www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Does
the
reduction
of
inferior
turbinate
affect
lower
airway
functions?
夽
Ozlem
Unsal
a,∗,
Mehtap
Ozkahraman
a,
Mufide
Arzu
Ozkarafakili
b,
Meltem
Akpinar
a,
Arzu
Yasemin
Korkut
a,
Senem
Kurt
Dizdar
a,
Berna
Uslu
Coskun
aaSisliHamidiyeEtfalTrainingandResearchHospital,ClinicofOtorhinolaryngology,Istanbul,Turkey bSisliHamidiyeEtfalTrainingandResearchHospital,ClinicofPulmonaryDiseases,Istanbul,Turkey
Received31July2017;accepted16October2017 Availableonline6November2017
KEYWORDS Acousticrhinometry; Turbinates; Hypertrophy; Spirometry; Respiratorysystem Abstract
Introduction:Althoughthenoseandlungsareseparateorgans,numerousstudieshavereported thattheentirerespiratorysystemcanbeconsideredasasingleanatomicalandfunctionalunit. Theupperandlowerairwaysaffecteachothereitherdirectlyorthroughreflexmechanisms.
Objective: Inthisstudy,weaimedtoevaluatetheeffectsoftheradiofrequencyablationof persistentinferiorturbinatehypertrophyonnasalandpulmonaryfunction.
Methods:Twenty-sevenpatientswithbilateralpersistentinferiorturbinatehypertrophy with-outseptaldeviationwereincludedinthisstudy.Allofthepatientswereevaluatedusinganterior rhinoscopy,nasalendoscopy,acousticrhinometry,avisualanaloguescale,andflow-sensitive spirometryonthedaybeforeand4monthsaftertheradiofrequencyablationprocedure.
Results:Thepost-ablationmeasurementsrevealedthattheinferiorturbinateablationcaused anincreaseinthemeancross-sectionalareaandvolumeofthenose,aswellasintheforced expiratoryvolumein1s,forcedvitalcapacity,andpeakexpiratoryflowofthepatients.These differencesbetweenthepre-andpost-ablationresultswerestatisticallysignificant.The post-ablationvisualanaloguescalescoreswerelowerwhencomparedwiththepre-ablationscores, andthisdifferencewasalsostatisticallysignificant.
Conclusion: Thisstudydemonstratedthatthewideningofthenasalpassageafterthereduction oftheinferiorturbinatesizehadafavorableeffectonthepulmonaryfunctiontests.
© 2017 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/).
夽 Pleasecitethisarticleas:UnsalO,OzkahramanM,OzkarafakiliMA,AkpinarM,KorkutAY,KurtDizdarS,etal.Doesthereductionof
inferiorturbinateaffectlowerairwayfunctions?BrazJOtorhinolaryngol.2019;85:43---9.
∗Correspondingauthor.
E-mail:ozlemunsal@hotmail.com(O.Unsal).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.
https://doi.org/10.1016/j.bjorl.2017.10.007
1808-8694/©2017Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen
PALAVRAS-CHAVE Rinometriaacústica; Conchasnasais; Hipertrofia; Espirometria; Sistemarespiratório
Areduc¸ãodaconchanasalinferiorafetaasfunc¸õesdasviasaéreasinferiores?
Resumo
Introduc¸ão:Emboraonarizeospulmõessejamórgãosseparados,numerososestudosrelataram quetodoosistemarespiratóriopodeserconsideradocomo umaúnica unidadeanatômicae funcional.Asviasaéreassuperioreseinferioresafetamumaàoutradiretamenteouatravésde mecanismosreflexos.
Objetivo:Avaliarosefeitosdaablac¸ãoporradiofrequênciaemconchasnasaisinferiorescom hipertrofiapersistentesobreafunc¸ãonasalepulmonar.
Método: Foramincluídos nesteestudo27 pacientescomhipertrofiapersistentebilateral de conchasinferioressemdesvioseptal.Todosospacientesforamavaliadoscomrinoscopia ante-rior,endoscopianasal,rinometriaacústica,escalavisualanalógicaeespirometriasensívelao fluxonodiaanteriorequatromesesapósoprocedimentodeablac¸ãoporradiofrequência.
Resultados: Asmedidaspós-ablac¸ãodemonstraramqueaablac¸ãodasconchasnasaisinferiores resultouemumaumentodaáreatransversalmédiaedovolumedonariz,bemcomodo vol-umeexpiratórioforc¸adoem umsegundo,dacapacidade vitalforc¸adaedofluxoexpiratório máximodos pacientes. Essas diferenc¸as entre os resultados pré e pós-ablac¸ão foram esta-tisticamentesignificantes.Osescores daescala visualanalógicapós-ablac¸ãoforammenores quandocomparadoscomosescorespré-ablac¸ãoeessadiferenc¸atambémfoiestatisticamente significante.
