Anais
Brasileiros
de
Dermatologia
www.anaisdedermatologia.org.brINVESTIGATION
Identifying
gram-positive
cocci
in
dermatoscopes
and
smartphone
adapters
using
MALDI-TOF
MS:
a
cross-sectional
study
夽,夽夽
Maurício
de
Quadros
a,b,∗,
Roberto
Carlos
Freitas
Bugs
a,
Renata
de
Oliveira
Soares
a,
Adriana
Medianeira
Rossato
a,
Lisiane
da
Luz
Rocha
a,
Pedro
Alves
d’Azevedo
aaGram-positiveCocciLaboratory,UniversidadeFederaldeCiênciasdaSaúdedePortoAlegre,PortoAlegre,RS,Brazil bDepartmentofDermatology,HospitalSantaCasadeMisericórdiadePortoAlegre,PortoAlegre,RS,Brazil
Received18February2019;accepted9November2019 Availableonline21March2020
KEYWORDS Dermoscopy; Gram-positivecocci; Massspectrometry; Microbialsensitivity tests Abstract
Background: Theincreasinglyfrequentuseofdermoscopymakesusthinkaboutthepossibility oftransferofmicroorganisms,throughthedermatoscope,betweendoctorandpatients. Objectives: Toidentify themostfrequent gram-positivecocciindermatoscopes and smart-phoneadapters,aswellastheresistanceprofile,andtoevaluatethefactorsassociatedwitha higherriskofbacterialcontaminationofthedermatoscopes.
Methods: A cross-sectional study was carried out with 118 dermatologists from Porto Ale-gre/Brazil between September2017 andJuly 2018. Gram-positivecocci were identified by MALDI-TOFMSandhabitsofuseofthedermatoscopewereevaluatedthroughananonymous questionnaire.
Results: Ofthedermatoscopesanalysed,46.6%hadgrowthofgram-positivecoccionthelens and37.3%ontheon/offbutton.ThemicroorganismsmostfrequentlyfoundwereS.epidermidis, S.hominisandS.warneri.Attendingahospital,usingthedermatoscopeatthehospital,with inpatients andin theintensive careunitwere significantlyassociated withcolonisation by gram-positivecocci.The highestresistancerateswereobservedforpenicillin,erythromycin andsulfamethoxazole-trimethoprim.
Studylimitations: Thenon-searchofgram-negativebacilli, fungiandviruses.Moreover,the smallnumberofadaptersdidnotmakeitpossibletobetterdefineifthefrequencydifferences werestatisticallysignificant.
夽 Howto citethisarticle: Quadros M,Bugs RCF,SoaresRO, RossatoAM, RochaLL,d’Azevedo PA.Identifyinggram-positive cocciin
dermatoscopesandsmartphoneadaptersusingMALDI-TOFMS:across-sectionalstudy.AnBrasDermatol.2020;95:298---306.
夽夽StudyconductedattheGram-positiveCocciLaboratory,UniversidadeFederaldeCiênciasdaSaúdedePortoAlegre,PortoAlegre,RS,
Brazil.
∗Correspondingauthor.
E-mail:mdquadros@gmail.com(M.Quadros).
https://doi.org/10.1016/j.abd.2019.11.004
0365-0596/©2020SociedadeBrasileiradeDermatologia.PublishedbyElsevierEspa˜na,S.L.U.ThisisanopenaccessarticleundertheCC BYlicense(http://creativecommons.org/licenses/by/4.0/).
Conclusion: Coagulase-negative staphylococci were frequently identified. S. aureus was detectedonlyonthelens.
©2020SociedadeBrasileira deDermatologia.PublishedbyElsevierEspa˜na,S.L.U.Thisisan openaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
Introduction
Dermoscopy is an excellent diagnostic tool in the daily practiceofthedermatologist.Inrecentyears,smartphone adapters have been usedtophotograph skin lesions,such asmelanocyticnevi,and allowtheirfollow-up, aswellas facilitatecasediscussionsamongdermatologists.
