Immersion Pulmonary Oedema and Alveolar Hemorrhage in a Long

Immersion Pulmonary Oedema and Alveolar Hemorrhage in a Long

Open Journal of
Clinical & Medical
Case Reports
Volume2(2016)
Issue15
ISSN2379-1039
ImmersionPulmonaryOedemaandAlveolarHemorrhageina
Long-DistanceAsthmaticSwimmer:ACaseReport
JulieTurmel;AnnieLemelin;PaulPoirier;Louis-PhilippeBoulet*
*Louis-PhilippeBoulet
ResearchCenteroftheQuebecHeartandLungInstitute,DepartmentofPulmonology,LavalUniversity,
Canada.
Phone:418-656-4747,Fax:418-656-4762;Email:lpboulet@med.ulaval.ca
Abstract
Thisreportdescribesrecurrentimmersionpulmonaryoedemaassociatedwithalveolarhemorrhageina
femaleasthmaticswimmerduringalongdistancecompetitioninopenwater.Duringtherace,shehad
repeated haemoptysis, shortness of breath and thoracic pain. A chest radiograph showed alveolar
in iltratesintherightupperlobe.Anelectrocardiogramshowedrightatriumhypertrophyandarightaxis
suggestiveofpulmonaryhypertension.Acomputedtomographypulmonaryangiographydemonstrated
diffuse ground glass opacities. A bronchoalveolar lavage showed large numbers of red blood cells,
neutrophilsandhemosiderin-ladenmacrophages,suggestiveofalveolarhemorrhage.Chestradiograph,
taken 4 days after the competition, showed an almost complete resolution of in iltrates. This report
illustratesthevariouscomponentsofthisprobleminsomecompetitiveswimmersandthepotential
contribution of unstable asthma and it also stresses the need to recognize this entity to provide
appropriatemanagement.
Keywords
Immersionpulmonaryoedema;asthma;exercise-inducedbronchoconstriction;swimmers
Abbreviations
BAL:BronchoalveolarLavage;ECG:Electrocardiogram;EIB:Exercise-inducedBronchoconstriction;
FEV1:ForcedExpiratoryVolumeinonesecond;FVC:ForcedVitalCapacity;LTB4:LeukotrieneB4;IPO:
ImmersionPulmonaryOedema;L:Liter;PC20:ProvocativeConcentrationofMethacholineinducinga
20%fallinFEV1;Vo2max:MaximalOxygenConsumption
Introduction
Immersioninwater,atthethoraxlevel,canprovokenumerousphysiologicaleffects.First,the
exertedwaterpressureincreaseshydrostaticpressurefromvenousandlymphaticcompression,which
leadstoaredistributionofthebloodfromthelegstothethorax,increasingcentralbloodvolume.This
increasedbloodvolumeinducesariseinatrialandpulmonaryarterialpressures,increasesrightandleft
ventricularstrokevolumesaswellasthecardiacoutput.
Waterpressurecompressesthethoraxaffectingthepulmonarysystem.Indeed,adecreaseof
about 10% of chest circumference increases airway resistance and decreases residual volume,
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expiratory lows, expiratory reserve volume, and vital capacity [1-3]. A slight decrease in diffusion
capacityalsooccursduetopulmonaryvascularbeddistention[4].Incoldwater,vitalcapacitywillfurther
decreaseduetoperipheralvasoconstriction,whichfurtherincreasescentralbloodvolume.Chestand
lungcompliancealsodecreaseasaconsequenceofwaterpressure[5].Theoutcomeofalltheseeffectsis
anincreasedbreathingburdenfortheswimmer[6].
Furthermore,immersionincreasesblood lowtothekidneysandthecreatinineclearance.Sodium
excretion is increased following atrial natriuretic peptide release due to atrial distension. Potassium
excretionisalsoincreasedwhilealdosteroneproductionisdecreased,resultinginincreaseddiuresis.
Finally,immersioncanreducethirst.Altogether,theseeffectscanpromotedehydration.