Conclusão:Oalargamentodapassagemnasalapósareduc¸ãodotamanhodasconchasnasais inferioresteveefeitofavorávelnostestesdefunc¸ãopulmonar.
© 2017 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Publicado por Elsevier Editora Ltda. Este ´e um artigo Open Access sob uma licenc¸a CC BY (http:// creativecommons.org/licenses/by/4.0/).
Introduction
InferiorTurbinateHypertrophy(ITH)isacommoncauseof chronic nasal obstruction.1,2 Although this enlargement is mostly reversible, it can persist, as in cases of vasomo-torrhinitis,allergicrhinitis,orcompensatoryhypertrophy, becauseof septaldeviation.3 Many differentconservative ITHtherapieshavebeenapplied,includingtheuseof anti-histamines,systemicdecongestants,orintranasalsprays.4,5 However,surgicalreductionmaybeagoodoptioninthose casesinwhichmedicaltreatment hasfailed,andit isthe mosteffectivetreatmentforITH.6RadiofrequencyAblation (RFA) is widely usedfor thesurgical reductionof inferior turbinate’s,althoughthereisalackofconsensusregarding theoptimalsurgicaltechnique.7---9
Even though the nose and lungs are usually treated as separate entities, the upper and lower airways can be regarded as a single anatomical and functional unit, since they directly affect each other.4 The treatment of sinonasalpathologies, includingallergic rhinitis, sinusitis, nasalpolyps,andseptaldeviation,helpstoresolvenotonly nasalobstruction,butcanalsopositivelyinfluencelower air-wayfunctions.10---13Forthisresearch,weaimedtoevaluate theeffectsofthetreatmentofpersistentITHonnasaland pulmonaryfunctions.
Methods
Thisprospective studywasperformed betweenJune 2015 and December 2016, and was approved by the Institu-tionalEthicalCommittee(approval protocolnumber238). Informedconsentwasobtainedfromallofthevolunteers.
Twenty-sevenadultpatients(21males,6females),between the agesof 20 and59 years old(32.16±10.48), whohad been sufferingfromnasalobstruction duetobilateralITH for atleast 1year,andwhohadbeen usingnasalsteroids foratleast3months,wereenrolledinthisstudy.
Themedicalhistoriesoftheparticipantswererecorded, and the standardized American Thoracic Society respi-ratory disease questionnaire for adults was used to assess their respiratory symptoms.14 Those patients with chronic obstructive pulmonary disease, asthma, allergic rhinitis, malignancy, cardiac disease, and blood coagula-tion pathologies, as well as active and ex-smokers, and those patients using systemic steroids, antileukotriene, nedocromil,teofilin,andanticoagulantswereexcludedfrom thisstudy.Nasalpathologies,suchasseptaldeviation,nasal valve disorders, alar collapse, septal perforation, middle turbinatehypertrophy,andnasalpolyposis,andaprevious history of nasal surgery, were also accepted as exclusion criteria.
An endoscopic examination was performed in each patientwitha4mm,0◦endoscope(KarlStorzGmbhCo., Tut-tlingen,Germany).A10pointVisualAnalogueScale(VAS)(1 beingtheleast,10beingthemost)wasusedtodetermine the severityof thenasalobstruction. This scale wasused beforeand4monthsaftertheRFAoftheinferiorturbinates. AllofthepatientsunderwentAcousticRhinometry(AR) usingaRhinoscan SRE2000(RhinoMetrics A/S,Lynge, Den-mark)inthesittingpositionbeforeand4monthsafterthe RFA.Nodecongestantswereusedbeforethetest,andeach nasal passage was tested separately. The measurements weretaken bythesame researcher.Aroundplastic nose-piecewitha13mm innerdiameterwasusedforthetest. The patientwasaskedtoholdhisor herbreath afterthe
nasaladaptorwasplaced.Meancross-sectionalarea(MCA)1 and2werethedistancefromthenostrilsto2.2cmandfrom 2.2to5.4cm,respectively.Volumes1and2weremeasured from0to2.2cmand2.2to5.4cm,respectively,whilethe totalvolumewasmeasuredusingthetotaldistance(from0 to5.4cm).Foreachpatient,werepeatedtheAR measure-mentsatleastthrice(bothpre-andpost-operatively) and recordedtheaveragevalues.
