Chronic symptoms and pulmonary dysfunction in post-tuberculosis Brazilian patients

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www .e l s e v i e r . c o m / l o c a t e / b j i d

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

Original

article

Chronic

symptoms

and

pulmonary

dysfunction

in

post-tuberculosis

Brazilian

patients

Simone

de

Sousa

Elias

Nihues

a,b

_,

_Eliane

_Viana

_Mancuzo

c

_,

_Nara

_Sulmonetti

c

_,

Flávia

Patussi

Correia

Sacchi

b

_,

_Vanessa

_de

_Souza

_Viana

c

_,

_Eduardo

_Martins

_Netto

d

_,

Silvana

Spindola

Miranda

c

_,

_Julio

_Croda

b,e,∗

a_Department_of_Physical_Therapy,_Centro_{Universitário}_da_Grande_Dourados,_Dourados,_MS,_Brazil

b_Faculdade_de_Ciências_da_Saúde,_Universidade_Federal_de_Garnde_Dourados_(UFGD),_Dourados,_MS,_Brazil

c_Faculdade_de_Medicina,_Universidade_Federal_de_Minas_Gerais_(UFMG),_Belo_Horizonte,_MG,_Brazil

d_Instituto_Brasileiro_para_{Investigac¸ão}_da_{Tuberculose/Fundac¸ão}_José_Silveira,_Salvador,_BA,_Brazil

e_Fundac¸ão_Oswaldo_Cruz,_Campo_Grande,_MS,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received17April2015

Accepted26June2015

Availableonline5August2015

Keywords: Brazil Dysfunction Spirometry Tuberculosis

a

b

s

t

r

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c

t

Background:Questionnaireandspirometrywereappliedtopost-tuberculosisindigenousand

non-indigenousindividualsfromDourados,Brazil,toinvestigatetheprevalenceofchronic

respiratorysymptomsandpulmonarydysfunction.

Methods:Thiswasacross-sectionalstudyincuredtuberculosisindividualsasreportedin

theNationalSystemonReportableDiseases(SINAN)from2002to2012.

Results:Onehundredandtwentyindividualswereincludedinthestudyandtheprevalence

ofchronicrespiratorysymptomswas45%(95%CI,34–59%).Respiratorysymptomsincluded

cough(28%),sputum(23%),wheezing(22%)anddyspnea(8%).Thesesymptomswere

associ-atedwithalcoholism,AOR:3.1(1.2–8.4);lessthan4yearsofschooling,AOR:5.0(1.4–17.7);and

previouspulmonarydiseases,AOR:5.4(1.7–17.3).Forty-onepercent(95%CI,29–56)had

pul-monarydisorders,ofwhichthemostprevalentwereobstructivedisorders(49%),followed

byobstructivedisorderwithreducedforcedvitalcapacitydisorders(46%)andrestrictive

disorders(5%).Thelifestyledifferencecouldnotexplaindifferencesinchronicsymptoms

and/ortheprevalenceofpulmonarydysfunction.

Conclusion:Thehighprevalenceofchronicrespiratorysymptomsandpulmonary

dysfunc-tioninpost-tuberculosispatientsindicatesaneedforfurtherinterventionstoreducesocial

vulnerabilityofpatientssuccessfullytreatedfortuberculosis.

∗ _{Corresponding}_author_at:_Faculdade_de_Ciências_da_Saúde,_Universidade_Federal_da_Grande_Dourados,_Rodovia_Dourados_–_Itaúm_Km_12,

Dourados,MatoGrossodoSul,79804-970,Brazil.

E-mailaddress:[email protected](J.Croda).

http://dx.doi.org/10.1016/j.bjid.2015.06.005

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Introduction

Tuberculosis(TB)isachronicdiseasewithoneofthehighest

morbidityandmortalityratesworldwide.Certaingroups,such

asindigenouspopulations,maybemoresusceptibleto

devel-opingthedisease.1–3_The_incidence_of_TB_among_indigenous

peopleisconsistentlyhigherthaninthegeneralpopulation.