Intense exercise increases cardiac output raising pulmonary capillary pressure which, during
immersion,causescentralredistributionandbloodpooling[7].Thisinadditiontotheeffectofthebody
proneorsupinepositionincreasescardiacpreload[8].Theperipheralvasoconstrictionresultingfrom
coldwaterimmersionincreasescardiacpreloadandafterload,aswellaspulmonaryarterypressure.
Immersionpulmonaryoedema(IPO)occursrarelyinhealthyindividuals,buthasbeenreported
with an increasing frequency in recent years, particularly in scuba divers, free divers [9-13], and
enduranceswimmers[14-17].IPOisconsideredtooccurin1.4-1.8%ofparticipantsinanopenwater
swimeventandhaemoptysiscanbeobservedinover50%ofallcases[18-19].Thisconditionisgenerally
associatedwithcoldwaterimmersion[20,21],butalsowithavarietyofconditionsincludingswimming
inwarmwater(29°C),usingawetsuitordrysuit,beingimmersedindepthsaslowas2.9meters,or
performinganendurancesurfaceswim[21].Clinicalsymptomssuchasdyspnoea,coughandpinkish
sputumusuallyresolvewithin24hours.Follow-upchestradiographsandechocardiogramsareusually
normal,butone-thirdofpatientswillhaverepeatepisodes[18].
AreviewonIPOshowedthatin60casesanalyzed,67%weremaleandhadameanageof36years
(range 18-61 years) [21]. Pre-existing medical conditions were present in 16%, arterial systemic
hypertensionbeingthemostcommon(5cases)whileonly2reportedhavingasthma.In22%ofthecases,
subjectshadapriororrecurrentepisodeofIPO.SomereportsfoundasimilarprevalenceofIPOinboth
sexes [22,23], but recent studies reported an increased prevalence of pulmonary edema in women
[24,25].
Thisreportpresentsthevariousclinical,imaging,andbronchoalveolarlavagefeaturesofacaseof
immersion pulmonary oedema associated with alveolar hemorrhage in a young asthmatic female
swimmerduringalongdistancecompetitioninopenwater.Wediscussthemechanismthatcouldleadto
thiscomplicationofswimming,particularlyinasthmaticsubjects.
CasePresentation
On July 2013, a 23 year-old non-smoker female swimmer experienced acute haemoptysis,
dyspneaandthoracicpainduringafreeopenwaterswimmingcompetitionnamed"Traversé eduLacStJean", a 32 km swimming race with a duration of 7 to 8 hours. The water temperature during this
competition was between 17-21°C (63-70°F). She has had asthma since childhood, has experienced
exercise-inducedasthma-likesymptoms,andhashadaconcentrationofinhaledmethacholinecausinga
20% decrease in the forced expiratory volume in one second (PC20) of 5.4 mg/ml (May 2013). She
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reported a respiratory tract infection in the days preceeding the race. Her medication included
ciclesonide200gwith2dailyinhalations,inhaledsalbutamol100gondemand,andpregabalin150mg
onceaday.Despitereportingamildexacerbationofasthmasymptoms4dayspriortothecompetition,
shehadnottakenherasthmamedication.Shereporteddrinkingapproximately4liters(L)ofwaterand
sportsbeveragestheeveningbeforeand1.5Lthemorningofthecompetition.Duringtherace,at20
minuteintervals,shedrankaround0.5Lofeitherasportsbeveragethatcontainedelectrolytes,orhot
chocolate.
Twoandahalfhoursafterthebeginningofthecompetition,atthetwelfthkilometer,shepresented
acute dyspnea, right thoracic pain, and haemoptysis. She reported no water aspiration. Despite the
persistenceofthesymptoms,she inishedthecompetitioninsevenhoursand41minutes,afterwhichshe
wasrapidlybroughttotheregionalhospital'semergencyroomformedicalevaluation.Itshouldbenoted
that the patient had reported a previous episode of mild haemoptysis, which had quickly resolved
followingthepreviousyear'ssameevent.