All of the surgeries were performed by a senior sur-geon under local anesthesia using the same technique. In each patient, topical lidocaine spray was applied to both mucosal surfaces. After 5min, 2mL of 40mg lido-caine HCl with 0.025mg adrenalin diluted with 2mL of 0.9%NaClwasinjectedintoeachinferiorturbinateusinga 22G×32mmdentalinjector.Theregulationandmonitoring oftheentiresoft-coagulationprocesswereconductedviaa radiofrequencygenerator(CelonLabENT;CelonAG,Teltow, Germany).Aconchalprobe(CelonProBreath,CelonAG, Tel-tow,Germany) wasinserted intothesubmucosal planeof theanterior,middle, andposterior one-thirdofeach infe-riorturbinate under endoscopic guidance(Figs. 1 and 2). The energysupplied foroneshot was12W,andatotalof 300J ofenergywasdeliveredtoeach turbinatefor 8---9s. Noadditionalout-fracturingwasperformedforthe turbino-plasty.
Eachof thepatientswasinvitedfor afollow-up exami-nation1 weekand4 monthsaftertheprocedure.Specific attentionwasgiventotheexistenceofanycrust,infection, dryness,and/orodor.Thecrustsorsecretionsinbothnasal cavitieswereremovedbeforetheARmeasurementcontrol andPulmonaryFunctionTest(PFT).ThePFTwasperformed using a Spirolab III spirometer (MIR, Rome, Italy) based ontheAmericanThoracicSocietyrecommendations.15 The Peak Expiratory Flow (PEF), Forced Expiratory Volume in 1second (FEV1),Forced VitalCapacity(FVC),andratioof theFEV1toFVC(FEV1/FVC)weremeasured.Thebestvalue ofthreetrialswasrecorded.
Figure1 Anendoscopicimageoftheleftnasalcavity. Hyper-trophicinferiorturbinate ofa patient before radiofrequency ablationisdemonstrated.S,Septum;IT,InferiorTurbinate.
Figure 2 An image showing the reduction of left inferior
turbinateofapatientusingradiofrequencyablationtechnique. Aconchalprobeisinsertedintothesubmucosalplaneofinferior turbinate,andposterior,middleandanterioronethirdsofthe turbinateareablatedbyatotalof300Jofenergy.S,Septum; IT,InferiorTurbinate;P,Conchalprobe.
ThestatisticalanalysiswasperformedusingSPSSversion 15.0forWindows.Thedescriptivestatisticsforthe numer-ical variables were expressed as the mean and standard deviation.Apairedt-testwasusedforthecomparisonofthe numericalvariablesbetweenthedependentgroupswhena normaldistributionwasshown;ifnot,theWilcoxontestwas used.Statisticalsignificancewasdefinedasp<0.05.
Results
Twenty-sevenpatientswereincludedinthepresentstudy; withameanageof32.16±10.48yearsold(range20---59). Therewere6females(22.2%)and21males(77.8%).RFAwas appliedtobothinferiorturbinatesofeachpatient.Intotal, 54nasalcavitieswereanalyzed.
Subjectiveevaluationofsymptoms
The pre-ablation mean VAS score (8.58±1.07) was com-paredwiththepost-ablationmeanVASscore(3.11±1.24) fortheleftnasalcavityandthepre-ablationmeanVASscore (8.63±1.07)wascomparedwiththepost-ablationmeanVAS score (3.26±1.37) for right nasal cavity. The descriptive statisticsoftheVASresultsrevealedthatthepre-operative values were significantly higher than the post-surgical 4 month measurementsfor the leftand right nasal cavities (p<0.001andp<0.001,respectively).
Objectiveevaluationofnasalcavitiesbyacoustic rhinometry
The pre- and post-ablation MCAs and nasal volumes for theright andleft nasalcavities were compared.As illus-trated in Figs. 3 and 4, the post-ablation left MCA 1
1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 LMCA1 LMCA2 Pre-ablation Post-ablation
Figure3 Demonstrationofthechangesintheleftmean cross-sectionalarea1and2(LMCA1,2)beforeandafterthereduction ofinferiorturbinatesize.Dataarepresentedasmedian, and minimumandmaximumvalues.TheincreaseintheLMCA1and2 afterthetreatmentofITHwasstatisticallysignificant(p<0.001 andp=0.001,respectively). LMCA1and 2,Left Mean Cross-sectionalArea1and2.