BetweenJanuary2002andDecember2008,themeanofannual

TBnotiﬁcationsintheindigenouspopulationofDouradoswas

260per100,000inhabitantscomparedtoonly25per100,000

inhabitantsinnon-indigenouspopulations.4–6_Among_treated

andcuredTBpatients,somemaydeveloprespiratory

seque-laecharacterizedbychronicrespiratorysymptoms,including

cough,sputum,anddyspnea.Thesesequelaemaypersisteven

inindividuals who have been properly treated forTB and

shouldnotbeoverlookedastheyhaveanegativeimpacton

theindividual’squalityoflife.7

Thereisnoconsensusonwhichdisorderisthemost

preva-lent in individuals with TB sequelae.7–12 _{Population-based}

studiesareneededtoinvestigatethepersistenceofchronic

symptomsandchangesinlungfunction.Inaddition,

indige-nouspopulationshavedifferentimmuneresponsesandrisk

factors associated withTB comparedwith non-indigenous

populations.13,14 _Thus,_further_studies_are _needed_to_clarify

whethertherearedifferenceswithregardtotheprevalenceof

thesechangesbetweenthesetwopopulations.Inthissense,

theobjectiveofthisstudywastoinvestigatetheprevalence

of chronic respiratory symptoms and pulmonary

dysfunc-tion inpost-tuberculosisindividuals and to comparethese

resultsbetweenindigenousandnon-indigenouspopulations

ofDourados-MS.

Material

and

methods

Studydesignandinclusionandexclusioncriteria

Thiswasacross-sectionalpopulation-basedstudyof

indige-nousand non-indigenous individuals with ahistory of TB

asreportedbythe NationalSystem onReportableDiseases

(SINAN)fromJanuary2002toDecember2012inDourados-MS.

WeincludedindividualswithnotiﬁcationsofTBtotheSINAN

diagnosedbetween2002and2012.Weexcludedindividuals

under18orover65yearsofage,prisoners,residentsofother

municipalities,andpatientswithchangesindiagnosisorwith

neurologicaldisorders.

Data collection was conducted by visiting each

partic-ipant’s home from November 2013 to October 2014. The

questionnairewasadministeredtotheparticipantsinorder

tocollectsociodemographic,clinicalandepidemiological

vari-ables that could be associated with the development of

pulmonary changes post-tuberculosis such as persistence

ofrespiratorysymptoms andpulmonary function.The

fol-lowing variables were considered: gender, age, educational

level,nationality,race,occupation,maritalstatus,alcoholuse,

smoking,passivesmoking,previouspulmonarydiseases

(pul-monaryemphysema,bronchitis,andpleuraleffusion),work

inadustyand/orsmokyenvironment,wood-stoveuse,and

persistenceofrespiratorysymptomssuchascough,phlegm,

sputum, wheezing, and dyspnea after successful TB

treat-ment.

Spirometry

Evaluations of pulmonary function were performed by

spirometry using a portable spirometer Koko Spirometer

(manufacturedbynSpireHealth,Inc,LefthandCircle,

Long-mont, USA,Koko PFT Software,Series No.1329K3A39)that

allowedforthenewBrazilianstandardsforcalculatingthe

the-oreticalvalueofadultsaccordingtothenewreferencevalues

forforcedspirometryinBrazilianpopulationstobeused.12_We

evaluatedtheforcedexpiratoryvolumeinonesecond(FEV1),

theforcedvitalcapacity(FVC),ratiooftheforcedexpiratory

volumeinonesecondtotheforcedvitalcapacity(FEV1/FVC),

andtheforcedexpiratoryﬂowbetween25and75%(FEF25–75%).

Thetestsconsistedofpre-andpost-bronchodilatorphases,

thelatterobtained15minaftertheadministrationof400␮g

ofsalbutamol.

PatientswereclassiﬁedinaccordancetotheGuidelinesfor

Pulmonary FunctionTestsofthe BrazilianSocietyof

Pneu-mologyandTisiology.Spirometrywasconsideredasnormal

whentheFVC,FEV1andFEV1/FVCwereequaltoorgreater

than80%ofthepredictedvalue.Obstructivedisorderwas

con-sideredwhentheFEV1/FVCratiowasbelow80%andFEV1was

less than 80%ofthe predictedvalue. Apatientwas

classi-ﬁedwitharestrictivedisorderwhentheFEV1/FVCratiowas

lessthan80%andFVCwasbelow80%ofthepredictedvalue.