Thesetechnologicalinnovationshaveenabledhealth pro-fessionals toquicklyaccessa widerrangeof information: using smartphones and tablets it is easier to search for articles,rapidlyaccessrelevanttopicsinbooksand applica-tions,discusscasesingroupswithexperts,andparticipate in teaching future health professionals.1,2 However, the
indiscriminate use of such objects provides a new chal-lenge: the possible transference of microorganisms, with or without pathogenic potential, from these devices to the hands of professionals, or vice versa, or person to persontransference.Forexample,patientswithnasal col-onization by Staphylococcus aureus are 2---9 times more likely to have S. aureus infection.3 The most frequently
identifiedpathogensassociatedwithhealthcare-associated infections were Coagulase-Negative Staphylococci (CoNS) (15%), S. aureus (15%), Enterococcus sp. (12%), Candida
sp.(11%),followedbyseveralgram-negativebacilli.4These
healthcare-related infections representa majorchallenge for the health system and are associated withsignificant costs,morbidity,andmortality.Atanyonetime,upto7%of patientsindevelopedand10%indevelopingcountrieswill acquireatleastonehealthcare-associatedinfection.5
Few studies have evaluated the contamination of microorganismsindermatoscopesandtherearenostudies onsmartphoneadapters.AstudyinSwitzerlandanalysedthe bacterialpresenceonthelensesofdermatoscopesbelonging to10dermatologists(n=10)involvedinthecareofpatients fromthedermatology outpatientclinicsoftwoSwiss hos-pitals. Of the 112 swabs taken, 65% showed the growth ofnon-pathogenic bacteria(includingalltheCoNS, Strep-tococcus ␣ and ␥-haemolytic, Corynebacterium, Bacillus and Lactobacillus). Methicillin-Susceptible Staphylococcus Aureus(MSSA)wasfound onthreeoccasions(onthethree swabs, for dermoscopy, immersion oil had been used on the apparatus ratherthan isopropylalcohol).6 In Austria,
researchers studied the spectrum of microorganisms in 4 dermatoscopes (lensandbody)usedinthedepartmentof dermatology at a Vienna hospitalafter dermoscopy in 39 patientsandfoundS.epidermidisin74%ofthedevicesand
S.aureusin7%.IntheUnitedKingdom,Chattopadhyayetal.
(2014)evaluatedbacterialgrowthon9dermatoscopelenses on60 occasions (30before dermoscopyand 30 after).An alcohol-gelcontaining70%ethanolwasusedasthe immer-sionliquid.TheauthorsfoundMethicillin-ResistantS.Aureus
(MRSA)in10%oftheexperiments(allfromswabsobtained afterdermoscopy).7
The present researchers have sought to identify the gram-positivecoccimostcommonlyfoundondermatoscopes andsmartphoneadapters andtoassess thefactors associ-atedwiththeincreasedriskofbacterialcontamination.
Methods
Between September 2017 andJuly 2018, we conducted a cross-sectional study amongdermatologists whoattended at a dermatology outpatient clinic of a public hospital andinprivate practices.The doctorsanswered an anony-mous questionnaire containing demographic information and about the habits of use of the dermatoscope, and providedtheir devicesfor bacteriologicalanalysis via the swabtechnique.Physicianswhodidnotwishtofilloutthe questionnaireorprovidetheirdermatoscopesorcellphone adaptersforswabbingwereexcluded.