1.2 1.0 0.8 0.6 0.4 0.2 0.0 RMCA1 RMCA2 Pre-ablation Post-ablation
Figure4 The post-operative valuesofRMCA 1and 2were
comparedwiththe pre-operativemeasurements.Statistically significantincreaseintheRMCAswasdeterminedafterreducing the inferior turbinate size (p<0.001 and p<0.001, respec-tively).RMCA1and2,RightMeanCross-sectionalArea1and2.
and 2 (LMCA 1, 2) and right MCA 1 and 2 (RMCA 1, 2) were higher when compared with the pre-ablation val-ues,and the differences between them werestatistically significant (p<0.001, p=0.001, p<0.001, and p<0.001, respectively). Similarly, the post-ablation right nasal vol-ume 1 and 2 (RVOL 1, 2), Right total Volume (RtotVOL) (Fig.5),leftnasal volume1and 2(LVOL1, 2),Left total Volume (LtotVOL) (Fig. 6) and total volume of the nose (totVOL)(Fig.7)wereincreasedwhen comparedwiththe pre-ablation volumes, and those differences were statis-ticallysignificant (p=0.003,p<0.001, p<0.001,p=0.001, p<0.001,p<0.001,andp<0.001,respectively). 14.0 12.0 10.0 8.0 6.0 4.0 2.0 0.0
RVOL1 RVOL2 RtotVOL
Pre-ablation Post-ablation
Figure 5 Illustration ofthechanges inright nasalvolumes (RVOL 1,2 andRtotVOL) before andafter reductionof infe-rior turbinate.The treatmentofITHhadpositiveeffectwith statisticalsignificanceontheallrightnasalvolumes(p=0.003,
p<0.001andp<0.001,respectively).RVOL1and2,Rightnasal Volume1and2;RtotVOL,TotalVolumeoftherightnasalcavity.
16.0 14.0 12.0 10.0 8.0 6.0 4.0 2.0 0.0
LVOL1 LVOL2 LtotVOL
Pre-ablation Post-ablation
Figure 6 The changes in left nasal volumes (LVOL 1, 2
andLtotVOL)beforeandafterreducingtheinferiorturbinate sizeweredemonstrated.Statisticallysignificantincreaseinall volumesoftheleftnasalcavitywasdeterminedafterthe treat-ment ofITH(p=0.001,p<0.001 andp<0.001,respectively). LVOL1and2,LeftnasalVolume1and2;LtotVOL,TotalVolume oftheleftnasalcavity.
Evaluationofpulmonaryfunctionbyflow-sensitive
spirometer
Thepost-ablationFVC,FEV1,andPEFresultswerefoundto behigherthanthepre-ablationmeasurements,andthe dif-ferenceswerestatistically significant(p<0.001, p<0.001, and p=0.042, respectively). However, when the pre- and post-ablation measurements of the FEV1/FVC ratio were compared, no marked difference was observed (p>0.05) (Fig.8).
30 25 20 15 10 5 0 TotVOL Pre-ablation Post-ablation
Figure 7 Demonstration of the Total Volume of the nose
(totVOL) increased significantly after the treatment of ITH (p<0.001).Theentirenasalcavityexpandedduetothe reduc-tionoftheinferiorturbinates.TotVOL,TotalVolumeofthenose (lefttotalvolume+righttotalvolume).
120 100 110 90 80 70 60 50 40 30 20 10 0
FVC FEV1 FEV1/FVC PEF
Pre-ablation Post-ablation
Figure 8 The spirometric measurements before and after
thereduction ofinferiorturbinate.FVC, FEV1andPEF eval-uated4monthsafterthetreatmentofITHaredeterminedto be increasedwith statistical significance (p<0.001,p<0.001 andp=0.042,respectively).FVC,ForcedVitalCapacity;FEV1, Forced Expiratory Volume in 1second; PEF, Peak Expiratory Flow.
Discussion
Forthisresearch,theupperandlowerairwayswere exam-ined before and after the RFA of persistent ITH. The treatment of sinonasalpathologies,such asrhinosinusitis, allergic rhinitis, or septal deviation, has been previously investigatedwith regard tothe effects onthe pulmonary system. However, there were no studies regarding infe-riorturbinateandlunginteractionsfoundintheliterature. Therefore, we aimed to evaluate the effects of inferior
turbinatesizereductiononbothnasalandpulmonary func-tions.Forthispurpose,RFwaspreferredwhichisawidely usedtechniquefor reducing the sizeof the inferiornasal turbinates. This reduction results in an enlargement of thenasalairwayandimprovestheflow volumeof inhaled air.16
AR provides an objective measurement of the cross-sectionalareas ofthe correspondingsectionsinthe nose, andARimprovementafteranRFAoftheinferiorturbinates hasbeenreportedin severalstudies.7,9,17,18 Inaccordance with these reports, our study revealed that the infe-rior turbinate size was successfully reduced since all of the AR parameters were found to be significantly higher thanthepre-ablationmeasurements.Astatistically signif-icantdecreasewasalsoobservedin thepost-ablationVAS scores when compared with the pre-ablation VAS scores of the patients. Overall, the reduction in the turbinate size enabled a widening of the nasal passages. In accor-dancewiththe ARresults, thespirometric measurements (including the FEV1, FVC, and PEF) were improved after thereductionofinferiorturbinatesize,withstatistical sig-nificance. However, it should be emphasized that these improvements inVAS scores, ARmeasurementsand spiro-metricvaluesindicateonlytheshorttermoutcomesofthe inferiorturbinatereductionandthewideningofthenasal passagesduetothe4month follow-uptime.Additionally, theseresultsdonotallowtoevaluatetheeffectivenessof the radiofrequency ablation technique that was used for reducing the size of the turbinate’s in this study. A sin-gle technique was preferred for the treatment of ITH in ourwork. Therefore,other methodsfor thesamepurpose suchasout-fracture,submucosalresectionor bipolar cau-terization of the inferior turbinate’s may provide similar effects.