Obstructive disorderwithreducedforcedvitalcapacitywas

consideredwhenthedifferencebetweenFVCandFEV1forthe

pre-bronchodilatorphasewaslessthanorequalto12%.15

Statisticalanalysis

All clinical data were entered in duplicate into the

elec-tronicdatabaseEpiData,version3.1(TheEpiDataAssociation,

Odense,Denmark),andSASversion9.2(SASInstitute,Cary,

NC)wasusedtoanalyzetheunivariateandmultivariate

mod-els associated with chronic symptoms. Dichotomized and

categoricaldatawereanalyzedwiththechi-squaredtestor

Fisher’s exact test. For continuous variables, the t-test or

analysisofvariance(ANOVA)wereutilized.Univariate

anal-yseswereperformedtoverify theassociationsbetweenthe

dependent andindependentvariables,and those achieving

a pre-speciﬁedlevel ofsigniﬁcance(p<0.20) were included

inthemultivariateanalysis.Logisticregressionanalysiswas

usedtoestimatetheadjustedoddsratios.

Ethicalconsiderations

Alleligibleindividualswereinformedaboutthestudy,andthe

questionnaireand spirometry were performedafter

receiv-ing a written approval in the informed consent. Informed

consent formsin the Guaranílanguage were used for the

indigenouspopulation.Theconsentformswerereadtothe

illiterateparticipantsandtheyprovidedtheirconsentusing

theirﬁngerprint.TheprojectwasapprovedbytheResearch

EthicsCommitteeoftheFederalUniversityofGrande

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Patients reported to SINAN: 2002 to 2012: 800 Excluded patients: 325 Age <18 or >65: 200 Eligible patients: 475 Diagnosis change: 4 Neurological disorders: 6 Deprived of

liberty: 74 Residents in _other municipalities: 41

Losses: 314 Patients found:

161 Change of address: 20 Deaths: 7 Patients who refused to participate in the study: 2 Patients included in the study: 65 Patients who underwent spirometry: 50 Patients who did not perform spirometry: 15

Patients who refused to participate in the study: 38

Patients included in the study: 56

Patients who underwent spirometry:

50

Patients who did not perform

spirometry: 6 Indigenous: 67 Non-indigenous: 94 Change of address: 146 Deaths: 11 Patients with incomplete address or phone in the notification: 130 Indigenous: 27 Non-indigenous: 287

Fig.1–FlowchartofindividualswithahistoryoftuberculosisinDourados,MatoGrossodoSul.

National Health Council (CAAE:

05532912.8.0000.5160/Num-ber:193.877).

Results

Duringthestudyperiod,800individualswerediagnosedwith

tuberculosisand reportedtothe SINAN.Ofthose,325were

excluded(Fig. 1). Wewerenot abletointerview 318ofthe

475individualsincludedinthis studybecause166changed

theirhomeaddress,18died,and130couldnotbefounddue

toincorrectaddressandphonecontactinformation.We

con-tacted161individuals,and25%refusedtoparticipateinthe

study.Theﬁnalsampleof121participantswasdividedinto

two groups: indigenous (n=61)and non-indigenous (n=60)

(Fig.1).Twenty-oneindividualsdidnotreproduceacceptable

spirometrycurves,includingtwowhopresentednausea,four

due to missing teeth, 10 failed to perform the maneuvers

becauseofdifﬁcultiesinunderstandingthecommands,and

ﬁvewereunabletoundergospirometryduetoseveredyspnea.

Table1showsthesociodemographiccharacteristicsofthe

indigenousandnon-indigenousindividualswithahistoryof

tuberculosis.Amongthe indigenousparticipants, 57%were

male,and87%hadlessthan fouryearsofschooling.Inthe

non-indigenous group, 47% were male, and 78% had less

thanfouryearsofschooling;thissamegroupalsoincluded

moreindividualswhousedalcohol,illicitdrugs,andsmoked.

Non-indigenousindividualshadmorecurrenthistoryof

spu-tumproductionthanindigenous(p=0.05).Cough,wheezing

anddyspnea,aswellasthespirometricvalues,weresimilar

betweentheethnicgroupsconsidered(Table1).

