w w w . j c o l . o r g . b r
Journal
of
Coloproctology
Original
Article
Association
between
pluviometric
index
and
the
occurrence
of
acute
appendicitis
Djalma
Ribeiro
Costa
a,b,c,∗,
Fabrícia
Leal
Bezerra
d,
Germano
de
Sousa
Leão
d,
Lucas
Alexandre
Gonc¸alves
do
Nascimento
Gomes
d,
Diego
Coimbra
Alencar
e,
Robson
David
de
Araújo
Lial
e,
Max
Brandão
de
Oliveira
faUniversidadeFederaldoPiauí(UFPI),ProgramadePós-graduac¸ãoemEstatística,Teresina,PI,Brazil bHospitalInfantilLucídioPortella,Teresina,PI,Brazil
cHospitaldeUrgênciadeTeresinaProf.ZenonRocha(HUT),Teresina,PI,Brazil dUniversidadeFederaldoPiauí(UFPI),Teresina,PI,Brazil
eFaculdadeIntegralDiferencial(FACID),Teresina,PI,Brazil
fUniversidadeFederaldoPiauí(UFPI),DepartamentodeEstatística,Teresina,PI,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received12December2016 Accepted19July2017
Availableonline12August2017
Keywords:
Appendicitis,associationwith Atmosphericprecipitation Measuresofoccurrenceofdiseases Statisticalanalysis
a
b
s
t
r
a
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t
Background:Epidemiologicalstudiesdemonstrate,forunknownreasons,theprevalenceof appendicitisinthesummerandinyoungmaleadults,andtherearecontroversiesabout itsassociationwiththerainyseason.TherearenostudiesintheStateofPiauíaboutsuch association.
Objective:Toestablishanassociationbetweentheoccurrenceofappendicitisandthe plu-viometricprecipitationindex.
Methodology:Thisisacross-sectionalstudythatwascarriedoutusingthedatabaseofthe pathologyserviceatapublicemergencyhospitalinPiauí,andthepluviometricprecipitation indexintheStateofPiauífromJanuary2009toApril2014,withdatafromtheNational InstituteofMeteorology.Descriptivestatisticsandassociationmeasureswereappliedusing thePearsoncorrelationcoefficientandthe2test.
Results:We foundapredominanceofappendicitiscasesinmalesubjects,from11to20 yearsofage,withapredominanceofthemonthlymeanofappendicitiscasesinthesecond semester,whichconformstothedryseasonintheStateofPiauí.Pearson’scorrelation coefficientwas−0.260.
Conclusion: Thereisanassociationbetweentheoccurrenceofappendicitisandthemonths oftheyear;however,thisisaweaknegativecorrelationbetweenthemonthlymeanofcases ofappendicitisandmonthlypluviometricprecipitationaverageintheStateofPiauí.
©2017SociedadeBrasileiradeColoproctologia.PublishedbyElsevierEditoraLtda.This isanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/ licenses/by-nc-nd/4.0/).
∗ Correspondingauthor.
E-mail:djalmacosta1@gmail.com(D.R.Costa). http://dx.doi.org/10.1016/j.jcol.2017.07.003
Associac¸ão
entre
índice
de
precipitac¸ão
e
a
ocorrência
de
apendicite
aguda
Palavras-chave:
Apendicite,associac¸ão Precipitac¸ãoatmosférica Medidasdeocorrênciade doenc¸as
Análiseestatística
r
e
s
u
m
o
Contexto: Estudosepidemiológicosdemonstram,porrazõesdesconhecidas,opredomínio doscasosdeapendicitenoverãoeemadultosjovensdosexomasculino,havendo contro-vérsiassobresuaassociac¸ãocomoperíodochuvoso.NãoháestudosrealizadosnoPiauí sobreestaassociac¸ão.
Objetivo: Estabelecer uma associac¸ão entre a ocorrência de apendicite e o índice de precipitac¸ãopluviométrica.