Onherarrivalatthehospital,thepatientwasalert,butdyspnoeic.Atthistime,herbloodpressure
was114/75mmHg,heartratewas83bpm,bodytemperaturewas36.3°C(97.3°F),andoxygensaturation
was87%.Theinitialphysicalexaminationrevealeddiffusecracklesonpulmonaryauscultationanda
prolonged expiration time suggestive of increased airway resistance. Blood neutrophil count was
9
9
increased(12.8x10 /L).Hemoglobinwas142g/Landplateletcount291x10 /L.
A chest radiograph showed alveolar in iltrates in the right upper lobe (Figure 1). An
electrocardiogram(ECG)showedarightatriumhypertrophyandarightaxisdeviation,suggestiveof
pulmonaryhypertension.Acomputedtomographypulmonaryangiographydemonstratedgroundglass
opacitiespredominantwithintherightupperlobeofthelung,butalsointheleftsuperiorlobe,themiddle
lobe,thelingula,andintheinferiorlobes(Figure2).Thiswascompatiblewithalveolarhemorrhage.
There was no pulmonary embolism, pleural, or pericardial effusion. The patient was considered too
dyspnoeictoperformaspirometry.Initially,shewastreatedwithinhaledsalbutamolandintravenous
methylprednisolone.Thenextday,shewastransferredtotheInstitutuniversitairedecardiologieetde
pneumologiedeQuébec,atertiarycarecenter,forfurtherevaluation.
A bronchoscopy was performed and the bronchoalveolar lavage (BAL) was increasingly
6
haemorrhagicfromthe irsttothethirdspecimenobtained.TheBALshowed26.0x10 cells,including
redbloodcells,33%neutrophils,andthepresenceofhemosiderin-laddenmacrophagessuggestiveof
alveolarhemorrhage.Exhaustivelaboratorytestsincludingantinuclearantibodies(C-ANCA,P-ANCA,
anti-ENA)andcryoglobulinemiawereallnegative,aswereanti-glomerularbasementmembrane(antiGBM), anti-double-stranded DNA antibody (anti-dsDNA), complement proteins (C3 and C4),
immunoglobulins(IgG,IgA,IgM),andserumproteinelectrophoresis.High-sensitivityC-reactiveprotein
(CRP-hs)was19.49mg/Land ibrinogen3.2g/L.Theurineanalysiswasnormal,aswerecreatinine,urea,
electrolytes, and complete blood count. These investigations excluded various conditions including
vasculitis.Twodaysafterthecompetition,anechocardiogramshowedanabnormallydilatedleftatrium
of 44ml/m2 (normal < 28; mild dilation 29-33; moderate 34-39; severe > 40ml/m2) and a tricuspid
regurgitation(1/4).Pulmonarypressurewascalculatedat25-30mmHg.AcontrolECGwasdonetheday
afterthecompetitionandshowedacompleteresolutionofsignsofrightatriumdilatationandrightaxis.
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Thissuggestedtransientpulmonaryhypertension.
Thespirometry,completed3daysaftertherace,showedaforcedexpiratoryvolumeinonesecond
(FEV1)of3.36L(90%ofpredicted),aFEV1/forcedvitalcapacity(FVC)of80%,andnormallungvolumes&
carbonmonoxidediffusingcapacity.Inthefollowingmonth,theFEV1furtherincreasedat3.92L(106%of
predicted);theairwayresponsivenesswasnormal(PC20>16mg/ml;andnofallinFEV1postEucapnic
VoluntaryHyperpnea),probablyre lectingtheintenseasthmatreatmentinitiallyreceived.Whenseen
onemonthlater,sheusedinhaledciclesonide200gtwoinhalationsdailyandrarelyinhaledsalbutamol.
Haemoptysishadpersistedfor48hoursfollowingthecompetition,butresolvedrapidly.Dyspnea
improvedgraduallyover48hours,butsheremainedwithcoughandchesttightnessduringexerciseuntil
December 2013. A chest radiograph taken 4 days after the competition showed an almost complete
resolutionofin iltratesandwasnormalatonemonth.Shereportednootherepisodeofhemoptysisor
exercise-induceddyspneainthefollowingmonths.
