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Ventilatory Response to Hypoxia of the 1-Day Old Chicken Hatchling After Prenatal Cold-Induced Hypometabolism - RPN 2013

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  This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institutionand sharing with colleagues.Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third partywebsites are prohibited.In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further informationregarding Elsevier’s archiving and manuscript policies areencouraged to visit:http://www.elsevier.com/authorsrights  Author's personal copy RespiratoryPhysiology&Neurobiology 188 (2013) 161–164 ContentslistsavailableatSciVerseScienceDirect Respiratory   Physiology   &   Neurobiology  journalhome   page:www.elsevier.com/locate/resphysiol Short   communication Ventilatory   response   to   hypoxia   of    the   1-day   old   chicken   hatchlingafter   prenatal   cold-induced   hypometabolism  Jacopo   P.   Mortola ∗ ,   Paula   Andrea   Toro-Velasquez DepartmentofPhysiology,McGillUniversity,3655PromenadeSirWilliamOsler,Montreal,QuebecH3G1Y6,Canada a   r   t   i   c   le   i   n   f   o  Articlehistory: Accepted22May   2013 Keywords: AvianembryosEmbryonicdevelopmentHypometabolismHypoxicventilatoryresponse a   b   s   t   r   a   c   t Sustained   prenatal   hypoxia   decreases   the   growth   and   metabolic   rate   of    the   embryo   andcauses   abluntedhypoxicventilatory   response   (HVR)   in   the   newborn.   The   most   likely   interpretation   isthat   the   sustainedhypoxic   stimulation   may   interfere   with   the   normal   prenatal   development   of    the   chemoreceptors.   How-ever,   we   wanted   to   consider   the   possibility   that   the   prolonged   hypoxic   hypometabolism   may   be   acontributing   factor.   Chicken   embryos   were   incubated   at   35 ◦ C( Cold   group,   N    =   14),   which   is   known   tolower   the   embryonic   oxygen   consumption   ( ˙ V  O 2 )by ∼ 30%   throughout   incubation,   or   at37.5 ◦ C( Controls , N    =   16).   Cold   incubation   delayed   hatching   by ∼ 2days.   The   1-day   old   hatchlings   had   normal   pulmonaryventilation( ˙ V  E ),   measured   bythe   barometric   technique,   and   oxygen   consumption   ( ˙ V  O 2 ),   simultaneouslymeasured   by   an   open   flow   methodology.   During   acute   hypoxia   ( ∼ 15%   or   ∼ 11%   O 2 )   the   hyperventilation(increase   in ˙ V  E /  ˙ V  O 2 ),the   hyperpnea   and   the   hypometabolism   were   almost   identical   between   the   twogroups   of    hatchlings.   We   conclude   that   a   sustained   decrease   inmetabolic   rate   during   the   embryonicperiod   byitself    does   not   carryobvious   consequences   onthe   newborn’s   resting ˙ V  E  and   HVR. © 2013 Elsevier B.V. All rights reserved. 