Samples were collected from two or three previously definedsites on the dermatoscopes: the lens, the on/off buttonandtheoutsideofthesmartphoneadapter(for pro-fessionalswhousedthatdevice). The swabswere sealed, labelledandforwardedfor analysis.Inthelaboratory,the swabswereplacedintubescontainingBHIenrichedmedium (brain-heartinfusion)(SigmaAldrich,Merck,Germany)and left in the oven at 35±2◦C for 24h. In the presence of turbidity (in which case the test is considered positive, i.e.there wasbacterial growth),the broths were seeded in5%sheep-bloodagarplates(Biomeriéux,MarcyL’Etoile, France)usingasterileloop.Theplateswerethenreturned totheoven at 35±2◦C for 24h. The platesshowing bac-terialgrowthwereplaced inskimmedmilkandfrozen for lateridentification. SamplesthatcloudedintheBHIbroth weresubsequentlythawedand,again,seededonbloodagar platesforidentificationbyMALDI-TOFMS.Inthisstudy,we used the Bruker Daltonics platform (microflex LT; Bruker DaltonikGmbH,Bremen,Germany).
Totestforsusceptibility,after24hinculturewith sheep-blood agar, the colonies were incubated at 35±2◦C for 18---24h andtestedfor thefollowingantibiotics: penicillin (10U),cefoxitin(30g),erythromycin(15g),clindamycin (2g),levofloxacin(5g),sulfamethoxazole---trimethoprim (1.25---23.75g),linezolid(30g),tetracycline(30g), gen-tamicin (10g) and rifampicin (5g). The plates were analysedaccordingtotherecommendationsoftheClinical andLaboratoryStandardsInstitute(CLSI,2018).8According
tothe diameter of the inhibition halo,the samples were classifiedassensitive,intermediateresistanceorresistant.
S. aureus ATCC25923 wasused to control the quality of
theantibioticdiscs,accordingtostandarddisc-diffusiontest procedures.
TheresearchwasapprovedbytheResearchEthics Com-mittee of the Santa Casade Misericórdiade Porto Alegre
Figure1 Sampleofdermatologist’sflowchart.
(protocoln◦9396017.5.0000.5335),UniversidadeFederalde CiênciasdaSaúde(protocoln◦ 69396017.5.0001.5345)and SecretariaEstadualdeSaúdedoRioGrandedoSul (proto-coln◦ 9396017.5.3002.5312). Alltheparticipants included inthestudysignedanInformedConsentTerm.
The data was entered into the Excel program and then exported tothe SPSS v. 20.0 for statistical analysis. Qualitativevariablesweredescribedbyfrequencyand per-centages.Symmetrically distributedquantitativevariables were described using the mean and standard deviation, whileforthosewithanasymmetricdistribution;themedian andtheinterquartilerangewereused.Categoricalvariables werecomparedusingtheChi-squaretestor Fisher’sexact test.Thequantitativevariableswerecomparedusing Mann-WhitneytestorStudentt-Test.Asignificancelevelof5%was consideredfortheestablishedcomparisons.
Regarding thesample size, withapproximately59 der-matologistspergroup,wewereabletodetectadifference of20percentagepointsinthefrequencyofbacterial colo-nization.Weconsideredabaselinecolonizationvalueof5% (inthecitedliterature,thevaluerangesfrom2.7%to10%), apowerof80%andasignificanceof5%.
Results
A total of 138 dermatologists were invited to participate in the study (Fig. 1). The characteristics of the 118 der-matologistswhosedeviceswereanalysed aredescribedin
table1.
Ofthedermatoscopesanalysed,46.6%hadgrampositive coccicoloniesonthelens and37.3% ontheon/offbutton (Table2).
Thefrequencyofgram-positivecocciwashigheramong males, but the difference was not statistically signifi-cant (Table3).The variables significantly associated with colonisationbygram-positivecocciwere:beingaresident. Attending a hospital or not attending exclusively in pri-vateoffice;Keepingthedermatoscopeinthecoatpocket; Usingthedermatoscopeatthehospital;Withinpatientsand; In the Intensive Care Unit (p<0.05). Using a smartphone adapterwasnotassociatedwithdermatoscope contamina-tion.
Bacterial contamination was more common among youngerdermatologists(Fig.2)andthosewihtlesstimeas dermatologist(Table4),andastatisticallysignificant rela-tionshipwasfoundbetweenthenumberofpatientstreated
per dayand thenumberof times theyusedthe dermato-scopeperday(Table4).
