The
current
spectrum
and
prevalence
of
intestinal
parasitosis
in
Campania
(region
of
southern
Italy)
and
their
relationship
with
migration
from
endemic
countries
Alberta
Belli
a,
Maria
Grazia
Coppola
b,
Luciana
Petrullo
b,
Gennaro
Lettieri
c,
Cristiana
Palumbo
c,
Chiara
Dell’Isola
c,
Riccardo
Smeraglia
b,
Maria
Triassi
a,
Enea
Spada
d,
Pietro
Amoroso
c,*
a
DepartmentofPreventiveMedicalSciences,UniversityofNaplesFedericoII,Naples,Italy
b
UnitofMicrobiology,CotugnoHospital,AORN‘‘OspedalideiColli’’,Naples,Italy
c
VIDivisionofInfectiousDiseases,CotugnoHospital,AORN‘‘OspedalideiColli’’,Naples,Italy
d
DepartmentofInfectious,ParasiticandImmuno-mediatedDiseases,IstitutoSuperiorediSanita`,Rome,Italy
1. Introduction
Intestinalparasitesrepresentamajorpublichealthproblemin developing countries. In 2004, the World Health Organization (WHO)estimatedthat3.5billionpeople,mostly intropicaland sub-tropical areas of the world, were infected with intestinal parasites, and that 450 million people, mainly children, had evidenceofrelateddisease.1
Mostparasitesareubiquitous,anduntilafewdecadesago,Italy was alsoconsidered tobe an endemic area for someof them. Indeed, before the year 2000, different studies reported the circulationof numerousprotozoaand helminthsin ourcountry (e.g.Entamoebahistolytica,Giardiaduodenalis,Dientamoebafragilis, Trichuristrichiura,Strongyloidesstercoralis,Ancylostomaduodenale, Ascaris lumbricoides, Hymenolepis nana, Taenia saginata/Taenia solium,Echinococcusgranulosus,andEnterobiusvermicularis),some ofwhichareassociatedwithmajorillnesses.2–5
The current opinion is that the incidence of intestinal parasitosis in Italy is low, with only sporadiccases identified, whiletheoccurrenceofdiseaseoutbreaksrepresentsarareevent.
ARTICLE INFO
Articlehistory:
Received20October2013
Receivedinrevisedform11March2014 Accepted20April2014
CorrespondingEditor:RaquelGonza´lez, Barcelona,Spain
Keywords: Intestinalparasitosis Immigrants
Chronicboweldiseases Protozoa
Helminths
SUMMARY
Background:In Italy,the currentclinical–epidemiological featuresof intestinal parasitosis and the impactofrecentmassivemigrationflowsfromendemicareasontheirdistributionarenotverywell known.
Methods:An analysiswas carriedout involving 1766patients(720natives and1046immigrants) observedduringtheperiod2009–2010(the‘currentgroup’)and771nativepatientsobservedduringthe period1996–1997(the‘historicalgroup’),atimeatwhichimmigrationintheareawasminimal.Patients wereanalyzedforintestinalparasitosisatfourhealthcarecentresinCampania.
Results:Awidevarietyofintestinalparasiteswasdetectedinthestudysubjects.Immigrantshada significantlyhigherprevalenceofparasitosisandmultiplesimultaneousinfectionsthannativesinboth groups.Inbothstudygroupsofnatives,thedetectionofatleastoneparasitewassignificantlyassociated withahistoryoftraveltoendemicareas.Amongimmigrants,wefoundaninversecorrelationbetween thefrequencyofparasitedetectionandtheamountoftimespentinItaly.Nocirculationofparasiteswas foundamongcontactsofparasitizedpatients.
Conclusions: Intestinal parasites are still a cause of intestinal infection in Campania. Although immigrantshaveasignificantlyhigherprevalenceofparasitosisthannatives,thisdoesnotincreasethe riskofinfectionforthatpopulation.Thisislikelyduetothelackofsuitablebiologicalconditionsinour area.
ß2014TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases. ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(
http://creativecommons.org/licenses/by-nc-nd/3.0/).
* Correspondingauthor.Tel./Fax:+390817067306. E-mailaddress:pietro.amoroso@gmail.com(P.Amoroso).
ContentslistsavailableatScienceDirect
International
Journal
of
Infectious
Diseases
j o urn a l hom e pa ge : ww w. e l s e v i e r. c om/ l o ca t e / i j i d
http://dx.doi.org/10.1016/j.ijid.2014.04.021
1201-9712/ß2014TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/3.0/).
However,sincethereportingofmostintestinalparasitosisisnot mandatoryinItaly,thereislittleinformationonrecentclinical– epidemiological features.6–9 Furthermore, there are no data
concerningtheimpactthat massivemigration flowsduringthe lasttwodecades,mostlyfromendemicareassuchasAfricaand southern Asia, may have had on the distribution of intestinal parasitosis in Italy. Indeed, a prevalence of intestinal parasites ranging from 20% to 60% has been reported in immigrants, dependingon thecountryoforiginanddifficultiesencountered during the migrant’s travel, with the highest prevalence rates observedinthoserecentlymigratedandinthosecomingfrom Sub-SaharanAfrica.10–18
Since, at present, immigrants represent 8% of the Italian population,19itmightbejustifiedtoassumethatahighprevalence
ofchroniccarriersofintestinalparasitesamongimmigrantscould resultinanincreaseinthecirculationandtransmissionofthese infectiousagents.