Theprevalenceofrespiratorysymptomswas45%(95%CI,

34–59%)andincludedcough(28%),sputum(23%),wheezing

(22%),anddyspnea(8%).Comparedwithasymptomatic

indi-viduals,post-tuberculosis individuals withsymptoms were

morelikelytohavelessthenfouryearsofschooling(93%

ver-sus74%,p<0.01),workindustyenvironment(44%versus25%,

p=0.03),andtohavehadpreviouspulmonarydiseases(25%

versus8%,p<0.01)Themajorityoftheindividualswhohad

symptomshadabnormalspirometrywhencomparedto

indi-vidualswithnosymptoms(65%versus35%,p<0.01)(Table2).

Inthemultivariatemodel,thefollowingvariableswere

asso-ciatedwiththepresenceofsymptoms:lessthanfouryearsof

schooling,AOR:5.0(1.4–17.7);alcoholabuse,AOR:3.1(1.2–8.3);

andpreviouspulmonarydiseases,AOR:5.4(1.7–17.4)(Table3).

Amongtheparticipants,41%(95%CI,29–56)hadpulmonary

disorders,ofwhichthemostprevalentwereobstructive

dis-orders (49%),followedbyobstructivedisorder withreduced

forcedvitalcapacitydisorders(46%),andrestrictivedisorders

(5%).Eighteenindividualshadmoderatepulmonary

dysfunc-tion,andonly1(6%)hadbeendiagnosedwithlungdisease

andwereundermedicalcare.

Discussion

Few studies have evaluated the permanence of

post-tuberculosis respiratory symptoms, which reinforces the

importanceofthisresearch,consideringthenegativeimpact

andinﬂuenceonthequalityoflifeofindividualsaffectedby

thesechangesinlungfunction.7,9,10,16

Inourpopulation-basedstudy,weobservedthepresence

ofchronicsymptomssuchascough,sputum,dyspnea, and

wheezingin45%ofsubjectsevenafterthecompletionof

treat-mentandcureofTB.Thispersistenceofrespiratorysymptoms

wasalsofoundinastudyofadultpatientstreatedinthe

out-patientTBclinicofauniversityhospitalinwhich72%ofthe

56patientshadchronicsymptomssimilartothosefoundin

thisstudy.9

Amongtheprevalentpost-tuberculosissymptoms,cough

andsputumhavebeenreported,andaccordingtoastudyin

theInstituteofPulmonology,thesesymptomswerepresentin

80%ofpatientsfollowed.Dyspneawasalsomentionedby45%

ofthepatients.17_Sputum_production_has_been_correlated_with

theresiduallungdamage,asreportedbyHnizdoetal.18_Even

inindividualswhoproperlytreatedfortuberculosis,thereis

persistenceofsymptoms;recentresearchhasshownthat3/5

ofthepopulationstudiedshowedpersistentpost-tuberculosis

respiratorysymptoms.7

Delays in the diagnosis and initiation of TB treatment

can lead to increasedinjury to the lung parenchyma, and

(4)

Table1–Sociodemographiccharacteristics,chronicrespiratorysymptomsandspirometryparametersofindigenousand non-indigenousindividualswithahistoryoftuberculosisinDourados(n=121).

Variables Race

Number(percentage)

pvalue

Indigenous(n=61) Non-indigenous(n=60)

Sex,male 35(57) 28(47) 0.24

Age,years,mean±SDa ₃₈_±₁₅ ₄₂_±₁₅ _0.20

Maritalstatus,single 9(15) 31(52) <0.01

Lessthan4yearsofschooling 53(87) 47(78) 0.21

BMI,mean±SDa ₂₅_±₄ ₂₄_±₅ _0.27

Currentsmoker 13(21) 30(50) <0.01

Passivesmoker 6(10) 13(22) 0.07

Druguse 1(2) 12(25) <0.01

Alcoholism 6(10) 18(30) <0.01

Workindustyenvironment 9(13) 31(52) <0.01

Workinsmokyenvironment 7(12) 6(10) 0.74

Previouspulmonarydiseasesb ₅₍₈₎ ₁₄₍₂₄₎ _0.02

Symptoms 24(20) 31(26) 0.17 Cough 18(15) 24(20) 0.23 Sputumproduction 14(12) 24(20) 0.05 Wheezing 14(12) 17(14) 0.50 Dyspneagrade2 1(1) 5(5) 0.11c Dyspneagrade3 3(3) 0(0) 0.24c Dyspneagrade4 0(0) 1(1) 0.49c Spirometryparameters FEV1/FVC×100 86% 89% 0.40 FEV1 85% 87% 0.62 FVC 89% 86% 0.67 FEF25–75% 82% 80% 0.57 Patternofspirometry 0.35 Normal 29(58) 30(60) Obstructive 8(16) 12(24)