ThemicroorganismsmostfrequentlyfoundwereS.
epi-dermidis, S. hominis and S. warneri. S. aureus was only
detectedonthelens(Fig.3).
The highest resistance rates among the gram-positive cocci were found to be against penicillin, erythromycin, Sulfamethoxazole-Trimethoprim(SMT-TMP)andclindamycin (Table5).Cefoxitinresistancewas6.6%andno microorgan-ismwasresistanttolinezolid.
S. epidermidis presented a high rate of resistance to
penicillin,erythromycinand SMP-TMP,whereasS. hominis
presented greater resistance to erythromycin than peni-cillin. While S. capitis presented high resistance rates to severalantibiotics,nocaseofresistancetoclindamycinand gentamicin wasfound. The highest rates of resistance to penicillinwerefoundforS.warneriandS.haemolyticus.All isolatesofS.haemolyticuswereresistanttopenicillinand ithadthehighestfrequenciesofresistancetoclindamycin, tetracycline,SMT-TMPandgentamicin(Table6).
Discussion
The dermatoscopes were mainly colonized by bacteria fromthecutaneousmicrobiota(CoNS),themostfrequently found beingS. epidermidis, which is accordancewiththe literature.9,10Thismicroorganismhasbecomethemost
com-moncauseofprimarybacteraemiaandinfectionofmedical devices,suchascatheters,particularlyin immunocompro-mised individuals and neonates. In contrast toS. aureus,
whichismuchmorevirulentandsynthesizesanarrayof tox-insandother virulencefactors, themainknownvirulence factor associatedwithS.epidermidisisitsabilitytoform biofilmsandcolonizebiomaterials.Again,incontrasttoS.
aureus,whichiscommonlylocatedinthenasalmucosa,S.
epidermidiscanbe easilytransferred totheskin ofother
individualsthroughsimplecontact.11
BothS. hominis,the secondmostcommon
microorgan-ismfoundinourstudy,whichiscitedintheliteratureasone ofthethreeCoNSmostfrequentlyfoundinneonatalblood culturesandimmunosuppressedpatients,12andS.warneri,
the third most common microorganism identified in der-matoscopesinourstudy,whichsomearticlessuggestisthe secondmostfrequentCoNS,13,14 havethecapacitytoform
biofilm,15,16 and have been associated with bacteraemia,
septicaemia,andendocarditis.16,17
S. capitis rarely causes infection in adults, but a
decreased susceptibilitytovancomycinhasbeen reported and a clonal population of methicillin-resistant S. capitis
withvancomycinheteroresistancehasspreadamongseveral neonatalICUs in Franceandelsewhere.18 Ehlersson etal.
evaluated S. capitis isolates from neonatal hemocultures inSwedenandfounda75%cefoxitinandgentamicin resis-tancerate,only3%erythromycinresistance,andnocaseof resistanceeithertonorfloxacinorSMT-TMP.19
We found that the dermatoscope can carry S. aureus.
Thisbacteriacolonizesthesuperficiallayeroftheskin, sur-vivesfor a shortperiodof time,andis often acquired by healthprofessionalsduringdirectcontactwiththepatient (colonizedorinfected),environment,surfacesclosetothe patient,contaminatedproductsandequipment.20,21 Infact
Table1 Characteristicsofthedermatologistsinthesampleandtheuseofthedermatoscope.