1.Introduction Sustainedhypoxiainnewbornshasalong-termdepressanteffectontheventilatoryresponsetoanewacutehypoxicepisodelaterinlife.Thisphenomenon,bothinmammalsandbirds,hasbeenattributedtoaderangementofthenormalpostnataldevel-opmentofthechemoreceptors(reviewedinCarroll,2003;Mortola,2009).Whetherornotthesamecanhappenwithsustainedprena-talhypoxiaisdifficulttoestablishinmammals,becausematernalorplacentalresponsesbecomemajorconfoundingvariables.Howeverinchickenembryos,thedevelopmentofwhichisfreeofextra-embryonicfactors,hypoxiasustainedforthewholedurationorforonlythelastthirdofincubationresultedinabluntedhypoxicventilatoryresponse(HVR)ofthehatchling(SzdzuyandMortola,2007b;FernerandMortola,2009).Likepostnatally,theeffectof embryonichypoxiaonthehatchling’sHVRhasbeenattributedtoadisturbanceinthenormaldevelopmentofthechemoreceptors(Mortola,2009).Insupportofthisinterpretationwas   theobser-vationthatprenatalhypoxiahadtooccurduringthelastportionofincubation,thatis,atthetimeofthefunctionaldevelopmentofthechemoreceptors,whileitcarriednoconsequencesonthenewborn’sHVRifitoccurredonlyatearlierembryonicstages(FernerandMortola,2009).Thefactthatalsoembryonichyper-capnia(SzdzuyandMortola,2008)orhyperoxia(BavisandSimons, ∗ Correspondingauthor.Fax:+15143987452. E-mailaddress:  jacopo.mortola@mcgill.ca(J.P.Mortola). 2008;Mortola,2011b)causedsomepostnatalbluntingoftheHVR wereconsideredcompatiblewiththeideathatsustainedstim-ulationofthechemoreceptorsmay   interferewiththeirnormalprenataldevelopment.Prenatalhypoxialowersmetabolicrateandstuntsthegrowthofmanyorgansincludingthelungs(Mortola,2009).Thepossibilitythatthelowbirthweightbyitselfandindependentlyoftheprenatalhypoxiamay   contributetothebluntingofthenewborn’sHVRhasbeentestedexperimentallyanddismissed(Mortola,2010).Simi-larly,thepossibilitythatprenatalhypoxiamay   resultinanincreaseofthemechanicalimpedanceofthenewborn’srespiratorysystemhasbeendeniedbyspecificmeasurements(Mortola,2011a).Whatremainsuntestedisthepossibilitythattheprenatalconditionof sustainedhypometabolismbyitself,andindependentlyofhypoxia,may   contributetosomedepressionoftheneonatalHVR.Totestthispossibilitywe   incubatedtheembryosinnormoxiaatthesub-optimalbutviabletemperatureof35 ◦ C(insteadof37.5 ◦ C),whichlowerstheembryonicoxygenconsumptionbyabout30%through-outdevelopment(Mortola,2006).Theincubationofthechickenembryointhecoldoffersanexperimentalopportunitytotestthehypothesisthat,eveninabsenceofhypoxia,asustaineddepressionofembryonicmetabolismmaybyitselfcausesomebluntingofthenewborn’sHVR. 2.Methods FreshlylaidfertilizedeggsofWhiteLeghornchickens( Gallus gallus )wereobtainedfromalocalsupplier.Atmidday(embryonic 1569-9048/$–seefrontmatter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.resp.2013.05.023  Author's personal copy 162  J.P.Mortola,P.A.Toro-Velasquez/RespiratoryPhysiology&Neurobiology 188 (2013) 161–164  Table1 Characteristicsoftheeggsandrestingventilatoryvariablesofthehatchlings.IncubationconditionsNormothermia( Control s)Hypothermia( Cold ) P  Numberofhatchlings1614Fresheggweight(g) 61.1 ± 0.862.6 ± 0.6nsIncubationageathatching(days)20.3 ± 0.222.2 ± 0.2<0.001Postnatalage(h)20.0 ± 2.317 ± 1.2nsBody   weight(W)   (g)41.6 ± 0.741.2 ± 0.6nsAmbienttemperatureatstudy( ◦ C)37.8 ± 0.137.8 ± 0.1nsBody   temperature( ◦ C)40.1 ± 0.138.8 ± 0.3<0.001O 2  consumption( ˙ V  O 2 )(ml STPD /min) 0.8 ± 0.03 0.8 ± 0.03 ns˙ V  O 2 /W  ((ml/kg)/min) 20.1 ± 0.8 20.0 ± 0.6 nsTidalvolume(  l) 307 ± 22303 ± 17nsTidal   volume/bodyweight(ml/kg)7.4 ± 0.67.4 ± 0.5nsBreathingfrequency(min − 1 )64 ± 468 ± 4nsVentilation( ˙ V  E )(ml BTPS /min)18.7 ± 1.019.9 ± 0.6ns˙ V  E / W((ml/kg)/min)454 ± 26483 ± 13nsVentilatoryequivalent( ˙ V  E /  ˙ V  O 2 )22.8 ± 