Obstructivedisorderwithreducedforcedvitalcapacity 11(22) 8(16)

Restrictive 2(4) 0(0)

BMI,BodyMassIndex;FVC,forcedvitalcapacity;FEV1,forcedexpiratoryvolumeinthefirstsecond;FEV1/FVC,ratioofforcedexpiratoryvolume inthefirstsecondandforcedvitalcapacity;FEF25–75%,forcedexpiratoryflowbetween25and75%.

a _Standard_deviation.

b _Previous_pulmonary_diseases:_bronchitis,_emphysema_and_pleural_effusion. c _Fisher’s_exact_test.

persistentrespiratorysymptomsandlungdysfunction.11,18–20

Theresultsofthis studyindicate thatsomefactorscan be

critical to the presence of chronic respiratory symptoms

inindividuals with ahistory oftuberculosis; amongthese

factors,thereisanemphasisoneducation,alcoholuse,and

previous respiratory diseases.2,21 Low level of education is

relatedtolowsocioeconomicstatus,andthisisarecognized

risk factor forTB. In addition, the social condition of the

individual can lead to less access to health services and,

consequently, to a diagnosis of tuberculosis. Alcohol

con-sumptioncan alsobeassociatedwithalatediagnosis,and

socioeconomicconditionsinbothdelayedsituationsexpose

theindividualtolongerdiseaseduration and,therefore,an

increasedlikelihoodofpulmonarysequelae.2,21

Usingdiagnosticservices,astudyinDourados-MSnoted

that75%ofindigenousand65%ofnon-indigenousindividuals

soughttreatmentattheonsetofsymptoms.However,most

patientsreportedadiagnosticdelay;46%ofindigenousand

44%ofnon-indigenouspatientsneedatleastthree(3)medical

consultationstoreceiveadiagnosisofTB,whichtookmore

thanﬁveweeks.Therefore,thesepatientsspentmoretime

exposed tothedisease andwere moresusceptibleto

post-pulmonarytuberculosissequelae.21

Another study involving an indigenous population of

Dourados-MS concluded that this population had greater

accesstodiagnostictestsandtreatmentcomparedwiththe

non-indigenous population. The diagnosis and consequent

earlytreatmentintheindigenouspopulationcomparedwith

thenon-indigenouspopulationmightexplainwhytherewere

nodifferencesinthelengthofsymptomsorchangesin

pul-monaryfunction betweenthepopulations studied,evenin

theface ofthedifferentlivinghabits,culturalbarriers,and

thelowerlevelofeducationandsocioeconomicstatusofthe

indigenouspopulation.5,21

Among the individuals who underwent spirometry in

our study,41%had pulmonaryfunction changes:themost

prevalent were obstructive disorders (49%), followed by

obstructivedisorderwithreducedforcedvitalcapacity(46%)

and restrictive disorders (5%). It remains unclear which

respiratory disorder is most prevalent in post-tuberculosis

sequelae due to the small number of studies conducted.

(5)

Table2–DifferencesamongpatientswithahistoryoftuberculosisstratiﬁedbypresenceofsymptomsinDourados (n=121). Variables Symptoms Number(percentage) pvalue Symptoms (n=55) Non-symptoms (n=66)

Clinicalandepidemiological

Sex,male 22(40) 41(62) 0.01

Race,indigenous 24(44) 31(56) 0.17

MaritalStatus,single 20(37) 21(32) 0.53

Age,years,mean±SDa ₄₃_±₁₄ ₃₈_±₁₅ _0.11

Lessthan4yearsofschooling 51(93) 49(74) <0.01

Currentsmoker 22(40) 21(32) 0.35

Passivesmoker 9(17) 10(15) 0.85

Druguse 10(18) 6(9) 0.14

Alcoholism 15(27) 9(14) 0.06

Workindustyenvironment 24(44) 16(25) 0.03

Workinsmokyenvironment 8(15) 5(8) 0.24

Cookwithawoodstove 16(30) 15(24) 0.48

Previouspulmonarydiseasesb ₁₄₍₂₅₎ ₅₍₈₎ _<0.01

Patternofspirometry <0.01

Normal 14(35) 45(75)

Obstructive 13(33) 7(12)

Obstructivedisorderwithreducedforcedvitalcapacity 11(27) 8(13)

Restrictive 2(5) 0(0)

a _Standard_deviation.

b _Previous_pulmonary_diseases:_bronchitis,_emphysema_and_pleural_effusion.