Due to the close relationship between the upper and lowerairways, they can be regarded asa single anatom-ical and functional unit.19 The upper respiratory mucosa helps to humidify, heat, and filter the inhaled air, and thusprotectthelowerrespiratorytract.Mucociliary clear-anceisimportantforprotectingthemucosaagainstforeign particles, preventing bacterial infection, and moisturiz-ing the epithelial cell layer. The humidity, mucociliary clearance, and temperature, which are the physiological conditionsofthenasalcavity,arenormallyaffectedbythe airstream,andcan deterioratein adecreasing airstream. The continuousairflow stimulationprovides optimalnasal cavityaerodynamics,andfacilitatesthephysiological func-tion of the mucociliary activity.20 The conditioning and filtering capacity of the nose protects the lower air-ways and in the case of partial or complete loss of function of the nose, the dry or cold air and poten-tially harmful agents entering the bronchi can lead to bronchoconstriction.21 The rhinobronchial reflex which is thoughttobeoneofthepathogenicmechanisms connect-ingthenose andlungscan bestimulated byinhalation of coldorunfilteredairandcauselowerairwayirritabilityand morbidities.12,22
Also,thetreatmentofsinonasalpathologiesmayaffect thelowerairway,andviceversa.Forinstance,Karuthedath etal.23 evaluatedthe effects of endoscopicsinus surgery onthepulmonaryfunctionofpatientswithchronic rhinosi-nusitis,andtheyobservedaremarkablerecoveryinthePFT
results after the surgery. Likewise, a significant improve-mentinthePFTparametersafterseptoplastywasreported in the literature, and was attributed to normalizing the nasalairstream.12 Inthepresent study,resultscompatible withthesereportswerefoundinthePFTparametersafter thereductionoftheinferiorturbinates.Thepost-operative FEV1,FVC,andPEFweredeterminedtobeincreasedwhen comparedwiththepre-operativemeasurements.Thismay havebeenduetotheimprovednasalaerodynamicsafterthe reductionoftheinferiorturbinatesize.
The major limitationof thisstudy was the inability to obtain a large number of cases due to the strict exclu-sion criteria. The selection of patients with an isolated ITH was quite difficult, since septal deviation is a fre-quently encountered nasalpathology. On the other hand, persistentITH ismost often seenin patients withallergic rhinitis. Other conditions, suchas pulmonary and cardiac diseases,smoking, or theuse ofbronchoactive drugs,can affect the PFT parameters; therefore, these cases were also excluded from the study in order to observe only theeffectsof theinferiorturbinatereductiononthe pul-monary function. Additionally, the patients who left the studyduringfollow-up alsolimitedthenumberof partici-pants.
Conclusion
Theupperandlowerairwayshavenotonlyanatomical con-tinuity;there is alsoa strong interaction between them. Impaired nasal conditions and aerodynamics may lead to a loss of the protective function of the nose, and may activatesinonasalreflexmechanismsaffectingthelower air-wayfunction.It has been reportedthatthe treatment of nasalpathologies,suchasseptaldeviation,chronic rhinos-inusitis,orallergicrhinitis,createsanimprovementinthe lowerairwayfunction.However,theinteractionsbetween thesurgicaltreatmentofITHandpulmonaryfunctionshave not been previously examined. This study revealed that thereductionintheinferiorturbinatesizeprovided signifi-cantimprovementinthePFTresults.Nevertheless,further studies using larger cohorts are needed to analyze these interactions.
Funding
Thisresearchdidnotreceiveanyspecificgrantfromfunding agenciesinthepublic,commercial,ornot-for-profitsectors.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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