Metodologia: Realizou-seumestudotransversalatravésdobancodedadosdoservic¸ode patologiadeumhospitaldeemergênciapúblicodoPiauíedoíndicedeprecipitac¸ãono Piauídejaneirode2009aabrilde2014doInstitutoNacionaldeMeteorologia.Aplicou-se estatísticadescritivaemedidasdeassociac¸ãopelocoeficientedecorrelac¸ãodePearsone pelotestequi-quadrado.
Resultados: Encontrou-seumpredomíniodoscasosdeapendicitenosexomasculino,de 11a20anosdeidade,predomíniodamédiamensaldecasosdeapendicitenosegundo semestre,coincidindocomoperíododeestiagemnoPiauí.Ocoeficientedecorrelac¸ãode Pearsonfoide-0,260.
Conclusão: Existeumaassociac¸ãodaocorrênciadeapendicitecomosmesesdoano,porém setratadeumafracacorrelac¸ãonegativaentreamédiamensaldecasosdeapendicitecom amédiadaprecipitac¸ãopluviométricamensalestadualnoPiauí.
©2017SociedadeBrasileiradeColoproctologia.PublicadoporElsevierEditoraLtda.Este ´eumartigoOpenAccesssobumalicenc¸aCCBY-NC-ND(http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Introduction
The cecal appendix is a blind-end, tubuliform structure locatedinthelargeintestine.Itssizeisvariable;itisestimated that the appendix measures, on average, 5cm. The cecal appendixisbelievedtohaveabsorptive, bacterial prolifera-tion(toestablishtheintestinalflorabalance),andimmunity (throughtheproductionofwhitebloodcells)functions. Nev-ertheless, its real function in the human species remains elusive.1
Acute appendicitis is the mostcommon surgical emer-gency inyoung adults,with apredominance ofmales. An incidenceratio of1.4mento1womanisestimated.Inthe UnitedStates, 11 out of10,000 Americans willsuffer from appendicitis throughouttheir lives.The etiology of appen-dicitishasnotyetbeenfullyelucidated.Themostaccepted theoriesare:viral,bacterial,fungal,andparasitic;but these theoriesarenotexclusiveandraisetheneedfor pathophysi-ologicalandepidemiologicalclarifications.2,3
The morbidity and mortality of acute appendicitis are directlyrelatedtothetimeofevolution,anditsmostcommon complicationisitsperforation.Itisestimatedthat,after36h ofevolution,theriskofperforationis16–36%,withanincrease of5%inevery12h.Inturn,mortalityisaconsequenceofthe timeofevolution,thatis,thepresenceofperforation.When thereisnoperforation,mortalityinpatientswithappendicitis is0.08%.Otherwise,thispercentageincreasesto0.51%.3
Theaveragecostsofanappendectomyworldwideareof theorderofUS$28,000.Thesecostsdonottakeintoaccount complicationsoranextendedhospitalstay.Thesevaluescan reachmorethanUS$180,000.4
In Brazil,since2003, the Braziliangovernment, through theMinistryofHealth,hasinstitutedtheNationalEmergency and UrgencyPlan,withtheaimoforganizingand structur-ingthecountry’semergencies.Withrespecttoappendicitis, anabdominalpainprotocolwasdevelopedwiththeaimof facilitatinganearlydiagnosis,inordertopromote,asquickly aspossible,thepatient’sreferralandtreatment.Thegoalis alwaysthesame:toreducemorbidityandmortality,inorder topromotehumanization incareand reducepublichealth spendings.5
Recently,severalepidemiologicalstudieshavereporteda historicalreductionintheoccurrenceofappendicitis, preva-lenceinindividualsaged10–19years,andaseasonalbehavior initsincidence.2
Inmostcountries, appendicitisoccursmoreofteninthe summer months; but this season assumes very different aspects,dependingonthecontinentandonthecountry, espe-ciallywithregardtothepluviometricindex.6InBrazil,studies
onthisassociationwerenotrecentlypublishedinBireme;the lastofthesestudieswaspublishedin1992.7Thepresentstudy
aimstoinvestigatetheexistenceofanassociationbetween pluviometricindexintheStateofPiauíandtheoccurrenceof confirmedcasesofacuteappendicitisseenatpublichospitals inTeresina–PI.