Table3–Riskfactorsassociatedwithrespiratorysymptomsinindividualswithahistoryoftuberculosis(n=121).

Variables CrudeOR(95%CI) AdjustedOR(95%CI)

Race,indigenous 1.64(0.80–3.39)

Age,peryear 0.98(0.95–1.00)

BMI 0.96(0.88–1.05)

Sex,male 2.46(1.18–5.12)

Maritalstatus,single 1.22(0.57–2.60)

Lessthan4yearofschooling 4.42(1.39–14.07) 5.01(1.42–17.66)

Smoking 1.42(0.68–3.02)

Passivesmoking 1.09(0.41–2.92)

Druguse 2.22(0.75–6.56)

Alcoholism 2.37(0.94–5.95) 3.10(1.16–8.30)

Previouspulmonarydiseasesa _4.09_{(1.37–12.25)} _5.42_{(1.69–17.34)}

Workindustyenvironment 2.37(1.09–5.15)

Workinsmokyenvironment 2.01(0.61–6.58)

Cookwithawoodstove 1.34(0.59–3.06)

BMI,BodyMassIndex;OR,oddsratio.

a _Previous_pulmonary_diseases:_bronchitis,_emphysema_and_pleural_effusion.

respective studies evaluated the association between TB

andalteredpulmonaryfunction,andtherewasnocommon

consensuson whichdisorder was the mostprevalent as a

sequel.9,19,20

Our study had some limitations, such as a number of

refusalstoparticipatebyindividualswhothoughttheywere

cured and had no symptoms and the difﬁculty of ﬁnding

the households due to the large number of records with

nonexistentphonenumbersandaddresses.Furthermore,8%

oftheindigenousand24%ofthenon-indigenousindividuals

hadprevious pulmonarydiseases andthereforecould have

symptomsand functionalchanges attributedtothe

under-lyingdiseaseandnotrelatedtoTBsequelae.Notallpatients

underwent chestX-raybecausetheexamwasnotincluded

inthestudyobjectives.

Itisimportanttoemphasizethat17%oftheindividuals

includedinthestudywereunabletocompletethespirometry

duetodifﬁcultyinunderstandingtheguidelines,dentalissues

and/orchronicrespiratory symptoms.Amongpatients who

didnotcompletethesurvey,66%hadalowlevelofeducation

and low socioeconomicstatus, which mostlikelyhindered

their comprehension of the guidelines for performing the

required expiratory maneuvers. Most of these individuals

wereindigenous,andinouropinion,theyneedfurther

atten-tion regardingtheirsymptomsforthediagnosisofpossible

(6)

Fortheindividualswhocouldnotperformthespirometry

test,possiblepulmonarysequelaecouldbediagnosedbythe

respiratorysymptomspresentedbytheseindividuals.

Accord-ingtoGlobalObstructiveLungDisease(GOLD,2014),chronic

symptomsshould beconsidered,as theymay indicate the

severityofpulmonarysequelae.22

The high prevalence of chronic respiratory symptoms

and pulmonary dysfunction in post-tuberculosis patients

indicatesaneedforfurtherinterventionstoreducesocial

vul-nerabilityinpatientswithpost-tuberculosis.

Conﬂicts

of

interest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgments

TheauthorsaregratefultotheSpecialSecretariatof

Indige-nousHealth(SecretariadeSaúdeIndígena;SESAI),theCouncil

ofIndigenousHealth(ConselhoDistritaldeSaúdeIndígena;

CONDISI)andtheDepartmentofHealthatDouradosandthe

District for their full support during the study period. We

thanktheindigenousandnon-indigenousparticipants,

with-out whomthis study couldnothavebeen performed. This

workwassupportedbyBrazilianNationalResearchCouncil

(CNPq,N◦404158/2012-9).

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