1.024.3 ± 0.6nsThe Cold groupwasincubatedat35 ◦ Cforthewholeincubation,hatchingincluded,insteadofthenormal37.5 ◦ C( Controls ).Valuesaremeans ± 1SEM. P  ,levelofthesignificantdifferencebetweenthetwo   groups(two-tailed t  -test).ns,nosignificantdifference( P  >0.05). day0,E0)theeggswereweighedandplacedintwo   stillairincubatorssetat60%relativehumidityandtemperatureof37.5 ◦ C( Controls , N  =16)or35 ◦ C(cold-incubatedgroup, Cold , N  =14).Frompreviousmeasurementsweknewthatincubationat35 ◦ Clowerstheembryo’soxygenconsumptionby ∼ 30%throughoutdevelopment,delayshatchingbutisstillcompatiblewithsurvival(Mortola,2006).Thecoldconditionwasmaintainedconstantforthewholeincubation,hatchingincluded.Thetemperatureandrelativehumidityinsidetheincubatorsweremonitoredbydataloggersanddirectlybyamercurythermometer.Experimentswereperformedbetween6hand24hafterhatching(usually ∼ 17–20h)toavoidtherapidlyoccurringphysiologicalchangesofthefirstpostnatalhours(Mortola,2009).Measurementsofbreathingpatternatrestandofthe ˙ V  E responsetohypoxiawereobtainedwithan‘adhoc’adaptationofthebarometrictechnique,whichallowedforsimultaneousmeasurementsofthebreathingpatternandoxygenconsumption(SzdzuyandMortola,2007a).Allaspectsofdataacquisition,anal-ysisandexperimentalprotocolwereaspreviouslyemployedinstudiesthatrequiredmeasurementsofventilatorychemosensitiv-ityinhatchlings(SzdzuyandMortola,2007b;FernerandMortola,2009;Mortola,2010).Briefly,theanimalchamberconsistedof twosectionsincommunicationwitheachother;thehatchlingwaspositionedinthesmallerofthetwo(“nest”compartment).Thetemperatureofthenestcompartment,monitoredbytelemetry,waskeptat ∼ 37.5 ◦ Cbyawaterbath;itaveragedabout9 ◦ Chigherthanthetemperatureoftheremainingportionoftheanimalchamber,tosatisfyaccuracyinthedeterminationoftidalvolume.Theanimalchamberhadfourleads;twowereusedfortherecordingofthebreathing-relatedpressureoscillationsandforthepressure–volumecalibrationofthechamber.Theremainingtwoleadswereforthepassageofasteadyflowofgasattheconstantrateof100ml/minunderthecontrolofaneedle-valveflowmeter.Thegasconsistedofairorofpremadehypoxicmixtures.CalibratedgasanalyzersmonitoredtheO 2  andCO 2  concentrationsoftheinflowingandoutflowinggases,afterwatervaporeliminationthroughadryingcolumn.Theoutputoftheanalyzers,togetherwiththebreathing-relatedpressureoscillations,temperatureandhumidityvalueswerecontinuouslyacquiredat100Hzwhiledis-playedonacomputermonitor.Thegasfractionalconcentrationsweremathematicallycorrectedfortheerrorintroducedbyarespi-ratoryexchangeratiodifferentfromunity(MortolaandBesterman,2007).Oxygenconsumption( ˙ V  O 2 ,ml/minatSTPD,standardtem-perature,pressureanddryconditions)wascalculatedfromtheflowandthechamberin–outdifferenceinO 2  concentration.Tidalvolume( V  T ,  l,atBTPS,bodytemperature,pressureandsaturationconditions),breathingfrequency(  f  ,breaths/min)andminuteventilation( ˙ V  E  =  f  × V  T ,ml/min)werecomputedfromthespirometricrecord(SzdzuyandMortola,2007a).Thehatchlingwas   leftundisturbedintherespirometerforatleasthalfhour.Then,datacollectionstartedinairfollowedbyhypoxia( ∼ 15%and ∼ 11%O 2  balanceN 2 ,20min   each).Dataof breathingpatternweretheaverageof150–200breathscollectedduringthelast3–5min   ofexposure,thatis,atatimewhengascompositionintherespirometerhasbeenstableforseveralmin-utes.Cloacaltemperaturewastakenasrepresentativeofbodytemperature( T  b )andwasmeasuredwithathinthermocoupledur-ingairbreathingandattheendofthehypoxicandhypercapnicruns.Dataarepresentedasmeans ± 1SEM.Foreachvariable,sta-tisticalcomparisonsbetween Controls and Cold weredonebytwo-tailed t  -test.Differenceswereconsideredstatisticallysignif-icantat P  <0.05. 