.Further investigations into this subject will bevaluablenotonlyfortropicalregions,butalsobecauseofclimatechangescausedbyglobalwarming.

Conflicts of interest

Theauthorsdeclaretheyhavenoconflictsofinterestwithregardtotheworkpresentedinthisreport.

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