Methodology
medicalrecordofthepatients,inordertoobtaininformation onpatientidentification,his/herorigin,andageatthetimeof diagnosisofappendicitis,andreportsofthesurgicalspecimen usedbythePathologyServiceforthediagnosisofappendicitis. AllcaseswhoseoriginwasfromanotherfederativeState orthatdid nothave adefinedorigin,andalsothose cases whosehistopathologicalreportshadadifferentdescriptionof appendicitis(malignantorbenignneoplasia)wereexcluded.
TheHospitaldeUrgênciadeTeresinaProf.Zenon Rocha (HUT)isthelargestpublicemergencycenterintheStateof Piauíandreceivespatientsfromalloveritsterritoryandfrom bordercitiesintheStateofMaranhão,thankstothefactthat amongallthepublichospitalsofthatCapital,thisCenteris providedwiththegreatestresourcesforlaboratoryand imag-ingexamsandintermsofclinicalbody.
The pluviometric data for the State of Piauí from Jan-uary 2009 to April 2014 were obtained by consulting the database of the National Meteorological Institute (INMET) website.Informationwasobtainedonthemonthly pluviomet-ricprecipitationaverageinmillimeters(mm)intheStateof Piauíforeachofthemonthsconsideredinthisstudy.Foreach monthoftheyear,asecondmeanofthemonthlyaveragesfor eachyearincludedinthesurveywasgenerated.8
ThedatawerecollectedandcomputedinaMicrosoftOffice Excel2016®worksheetandtransposedtoaspreadsheetofthe IBMSPSS(version20)software;inthislastprogram, descrip-tivestatisticsand inferentialstatisticswerecalculated.The casesofappendicitiswerestudiedbyage,monthlymeanof casesofappendicitis,andmonthlypluviometricprecipitation average(inmm)intheStateofPiauífortheintervalstudied. Thefrequencyofcaseswasalsocalculatedaccordingto gen-der,agegroup,origin(Teresina,orPiauí’s countryside),and monthoftheyear.Ap-value<0.05wasconsideredas statisti-callysignificant.
Aftercalculatingthemeasuresofcentraltendencyand dis-persion,chartswereelaboratedforapreliminaryanalysis.In inferential statistics,inturn,we testednormality withthe Kolmogorov–Smirnovtest,atacriticallevelof5%.Amongthe quantitativevariables(monthlymeanofcasesof appendici-tis,andmeanofmonthlypluviometricprecipitationaverages intheStateofPiauí),weelaboratedascatterplotand calcu-latedthePearson’scorrelationcoefficient.Amongcategorical or categorized variables, we evaluated the presence of an associationbetweenthevariableswiththeapplicationofthe Pearson’schi-squaredtest,inaccordancewithCochran’srules (thetotalsampleshouldbegreaterthan25;atmost,20%ofthe expectedvaluesshouldbelessthan5.0;andnoexpectedvalue shouldbelessthan1.0).9,10
We used the strength of the association through the Pearson’scorrelation to measure the degree ofassociation betweenvariables,thatis,|r|=0meansnocorrelation,upto 0.3indicatesaweakcorrelation,upto0.6suggestsaregular correlation,upto0.9meansastrongcorrelation,from0.9to1 indicatesaverystrongcorrelation,and|r|=1impliesaperfect
correlation.9
The chi-squared test is classified as an association, adhesion or adjustment, and proportions or heterogene-ity test. We reserved the first option in order to evaluate the existence of an association between two categorical variables,andthesecondoptionwasusedtodetermineifthe
Table1–Agestratificationbygender. Age
group
Gender Gender
index (M:F)
2 p-Value Total
Female Male
0–10 137 258 1.88 37.06 <0.0001 395
11–20 226 404 1.78 50.29 <0.0001 630
21–30 170 337 1.98 55 <0.0001 507
31–40 108 218 1.28 37.11 <0.0001 326
41–50 62 131 2.11 24.66 <0.0001 193
51–60 53 107 2.01 18.22 <0.0001 160
61–70 37 75 2.02 12.89 0.0003 112
71–80 21 42 2 7 0.0082 63
>80 5 15 3 5 0.0253 20
Total 819 1587 1.93 245.1 <0.0001 2406
Source:DatabaseofthePathologyService,HospitaldeUrgênciade TeresinaProf.ZenonRocha(HUT),2016.