Variable Descriptivemeasures
Age,years---mean±SD 36.4±8.4
Sex,n(%)
Male 16(13.5)
Female 102(86.5)
Timeasadermatologist,median---years(interquartilerange) 6.5(2---15) Wheredoyouattendpatients?---n(%)
Intheprivateoffice 47(39.8)
Athospital 25(21.2)
Intheprivateofficeandathospital 46(39)
Numberoftimesthedermatoscopeidusedperday---median(interquartilerange) 15(10---20) Amountoftimethedermatoscopeisusedduringconsultation,inminutes---median
(interquartilerange) 5(3---7) Modelofdermatoscope,n(%) DL100 6(5.1) DL200 2(1.7) DL3 24(20.3) DL4 34(28.8) Hybrid 42(35.6) MiniHeineorHeine 8(6.8) WellchAllyn 1(0.8) VeosCanfield 1(0.8)
Doesthedevicetouchthepatient’sskinduringtheexamination?---n(%)
Yes 92(78)
No 26(22)
Wheredoyoukeepthedermatoscope?---n(%)
Coatpocket 68(57.6)
Desktop 76(64.4)
Wardrobe 21(17.8)
Case 15(12.7)
Doyouusethedermatoscopeintheprivateoffice?---n(%)
Yes 102(86.4)
No 16(13.6)
Doyouusethedermatoscopeatthehospital?---n(%)
Yes 64(54.2)
No 54(45.8)
Doyouusethedermatoscopewithinpatients?---n(%)
Yes 39(33)
No 79(67)
DoyouusethedermatoscopeintheICU?---n(%)
Yes 20(17)
No 98(83)
Haveyouattendedaninpatientinisolationduetomultidrugresistantbacteriainthelast30days?---n(%)
Yes 15(12.7)
No 103(87.3)
Haveyouusedthedermatoscopeonaninpatientwithmultidrugresistantbacteriainthelast30days?---n(%)
Yes 2(1.7)
No 116(98.3)
Table1(Continued)
Variable Descriptivemeasures
Yes 92(78)
No 26(22)
Doyouuseasmartphoneadapter?---n(%)
Yes 27(22.9)
No 91(77.1)
SD,standarddeviation;ICU,intensivecareunit.
Table2 Frequencyofbacterialcolonizationbygram-positivecocciindermatoscopesandsmartphoneadapters.
Variable n/total Frequency(%) 95%CI
Bacterialgrowthinthedermatoscope(lensoron/off button)
70/118 59.3 49.9---68.3
Bacterialgrowthinthelens 55/118 46.6 37.4---56.0
Bacterialgrowthontheon/offbutton 44/118 37.3 28.6---46.7
Bacterialgrowthonsmartphoneadapter 10/27 37 19.4---57.6
CI,confidenceinterval.
Table3 Categoricalvariablesandtheirrelationtothepresenceofbacterialcontaminationonthelensorontheon/offbutton.
Variable Frequency(n) Contaminationbygram
positivecocci(%) p-Value Sex 0.581a Male 11 68.8 Female 59 57.8 Resident 0.013a Yes 33 75 No 37 50
Wheredoyouattend? 0.010a
Privateoffice 20 42.6
Hospital 18 72
Privateofficeandhospital 32 69.6
Wheredoyouattend? 0.005a
Onlyprivateoffice 20 42.6
Onlyhospitalorprivateofficeplushospital 50 70.4
Modelofdermatoscope 0.361a
DL100andDL200 4 50
DL3,DL4,VeosCanfield 37 62.7
Hybrid 26 61.9
WellchAllynorHeine 3 33.3
Doesittouchtheskin? 0.676a
Yes 56 60.9
No 14 53.8
Keepthedermatoscopeinthecoatpocket 0.019a
Yes 47 69.1
No 23 46
Putthedermatoscopeonthetable 0.819a
Yes 44 57.9
No 26 61.9
Table3(Continued)
Variable Frequency(n) Contaminationbygram
positivecocci(%)
p-Value
Yes 12 57.1
No 58 59.8
Storethedermatoscopeinacase 0.735a
Yes 10 66.7
No 60 58.3
Doyouusethedermatoscopeintheprivateoffice? 0.272a
Yes 58 56.9
No 12 75.0
Doyouusethedermatoscopeatthehospital? 0.001a
Yes 47 73.4
No 23 42.6
Doyouusethedermatoscopewithinpatients? <0.001a
Yes 33 84.6
No 37 46.8
DoyouusethedermatoscopeintheICU? <0.001a
Yes 20 100
No 50 51
Haveyouattendedpatientsinisolationduetomultidrugresistantbacteriainthelast30days? 0.143a
Yes 12 80
No 58 56.3
Haveyouusedthedermatoscopeonapatientwithmultidrugresistantbacteriainthelast30days? 0.513b
Yes 2 100
No 68 58.6
Doyoucleanthedermatoscope? 0.348a
Yes 52 56.5
No 18 69.2
Doyouuseasmartphoneadapter? 0.999a
Yes 16 59.3
No 54 59.3
ICU,intensivecareunit.