Theaimofthisstudywastoinvestigatetheprevalenceandthe spectrumofcurrentintestinalparasitesinCampania,aregionof southern Italy, and to assess the potential epidemiological consequencesofmigrationfromendemiccountriestothisregion. Campaniaisthesecondmostpopulous(5769750inhabitants)and the most densely populated region of Italy (428 inhabitants/ km2).20 The population of Campania region includes a not
negligible percentage of immigrants, estimated to be approxi-mately3%(200000individuals)oftheresidentpopulation.15In
ordertoachievetheobjective ofthestudy,a groupofpatients observedduring2009–2010includingbothnativeandimmigrant people,andagroupofanativepatientsobservedin1996–1997 (whenimmigrationwasnot presentyetorwasminimal),were comparedandanalyzedforintestinalparasitosisatfourhealthcare centresinCampania.
2. Materialsandmethods
Thisprevalencestudywasconductedontwogroupsofpatients observedduringdifferenttime-periods.Thefirstgroup,observed during2009–2010,included1776consecutivepatients(without adoptinginclusionorexclusioncriteria)withintestinalsymptoms whowerereferredtoahealthcareserviceforimmigrantsandthe regionalhospitalforinfectiousdiseasesinNaples,wheretheywere testedforintestinalparasites.Throughoutthisarticle,allpatients recruitedduring2009–2010arereferredtoasthecurrentpatient group. Among these, 720 were native (44% female, mean age 3816years)and1046wereimmigrants(27%female,meanage 249years),whoweremostlyfromCentralAfrica(46%),theIndian sub-continent(23%),andNorthAfrica(16%).
Allpatientsshowedclinicalsigns,mainlychronic,compatible withintestinalparasitosis(fever,bloody diarrhoeaordiarrhoea, irritable bowel syndrome, anaemia, eosinophilia, itching, and dermatitis).Inmostofthepatients,thesesymptomsrepresented theprimary cause of hospitalization, while in about a third of patients, these symptoms coexisted with other pathological conditions.Inparticular,96patientswereHIV-positive(54natives and42immigrants)andallofthembut10(twonativesandeight immigrants)wereundergoinghighlyactiveanti-retroviraltherapy (HAART).ThetimeofarrivalinItalywasknownforallimmigrants participatinginthestudy.
Theresultsfoundinthisgroupofpatientswerecomparedto thoseobtainedinagroupof771consecutivenativepatients(38% female,meanage3910years;60HIV-positive,ofwhomonlyeight wereundergoingHAART)referredforgastrointestinalsymptomsto theparticipatingunitsduring theperiod1996–1997,when immi-grationwasnotpresentyetorwasminimalinthisarea.Inthepresent study, these 771patientsare referred to asthehistorical patient group.
Nopatientineitherthecurrentorhistoricalgroupwasagedless than12years.
Inafurtherinvestigationtoanalyzethepotentialinter-human transmissibility of parasites, we studied the households of 48parasitizedimmigrants,foratotalof246subjects.
Faecalspecimenscollectedfromallpatientsparticipatinginthe studywereanalyzedthroughdirectmicroscopicexamination,as wellas after fixationand concentration. For direct microscopic examination,1–2goffaecalspecimenweredissolvedin1–2mlof normal saline to show the mobile forms, if present, and with Lugol’ssolutionforstainingofnucleiandprotozoaintracellular structures.Smearswerepreparedfromsamplesinnormalsaline for staining by modified Ziehl–Neelsen method (for Coccidia), Weber method(for Microsporidia), and Giemsacolouration for protozoa. Specific fluorescent monoclonal antibodies were also usedfortheidentificationofCryptosporidiumspp,G.duodenalis,and E.histolytica/dispar.21
Fortheconcentration,2–3goffaecalspecimenwerefixedin5% formalin(dilutionratio1:4).Allsampleswerethenanalyzedwith theclassicalconcentrationtechniqueofsedimentation.Moreover, flotationthroughtheFLOTACdualpellet400techniquewasalso performed fortheconcentration ofspecimens fromthecurrent prospectivegroupofpatients,usingtwofloatingsolutions(SF4: waterysolutionofsodiumnitrate(specificweight=1200);SF7: watery solution of zinc sulphate (specific weight=1350)); the pellet wasfirsttreated withdiethyl ether (2ml diethyl ether+ 10mlsalinesolution).22–27NoDNA-basedmethodswerecarried
outtodifferentiateEntamoebahistolyticafromE.dispar.Because this differentiationcannotbemadeonamorphologicalbasis,it wasbasedonly onclinical criteria(i.e.,thepresenceofspecific clinicalpatternsofintestinalamoebiasisforE.histolyticathatare lackingforE.dispar,thislatterspeciesbeingnon-pathogenic).28
Onlyonesampleperpatientwasavailablein62%ofthecases, twosampleswereavailablefor22%,andthreeormoresamples were available for 16%, for a total of 3815 stool specimens examined.Thenumbersofsampleswerehomogeneously distrib-utedamongallgroupsofpatients.