Note:Regardinggender,H=male;M=female.2referstothe
Chi-squaredtestofPearson.
categoricalvariables’dataadjustedtoanexpectedor theoret-icaldistribution.Thethirdoption,whichwasnotusedinthis study,servestocomparetwoormorepopulationsinrelation toacategoricalvariable.TheYatescorrectionwasreserved only for2 testswith adegree offreedom (d.F.)=1 in
sin-gle inputtableswith twocategories,orin2×2tables.The Yatescorrectionconsistsofsubtracting0.5fromeachabsolute differencebetweenobservedandexpectednumbers,before calculatingthedifferencesquared.9
Thisstudydidnotconferbioethicalormedicalriskstothe study subjectssincepatientswere notdirectly approached. This study includedonlysecondary datafrom information systems,beinginlinewiththeguidelinesdeterminedbythe TreatyofHelsinki.Theinformationisbeingkeptunderthefull confidentialityoftheauthors;therefore,itmaybemade avail-abletotheeditorsofthejournalatanytime,uponexpressand officialrequest.
Theprimaryandsecondaryinformationinferredthrough thisresearchisofinteresttoPublicHealth,consideringthat suchinformationmay serveas atoolforlocal administra-torsintheprocessofevidence-baseddecisionmakingthrough localepidemiologicalobservations.
Results
FromJanuary2009toApril2014,3793casesofacute appen-dicitisoperatedintheHospitaldeUrgênciadeTeresinaProf. Zenon Rocha(HUT)were recorded,ofthese,2426casesdid not meetthe exclusion criteria ofthe study. Amongthese cases,therewere1599menand827women,aged0–92years (mode=12 years, median=23.88 years, mean=28.16 years, andstandarddeviation=18.88years),totaling2406caseswith validdata.
Table2–Acuteappendicitiscases’counting,according tothemonthofdiagnosisandthecorrespondingyear. Monthof
diagnosis
Diagnosisyear Total Mean
(cases/year) 2009 2010 2011 2012 2013 2014
January 3 28 30 33 59 42 195 39
February 1 34 49 35 53 30 202 40.4
March 5 52 24 43 59 62 245 49
April 0 45 25 24 63 39 196 39.2
May 0 37 34 39 60 – 170 42.5
June 4 37 28 21 55 – 145 36.25
July 11 29 40 0 44 – 124 31
August 40 46 52 61 70 – 269 67
September 37 44 25 45 46 – 197 49.25
October 42 44 38 65 39 – 228 57
November 49 53 28 60 51 – 241 60.25
December 30 66 30 47 41 – 214 53.5
Total 222 515 403 473 640 173 2426
Source:DatabaseofthePathologyService,HospitaldeUrgênciade TeresinaProf.ZenonRocha(HUT),2016.
1252(51.6%)ofthecaseswerefromtheinterioroftheState, andtheothercaseswerefromtheCapital,withnostatistically significantdifference(2:2.508,1d.F.andp-value=0.1133).
Thecasesofacuteappendicitisweredistributedaccording tomonthsandyears(Table2).Exceptforthefirstsixmonthsof 2009,allothermonthshaveverysimilarabsolutefrequencies, andatfirst,itisnotpossibletoperceiveapatternof distri-butionofcasesoverthemonths.However,withtheuseofa non-skewedestimator(themeannumberofcases),itwas pos-sibletodemonstrateapredominanceofcasesinthesecond halfoftheyear,withapeakinAugust(Fig.1).