a Chi-squaredtest. b Fisher’sexacttest.
theon-offbuttonorsmartphoneadapter,placesmorelikely toberelatedtodirectcontactwiththeskinofthehealth professional.
Hands of health professionals may be persistently col-onized by pathogenic microorganisms (such as S. aureus,
gram-negativebacillioryeasts),whichincriticalareas,such asintensivecareunitsandunitswithimmunocompromised orsurgicalpatients,canplayanimportantroleasacause ofinfectionrelatedtohealthcare.22
In our study, cefoxitin resistance was considered low. Resistancetoerythromycinwasnotably highinS. hominis
isolates(83.3%),afactalreadymentionedinotherstudies.23
Szczuka et al. (2016) found an erythromycin resistance rateof 75% in isolatesfromblood andsurgical woundsof hospitalizedpatients.24 The highest rates ofresistance to
variousantibioticswereseeninS. haemolyticus,as previ-ouslyreported.23RecentstudieshavecitedS.haemolyticus
asthesecond CoNS,afterS.epidermidis, mostfrequently isolatedfromclinicalcases,includingsepsispatients.25---27
Figure2 Ageofdermatologistsandtheirrelationtothe pres-enceorabsenceofbacterialcontaminationondermatoscopes. StatisticTest:Studentt-test.Standarddeviationinthegroup withgram-positivecocci6.4.Standarddeviationinthegroup withoutgram-positivecocci9.8.
Table4 Numericalvariablesandtheirrelationtothepresenceorabsenceofbacterialcontaminationonthelensoronthe on/offbutton. Variable Presenceof gram-positivemedian cocci(interquartile range) Absenceof gram-positive-median cocci(interquartile range) p-Value
Timeasadermatologist,years 4(1---11.25) 11(4.25---18) <0.001
Numberoftimesthedermatoscopeisusedperday 15(10---20) 10(10---16.5) 0.004
Numberofpatientsseenperday 20(15---25) 15.5(12.25---20) 0.035
Dermoscopytimeperconsultation,minutes 5(3---7.25) 5(3---5) 0.881
Howmanytimesadaydoyouaccessyourmobilephone? 10(4.75---15) 10(5---15) 0.862
Statisticaltestused:Mann---Whitneytest.
Figure3 Gram-positivecocciidentifiedbyMALDI-TOFMS.
Table5 Antimicrobial resistanceprofileofgram-positive cocciisolatesobtainedfromdermatoscopesandsmartphone adapters. Gram-positivecocci Sensitivity Resistance Antibiotic n % n % Penicillin 26 23.6 84 77.4 Erythromycin 31 28.4 78 71.6 Clindamycin 75 68.8 34 31.2 Tetracycline 95 86.4 15 13.6 SMT-TMP 66 60.6 43 39.4 Cefoxitin 103 93.6 7 6.4 Gentamicin 104 94.5 6 5.5 Rifampicin 105 95.4 5 4.6 Levofloxacin 103 93.6 7 6.4 Linezolid 110 100 0 0 SMT-TMP,sulfamethoxazole-trimethoprim.