3.Resultsanddiscussion Hatchingin Controls occurredafter20.3daysofincubation;in Cold ,incubationlastedabout2additionaldays(Table1).Thislongerincubationin Cold was   theexpectedeffectofthedecreasedmetabolismandgrowthrate(Mortola,2006).Infact,coldactslikeabrakeonembryonicgrowth,withoutcompromisingthemainte-nancecomponentofmetabolicrate(VleckandVleck,1987;Hoyt,1987);hence,throughoutincubation ˙ V  O 2  islessthansame-agecontrolsbutappropriatefortheweightoftheembryo(Mortola,2006).Liketheembryo,thechorioallantoicmembranegrowslessinthecoldkeepingitsfunctionaladequacytotheembryo’sgasexchangerequirements(Tazawa,1973).Asitisthecasefollowingincubationinhypoxia(SzdzuyandMortola,2007b),aftercold-incubationthehatchlingshavebodyweightssimilartocontrols(Mortola,2006;Table1).Thisisdue,partly,tothelongerincuba-tionandmostlytotheincorporationofanyremainingyolkintotheabdomen(Williams,1994).Innormoxia,noneofthemetabolicandrespiratoryvariablesdifferedsignificantlybetweenthetwogroups(Table1).Theonlyexceptionwas   T  b ,whichaveraged1.3 ◦ Clessin Cold ,presumablybecauseprolongedprenatalcoldlowersthedevelopmentofther-mogenesis(reviewedinMortola,2009).Thehyperventilatoryresponsetohypoxia(increasein ˙ V  E /  ˙ V  O 2 )andtheresponseofitstwocomponents(theincreasein ˙ V  E  and  Author's personal copy  J.P.Mortola,P.A.Toro-Velasquez/RespiratoryPhysiology&Neurobiology 188 (2013) 161–164 163 102030 Controls 2040 Cold-incubation O 2  % 10 15 20 10 15 20 V E /V O 2 .. V E ml/min . 0.20.40.60.81.0 V O 2 ml/min . 100200300400 V T ml 20406080100 f breaths/min 363738394041 Tb o C ** Fig.1. Pulmonaryventilation( ˙ V  E ),breathingfrequency(  f  )andtidalvolume( V  T ),oxygenconsumption( ˙ V  O 2 )andventilatoryequivalent( ˙ V  E /  ˙ V  O 2 )duringairbreathing(20.9%O 2 )andhypoxia( ∼ 15%and ∼ 11%O 2 )in1-dayoldhatchlings. Controls and Cold referstohatchlingsincubated,respectively,at37.5 ◦ C(  , N  =16)or35 ◦ C(  , N  =14).Symbolsindicatemeanvalues,barsare1SEM.*Statisticallysignificantdifferencefromcontrols( P  <0.05). thedropin ˙ V  O 2 )werealmostundistinguishablebetween Cold and Controls (Fig.1).Theonlyminor(andinsignificant)differ-enceswerefoundintheresponseofthebreathingpatternitself,whichtendedtobemorerapidandshallowerin Cold ;itisinter-estingthatthisisthepatternmostcommonlyadoptedbyadultmammalsandbirdsduringhypothermia,inanattempttoreducerespiratoryheatloss(MortolaandMaskrey,2011).Hence,theques-tionthatpromptedthestudy,whetherornotpersistentprenatalhypometabolismmay   lowertheHVRofthenewborn,receivedanegativeanswer.Thequestionwasmotivatedbythegeneralnotionthatthedevelopmentofneuralfunctionsiscontributedbythetypeofsensoryinformation.Withrespecttorespiratorycontrol,manystudieshaveshownthattheHVRundergoesdevelopmentalplas-ticityfollowingaprolongedmodificationofthegaseousstimuli,especiallywhenthishappensintheneonatalperiod(reviewedinCarroll,2003;Mortola,2009).Asfarasweknow,thisisthefirstexperimentalreporttoshowthatamajordisturbanceof