Discussion
IPOfollowingswimmingisanunusualeventthathasbeenreportedmorefrequentlyinrecent
years[21,25].ThecausesofIPOarenotcompletelyunderstoodandseveralmechanismsmaybeinvolved.
Moreover,itisnotcurrentlypossibletopredictwhoisatanincreasedriskofdevelopingthiscondition,as
manyfactorscantriggerthisphenomenon.Asthereisnospeci icdiagnostictestforthiscondition,the
diagnosismainlystemsfromtheclinicalhistory,biologicalassessment(bloodgases,cardiacenzymes,
blood&urinecatecholamine's),chestradiographorcomputedtomography(CT-scan)(lungin iltrates),
andcardiacechography[26].
Inhealthysubjects,acombinationoffactorsincludingintenseexercise,immersion,coldwater,
and over hydration can trigger a transient increase in the pulmonary capillary pressure resulting in
oedemaandhemoptysis.Inthisreport,thecombinationofapreviousepisode,uncontrolledasthma,cold
waterandtakingmedicationthatpromote luidretentionmaybeinvolvedinthepulmonaryoedemaand
alveolarhemorrhageofthisyoungasthmaticfemalelong-distanceswimmer.
Shehadreportedapreviousepisodeofslighthemoptysisfollowingthesamecompetitiontheyear
before, suggesting a predisposition to this phenomenon. However, she reported no episode during
training between the two events. This can be explained by the fact that the training sessions were
performedinwarmerwatertemperature,atlowerintensity,shorterdistanceandsmallerwaveswhich
representconditionsthatarenotasrigorousastheeventitself.Furthermore,shehadahistoryofasthma,
butpresentednootherpre-existingmedicalconditionassociatedwithpulmonaryoedema.Afewdays
beforethecompetition,shepresentedsymptomsofthecommoncold,whichcouldhaveaffectedher
asthma,butinspiteofthis,shedidnotuseherasthmamedicationatthistime.Thecombinationofa
prolongedimmersionincoldwaterandintenseexerciseinunstableasthmacouldhaveproduceddamage
tothecapillary-alveolarbarrier[21,27].
During strenuous exercise, hyperventilation induced dehydration and heat loss of the airway
mucosamaytriggerbronchoconstrictionandmucosalhypersecretion[28].IPOcanthenbetriggeredby
changes in respiratory mechanics. The forced inhalation against resistance, such as during a
bronchospasm,mayinduceshearforcesintheairwaywallwithmechanicalandin lammatoryinjuriesof
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thebronchoalveolarstructures[18,22,29]andmaypromote luidleakageoutofthecapillariesandinto
the alveoli. Haemoptysis, observed in the present case, probably re lects such mechanical strain of
capillary-alveolarnetworkinducedbystrenuousexerciseandbronchoconstriction[18,30].Moreover,
thevasculatureofthelaminapropriahasbeenshowntobemoreprominentinasthmaticairwaysthanin
normalcontrols[31].Thebronchialcirculationplaysanimportantroleintheregulationofheatand
water loss in the airway, thus increased vascularity may predispose to exercise-induced
bronchoconstriction(EIB)[32].
However,pulmonaryoedemawithacuteasthmaisanuncommoncondition[33].Thenegative
pleuralpressureandhyperin lationinasthmacanincreasethehydrostaticpressureofthepulmonary
vasculatureinducingdamagetopulmonarycapillariescausingleakageofplasmaproteinsandredcells
intotheinterstitialspace[34].Intenseexercisealsocancauseanincreaseinhydrostaticpressurebecause
ofthelarge illingpressuredemandedbytheleftventricletodevelopthenecessarycardiacoutput[35]
addinganadditionalstressonthewallofthecapillary,whichcaneventuallybreakcollagen ibersthatare
responsible for wall strength. Exercise-induced pulmonary hemorrhage was irst described in race
horses[36,37],butevidenceofincreasedredbloodcellsinbronchoalveolarlavage luid,increasedlung
opacities, and reduced pulmonary capacity was observed in triathletes, following a competition
[17,38,39].