Bystudyingthemonthlypluviometricindexaverageover theperiodstudied,wewereabletoobserveahigher precipita-tioninthefirstsemester,withasignificantnadirinthesecond halfoftheyear(Table3).Thisfindingallowedustoinferthe existenceoftwowell-definedseasonsinthestateofPiauí:the rainyseasonandthedryseason(Fig.2).
Mean n
umber of cases of appendicitis
J
an
uar
y
F
ebr
uar
y
March Apr
il
Ma
y
J
une July August September October No
vember
December
Month
60
50
40
30
20
Fig.1–Meannumberofcasesofappendicitisduringthe monthsfromJanuary2009toApril2014.
Source:DatabaseofthePathologyService,Hospitalde
UrgênciadeTeresinaProf.ZenonRocha(HUT),2016.
Table3–Monthlypluviometricprecipitationaveragein theStateofPiauífromJanuary2009toApril2014.
Month Year Mean
2009 2010 2011 2012 2013 2014
January 4.89 3.71 5.59 3.01 5.18 3.27 4.27 February 6.88 3.21 7.99 5.45 2.68 7.07 5.54
March 8.11 6.39 8.39 5.33 5.28 5.4 6.48
April 11.37 5.85 6.84 2.27 5.51 5.98 6.30
May 7.8 1.67 3.88 0.82 2.07 – 3.24
June 4.89 1.39 0.71 0.87 0.65 – 1.70
July 0.73 0.2 0.78 0.126 0.67 – 0.50
August 0.157 0.02 0.217 0.008 0.18 – 0.11
September 0.05 0.043 0.03 0 0.19 – 0.06
October 2.53 2.2 2.53 0.041 0.497 – 1.55
November 0.834 1.7 1.99 1.84 1.934 – 1.65
December 3.37 4.8 0.98 1.85 3.79 – 2.95
Total 4.30 2.59 3.32 1.80 2.38 5.43 –
Source:NationalInstituteofMeteorology(INMET),2016.
Thedistributionofthemonthlymeansofcasesof appen-dicitisandofthemeansofmonthlypluviometricprecipitation averagesintheStateofPiauíwasnormal,accordingtothe Kolmogorov–Smirnov test (p-value=0.20); thus, a Pearson’s correlationwasobtained.
Afterobservinganinversegraphicassociationbetweenthe monthlymeanofappendicitiscasesversusmonthsoftheyear, andbetweenthemeanofaverageannualpluviometric pre-cipitationaveragesintheStateofPiauíversusmonthsofthe year,weperformedananalysisusingthescatterplotanda calculation ofthe Pearson’scorrelationcoefficient between themonthlymeansofappendicitiscasesandthemeansof monthlypluviometricprecipitation averagesinthe Stateof Piauí, resultingin acoefficient=−0.260 (weaknegative cor-relation) and inascatterplotwithout awell-definedtrend (Fig.3).
Mean of monthly pluviometr
ic precipitation a
ver
ages
(in mm/month) in the State of Piauí
6
4
2
0
J
an
uar
y
F
ebr
uar
y
March Apr
il
Ma
y
J
une July August September October No
vember
December
Month
Fig.2–Meansofmonthlypluviometricprecipitation averages(inmillimeters)fromJanuary2009toMay2014in theStateofPiauí.
Mean of monthly counts of appendicitis cases
Mean of monthly pluviometric precipitation averages in the State of Piauí
60,00
50,00
40,00
30,00
20,00
,00 2,00 4,00 6,00
Fig.3–Meansofmonthlyappendicitiscasesbymeansof monthlypluviometricprecipitationaverages.
Sources:SecondarydataobtainedfromthestudyofINMET
dataandfromthePathologyService,HospitaldeUrgência deTeresinaProf.ZenonRocha(HUT),2015and2016.