Thisisthefirststudyintheliteraturetoevaluate antimi-crobialresistanceofCoNSindermatoscopesandsmartphone adapters. Knowing the resistance pattern of CoNS in der-matoscopes, andonourownskin, isimportant giventhat this bacterial group can act as reservoir of antimicrobial resistant genes by horizontal transfer between staphylo-coccal species. Furthermore,they maybe acquired by S.
aureus,26,28,29andsubsequentlytransferredbetween
derma-tologistsandtheirpatients,especiallyphysiciansworkingin hospital settings where antimicrobial resistance rates are highest.26 According toacohortof2518patientsinIsrael,
identifyingtheCoNSresistancepatternsobtainedbyblood cultures,evenwhencontaminants,couldhelppredict mor-talityandcorrectempiricalantibiotictherapy.30
Amongthelimitations ofourstudyisthenon-screening ofgram-negativebacteria,fungi,andviruses.Moreover,the small number of adapters meant it we were unable bet-ter determine whetherthe differencesin frequency were statisticallysignificant.
Table6 Antimicrobialresistanceprofileoftheisolatesofthemostfrequentgram-positivecocciobtainedfromdermatoscopes andsmartphoneadapters.
Frequencyofresistanceamonggram-positivecocci(%)
Antibiotic S.epidermidis S.hominis S.warneri S.capitis S.haemolyticus
Penicillin 79.4 50 88.9 75 100 Erythromycin 73.6 83.3 55.6 50 80 Clindamycin 36.6 25 11.1 0 40 Tetracycline 15.1 8.3 0 25 40 SMT-TMP 44.4 25 22.2 50 60 Cefoxitin 6.8 0 0 25 20 Gentamicin 5.5 0 0 0 40 Rifampicin 4.1 0 0 25 0 Levofloxacin 5.5 0 0 75 0 Linezolid 0 0 0 0 0 SMT-TMP,sulfametoxazol-trimetropim.
Conclusions
Weidentifiedahighfrequencyofgram-positivecoccionthe tested devices. Staphylococcus epidermidis wasthe most frequently observed, both onthe lens, the on/off button andthesmartphone adapter.S. aureuswasdetectedonly onthelens.
This study concerns the association between the der-matologist and the contamination of dermatoscopes. Professionals should take measures to prevent contami-nation of their devices and cross-colonization with their patients.
Financial
support
Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior(CAPES), ConselhoNacionaldePesquisae Desen-volvimentoTecnológico(CNPq) andFundac¸ãodeAmparoà PesquisadoRioGrandedoSul(FAPERGS).
Authors’
contributions
MauríciodeQuadros:Statisticanalysis;approvalofthefinal versionofthemanuscript;conceptionandplanningof the study;elaborationandwritingofthemanuscript;obtaining, analysis,andinterpretationofthedata;effective participa-tioninresearchorientation;criticalreviewoftheliterature; criticalreviewofthemanuscript.
RobertoCarlosFreitasBugs:Approvalofthefinalversion of the manuscript;conception and planning of thestudy; obtaining,analysis,andinterpretationofthedata;critical reviewoftheliterature.
Renata deOliveiraSoares:Approvalofthefinalversion of the manuscript;conception and planning of thestudy; obtaining,analysis,andinterpretationofthedata;effective participationinresearchorientation.
AdrianaMedianeiraRossato:Approvalofthefinalversion of the manuscript;conception and planning of thestudy; elaborationandwritingofthemanuscript;obtaining, anal-ysis,andinterpretationofthedata;effectiveparticipation
in research orientation; critical review of the literature; criticalreviewofthemanuscript.
LisianedaLuzRocha:Approvalofthefinalversionofthe manuscript;conceptionandplanningofthestudy; elabora-tionandwritingofthemanuscript;obtaining,analysis,and interpretationofthedata;criticalreviewofthemanuscript. PedroAlvesd’Azevedo:Statisticanalysis;approvalofthe final version of the manuscript; conception and planning of the study; elaboration and writing of the manuscript; obtaining,analysis,and interpretationof the data; effec-tiveparticipationinresearchorientation;criticalreviewof theliterature;criticalreviewofthemanuscript.
Conflicts
of
interest
Nonedeclared.
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