Indeed,itseemsthattheintegrityoftheblood-gasbarriercanbealteredinathletesatintense
levelsofexercise.Thereareseveralreportsofhemoptysisand/orhemorrhagicpulmonaryoedemain
eliteathletes[15,17,38,40,41].Thecombinationofhemoptysis,oedemaandrapidrecovery(24hours)
stronglysuggestsstressfailureofthepulmonarycapillaries[42].Hopkinsetal.[39]showedthatcyclists
hadhigherconcentrationsofredbloodcells,totalprotein,albumin,andleukotrieneB4(LTB4)inBAL luid,
followingamaximalexercise(6to8minutesat90%VO2max),comparedwithsedentarysubjectswhodid
notexercise.ExceptforLTB4,theabsenceofactivationoftheproin lammatoryprocesssuggeststhatthe
mechanismforalteredblood-gasbarrierwasmechanicalstress.TheincreaseinLTB4ispossiblydueto
the activation of alveolar macrophages resulting from the disruption of alveolar epithelial cells [42].
However,followingsubmaximalexercise(1hourat75-80%ofVO2max),thereisnodifferencebetween
athletes and controls, suggesting that submaximal exercise is not suf icient to impair the blood-gas
barrier[43].
IPOmightresultfromamismatchbetweenrightandleftstrokevolumes,e.g.alimitedincreasein
leftventricularstrokevolumecomparedwitharelativelygreaterriseinrightventricularstrokevolume
duringintenseexercise[19].However,healthyindividualsshouldbeabletoadapttosuch luidshift[21].
Thelymphaticsystemmaybeoverloadedduetoincreased low,but,ontheotherhand,thelymphatic low
maybealsoreducedfollowingrespiratorypatternchangesandsupinepositionofswimming[44].Inthis
case, taking pregabalin may have contributed to increased circulatory volume, as it promotes luid
retention.
Inthecasereportedhere,coldwater,prolongedexercisedurationanditsintensitymayhavealso
promotedIPO.Thetemperatureofthewaterwasaround17-21°C(63-70°F)andtheswimmerworean
openwaterfullbodylonglegopenswimwear,whichprovidesnocoldprotection.Anincreasedcardiac
preloadfromimmersionandasupinepositioninswimmersmaybeaugmentedbywearingtight- itting
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wetsuitsandincreaseperipheralvasoconstrictionduetocold,allleadingtoanevengreaterincrease
incentralshiftofthebloodvolume[16,17,19].
Overhydrationcanalsobeatriggerforpulmonaryoedemabyincreasingpulmonaryvascular
permeabilityandpressure[45,46].Alterationin luid-electrolytebalancemakesthebloodhypotonicand
luiddiffusesacrossanosmoticgradientintothebraintocompensateforhyponatremia[47,48].Several
reportshaveconsideredpre-swimoverhydration(e.g.5Lconsumed2hpriortoswimming)asarisk
factor of IPO [16,17]. The recommendations from the 2008 International Exercise-Associated
HyponatremiaConsensusDevelopmentConferencestatesthatathletesshoulddrinkamaximumof0.4to
0.8L/hduringanevent[49].Inthepresentcase,theswimmerhadnotbeendrinkinglargevolumesof
beveragesbeforethecompetition(1.5Linthemorningbeforetherace),butshehadtakenpregabalin
whichpromotes luidretention.However,shehadanormalnatremia(138mmol/L)onherarrivalatthe
hospital.