metabolicratesustainedthroughoutthewholeprenataldevel-opmentbyitselfdoesnotcompromisethenewborn’sbreathingpatternatrestoritsresponsetoahypoxicstimulus.Previously,inneonatalrats,wefoundthatsustainedchangesinmetabolicratecausedbyprolongedcoldorbyundernutritioncarriednoconse-quencesonHVR(Sant’AnnaandMortola,2002,2003).Thenotionthatchangesin ˙ V  E  occurpromptlywithchangesinmetabolicrateisatenetofrespiratorycontrol,withinnumerableexperimentaldemonstrationsevenifthemechanisticbasisofitremainspoorlyunderstood(MortolaandMaskrey,2011).Thecurrentresultsindi-catethattheproperfunctionalityofthe ˙ V  O 2  −  ˙ V  E  couplingdoesnotdependonthelevelof  ˙ V  O 2  attainedthroughoutdevelopment.Presumably,thisindependencereflectstheimportanceofhavinganappropriategasexchangefunctionirrespectiveoftheindivid-ual’smetabolichistory.Fromtheperspectivethatmotivatedthisstudy,thecurrentresultsexcludethepossibilitythatthesustainedhypometabolism,byitself,may   contributetothebluntedHVRof thenewbornfollowingprenatalhypoxia,forwhichthealtereddevelopmentofthechemoreceptorsremainsthesoleplausibleinterpretation.  Acknowledgement PaulaA.ToroVelasquezwas   financiallysupportedbyaBEPE-FAPESPfellowship(ResearchInternshipabroad,SãoPauloResearchFoundation,Brazil). References Bavis,R.W.,Simons,J.C.,2008.DevelopmentalhyperoxiaattenuatesthehypoxicventilatoryresponseinJapanesequail( Coturnixjaponica ).RespiratoryPhysiol-ogy&Neurobiology164,411–418.Carroll,J.L.,2003.Plasticityinrespiratorymotorcontrol.Invitedreview:devel-opmentalplasticityinrespiratorycontrol.JournalofAppliedPhysiology94,375–389.Ferner,K.,Mortola,J.P.,2009.Ventilatoryresponsetohypoxiainchickenhatch-lings:adevelopmentalwindowofsensitivitytoembryonichypoxia.RespiratoryPhysiology&Neurobiology165,49–53.Hoyt,D.F.,1987.Anewmodelofavianembryonicmetabolism.JournalofExperi-mentalZoology1(Suppl.),127–138.Mortola,J.P.,2006.Metabolicresponsetocoolingtemperaturesinchickenembryosandhatchlingsaftercoldincubation.ComparativeBiochemistryandPhysiologyA   145,441–448.Mortola,J.P.,2009.Gasexchangeinavianembryosandhatchlings.ComparativeBiochemistryandPhysiologyA153,359–377.Mortola,J.P.,2010.Smallbirthweightdoesnotcompromiseventilatorychemosen-sitivityinthe1-dayoldhatchling.RespiratoryPhysiology&Neurobiology172,206–209.Mortola,J.P.,2011a.Respiratorymechanicsin1-dayoldchickenhatchlingsand   effectsofprenatalhypoxia.RespiratoryPhysiology&Neurobiology175,357–364.Mortola,J.P.,2011b.Metabolicandventilatorysensitivitytohypoxiainavianembryos.RespiratoryPhysiology&Neurobiology178,352–356.Mortola,J.P.,Besterman,A.D.,2007.Gaseousmetabolismofthechickenembryoandhatchlingduringpost-hypoxicrecovery.RespiratoryPhysiology&Neurobiology156,212–219.Mortola,J.P.,Maskrey,M.,   2011.Metabolism.In:Mitchell,G.S.,Milsom,W.K.,McCrimmon,D.R.,Dempsey,J.A.(Eds.),TemperatureandVentilation.Compre-hensivePhysiology–ControlofBreathing,vol.1.AmericanPhysiologicalSociety,Washington,DC,pp.1679–1709.Sant’Anna,G.M.,Mortola,J.P.,2002.Thermalandrespiratorycontrolinyoungratswithalteredcaloricintakeduringpostnataldevelopment.RespiratoryPhysiol-ogy133,215–227.Sant’Anna,G.M.,Mortola,J.P.,2003.Thermalandrespiratorycontrolinyoungratsexposedtocoldduringpostnataldevelopment.ComparativeBiochemistryandPhysiologyA134,449–459.
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