Discussion
Theepidemiologicalstudyofappendicitishasbeenthefocus ofresearchersthroughoutthe20thcentury.Inthequestfor causality,therearereferencestoitsassociationwithviral dis-easesknowntobeseasonal,suchasinfluenza. Timeseries obtainedfrom1970to1995demonstrateasimilargraphical behaviorbetweeninfluenzaversusunperforatedappendicitis andabsenceofatemporalrelationshipbetweenappendicitis
versusenteritis.11
InanationalepidemiologicalreviewinTaiwanforaperiod of10 years,theauthors stratifiedthe occurrenceof appen-dicitisaccordingto the year’sseasons,taking into account the gender factor, withcurves with similar tendencies for menand women,and differentcurvesastothefrequency, that was higher for males in all monthsof the year. The peakincidenceofappendicitisoccursinthemonthsofMay throughJuly,withnadirsbetweenAugustandFebruary. Coin-cidentally, the authors demonstrated a positivecorrelation between the incidence of appendicitis and environmental temperature.Ontheotherhand,itshouldbenotedthatthe monthsofMay toJulyshowthe highestrainfallrecords in Taiwan.12,13
ThestudybyRakeshetal.defines,inIndia,threeseasons: summer,rainyseason,andwinter.Therewasapredominance ofcasesofappendicitisinthesummer,andnotintherainy season,aswouldbeexpectedbythepreliminaryassociation establishedbetweenpluviometricprecipitationandthe occur-renceofviraldiseases.However,thestudybyOguntolaetal. showedthat68%ofthecasesofthediseaseoccurredinthe rainyseason,whichgoesfromApriltoSeptemberinNigeria. Thus,itcanbeassumedthatotherfactors–asyetunclarified –areassociated.14,15
Thefindingsofanassociationbetweentheoccurrenceof appendicitisandmonthsoftheyearledJangratoproposea hypothesis,ofapossibleassociationalsowiththedaysofthe week.Thesameauthorstudiedtheseasonalityof appendici-tisinNorthernIndianchildrenthroughoutthemonthsand daysoftheweek,concludingthatthereweremorecasesof appendicitis between the monthsofJulyand October, and that,duringtheweek,therewasapeakfrequencyonFridays.16
In the Federal District, Brazil, Vianna et al. observed a peakofincidencebetweenFebruaryandJuly,apredominance of casesamong individuals aged11–20 years,and a slight predominanceinmales(51.9%versus48.1%).Thedatafrom theseinvestigatorsareinlinewithstudiesmentioneda pri-ori, consideringthatthemonthsofFebruarytoJulyinclude twoseasons:summer(historicallyarainyseason)andautumn (historicallyanon-rainyseason),inwhichveryhigh temper-aturesandlowairhumidity,orlongperiodsofprecipitation andstrongwinds,canberegistered.7,17
Therefore,thereisanassociationbetweentheoccurrence ofappendicitisandthemonthsoftheyear,withdifferences amongcountries; inaddition, its association withthe plu-viometricprecipitation indexisverycontroversial.Thereis nostrongscientificevidenceonthesubject,butregionalized studies(citedabove)thatdemonstratewell-establishedlocal patternshavebeenpublished.
Conclusion
Withthestudyofthemonthlyaveragesfortheintervalfrom January2009toApril2014,itwaspossibletoverifya predom-inance ofcasesofacuteappendicitis inthesecond halfof the year.Itwasalsopossibletoverify theexistenceoftwo well-definedseasons,usingthemonthlypluviometric precip-itationaverageintheStateofPiauí:arainyseasoninthefirst semesterand adry seasoninthesecond semester. There-fore,anannualdichotomyforbothvariableswasperceived, whichenabledustocorrelatethemwiththePearson coeffi-cient.Wefoundaweaknegativecorrelation,thatis,thehigher themonthlypluviometricprecipitationaverage,thelowerthe meanofmonthlycasesofappendicitis.
Theexistenceofcontroversialstudiesintheliteraturedoes notallowustoaffirmthatthefindingsdescribedabove coin-cidewiththefindingsofallcitedauthors.Ontheotherhand, ourstudyshowsalocalreferentialofthepatternofoccurrence ofappendicitistotheclimaticconditionsoftheStateofPiauí.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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