PredictionofrecurrentIPOinanathletewithapreviousepisoderemainsdif icult.Whetherornot
anathleteshouldreturntodivingorswimmingafteranepisodeofIPOshouldbedeterminedonacaseby
case basis. The decision should be based on the physical condition, history of hypertension or
cardiovasculardiseaseandthetypeofexercisebeingconsidered.However,athletesshouldbeawareof
theapparitionofIPOsymptomsduringfutureexerciseandshouldstopiftheydevelopmarkeddyspneaor
haemoptysis.Currently,notreatmenthasbeenshowntopreventtheonsetofIPO,butsomeprecautions
canbetakenbyathletestoavoidsuchanepisode(Table1).Ensuringadequateasthmacontrolcould
reducethisriskasasthmaisoftenundertreatedinathletes.
Inthiscasestudy,theswimmercontinuedtotrainandcompetewithoutanyfurtherepisodeof
haemoptysisordyspneaduringthemonthfollowingtheIPOepisode.Herasthmawaswellcontrolled,
withadailyintakeofinhaledcorticosteroidsandherchestradiographremainednormal.Asthelongterm consequences of repeated IPO episodes are unknown, further studies are necessary to better
understandwhythisphenomenonoccursandtouncoverhowitcouldbeprevented.
Conclusion
Wereportthecaseofalong-distanceasthmaticswimmerwhohadevidencesofIPOandalveolar
hemorrhageduringalongdistanceswimmingcompetitioninopenwater.Inthiscase,itlikelyrepresents
asecondepisodecausedbyacombinationofprolongedswimmingincoldwater,uncontrolledasthma,
andmedicationfavoring luidretention.Thisreportreviewsthegeneralmanagementofthiscondition
andstressestheneedtoidentifythisprobleminathletes,whichcanmimicorbeassociatedwithasthma.
Acknowledgments
Wethanktheathletewhoconsentedforthepublicationofthiscaseandforhertimetoanswerthe
additionalquestionsandprecisions.
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Figures
Figure1:(28-07-20138h30am)Chestradiographshowedalveolarin iltrateswithintherightupperlobe.
Figure 2: (27-07-2013 6h14pm) Computed tomography pulmonary angiography demonstrated ground glass
opacitiespredominantwithintherightupperlobeofthelung,butalsointheleftsuperiorlobeandthemiddlelobe.
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Table
Potentialcontributorsorrisk
factorstoIPO
Potentialpreventivemeasures
Warm-upswimimmediatelybeforethecompetition
Exerciseinopenwater
Requestassistanceduringtheswimifsymptomsofunusual
breathlessnessorhemoptysisdevelop
Watertemperature
Avoidtrainingorcompetingincoldwater(16-30°C)
Acclimatetothewaterconditionsandtemperature
Chestwallcompression
Avoidusingaswimsuit/wetsuit/drysuitwhichistootight
PreviousIPOepisodes
Searchforriskfactors
Stopexerciseifsymptomsofunusualbreathlessnessor
hemoptysisoccur
Asthmaworsening
Ensurecontrolofasthmabeforethecompetition(perform
spirometry)
Viralrespiratoryinfection
Avoidhighintensityexercise
Speci icmedicalcondition
(Systemichypertension)
Ensuretreatmentandcontrolofthecondition
Overhydration
Avoiddrinkingtoomuchbeforetheevent(lessthan5Lin2
hours)
Limithydrationto400to800ml/hduringtheevent
Drinkbeveragesthatcontainelectrolytes(atleast10%ofNaand
K).Note:Na:Sodium,K:Potassium
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ManuscriptInformation:Received:March16,2016;Accepted:August06,2016;Published:August10,2016
AuthorsInformation:JulieTurmel1;AnnieLemelin1;PaulPoirier1,2;Louis-PhilippeBoulet1,3*
ResearchCenteroftheQuebecHeartandLungInstitute,DepartmentofPulmonology,LavalUniversity,Canada.
2
DepartmentofPharmacy,LavalUniversity,Canada.
3
DepartmentofMedicine,LavalUniversity,Canada.
1
Citation:TurmelJ,LemelinA,PoirierP,BouletLP.Immersionpulmonaryoedemaandlveolarhemorrhageinalongdistanceasthmaticswimmer:acasereport.OpenJClinMedCaseRep.2016;1147
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