The United Kingdom National External Quality Assessment Service(UKNEQAS;DepartmentofClinicalParasitology,Hospital for Tropical Diseases, London) provided specimens for faecal parasitology quality control. All samples were processed and analyzedbythesameteamofparasitologists.
2.1. Statisticalanalysis
StatisticalanalyseswereperformedusingtheStudent’st-test for comparisons between means. For categorical variables, differences between groups were calculated by Chi-square test andFisher’sexacttest,whennecessary.Atwo-sidedp-valueofless than 0.05 was considered statistically significant. Analysis for linear trendsinproportions wasconductedusing theextended Mantel–Haenszel test. All statistical analyses were performed usingStataversion11.2(StataCorpLP,CollegeStation,TX,USA). ThestudywasapprovedbytheEthicsCommitteeofCotugno Hospital. All participating patients provided signed informed consent.
3. Results
3.1. Overallprevalenceofintestinalparasitosis
Considering all patient groups (current natives, current immigrants, and historical natives), a total of 1065 intestinal parasites were found in 664 patients. Most of the parasites identified wereprotozoaconsidered asnon-obligate pathogens, whichwereoftenfoundinconjunctionwithpathogenic species
(Table1).Noassociationsbetweenageand/orsexandprevalence ofthedifferentparasiteswerefound(datanotshown).
Among all patient groups, Blastocystis spp was the most frequentlydetectedparasite(410totalcases),andin48%ofcases itcoexistedwithoneormoreotheragents.
3.2. Prevalenceofintestinalparasitosisamongnativepatients Currentandhistoricalnativepatientswereparasitizedin9.6% (69/720)and 11.4% (88/771)of cases,respectively (p=0.28). E. histolyticawasdetectedin threepatients inthehistoricalgroup and in eight subjects in the current group (Table 1). Allthese patientshadaclinicalpictureofintestinalamoebiasisandallof themreportedrecenttraveltoanendemicarea.
Ofnote,consideringpatientswithHIVinfection, Cryptosporidi-umspp was detected at a significantly lower frequency in the currentgroupthaninthe1996–1997group(1casevs.40cases, respectively; p < 0.001) (Table 1). With the exception of Cryptosporidiumspp,noothersignificantdifferencewasfoundin
theprevalenceofthedifferentparasitesbetweenthetwogroupsof nativepatients,norwasanyparasitedetectedthathadpreviously beenabsentinourterritory.
Amongnativepatients,thosebelongingtothecurrentgroup reported a significantly higher frequency of recent travel to endemicareasincomparisontopatientsinthehistoricalgroup (12%vs.7%;p<0.005).Also,thedetectionofatleastoneparasite wassignificantlyassociatedwithrecenttraveltoendemicareasin both thecurrent and historical native groups.In fact, travel to endemicareaswasreportedin38%ofparasitizedpatientsandin only7%ofnon-parasitizedpatients(p<0.0001).Thesamepattern wasnotedinthehistoricalnativegroup,inwhichtraveltoendemic areaswasreportedby21%ofparasitizedpatientscomparedto4.5% ofthenon-parasitized(p<0.001).
Onlyabout18%ofthisreportedtravelwasrelatedtobusiness purposes and had a duration of 98 months; no significant association was found betweenthe time ofpermanence and the frequencyofparasitosis(datanotshown).
3.3. Prevalenceofintestinalparasitosisamongimmigrantpatients Amongimmigrants,862parasitesweredetectedin507/1046 subjects(48.5%ofcases).Themostfrequentparasitesidentified,in decreasingorder,wereBlastocystisspp,Entamoebacoli,Endolimax nana, E. histolytica, Entamoeba hartmanni, T. trichiura, and A. duodenale.Theprevalenceofparasitizedindividualswitheachof theseparasiteswassignificantlyhigherinimmigrantsthaninboth ofthegroupsofnativepatients(p<0.001forallthesedifferences). 3.4. Prevalenceofinfectionwithpathogenicagents
Whenonlypathogenicagentswereconsidered(Table1),the prevalencesofpatientsparasitizedwithhelminthsandprotozoa(if cases of Cryptosporidium spp in HIV-positive patients in the
Table1
Distributionofdetectedparasitesinthethreegroupsofpatients(immigrants,currentnatives,andhistoricalnatives)participatinginthestudy Immigrants(n=1046) Currentnatives(n=720) Historicalnatives(n=771) n %ofisolated parasites %ofpatients n %ofisolated parasites %ofpatients p-Valuea n %ofisolated parasites %ofpatients p-Valueb Helminths Trichuristrichiura 40 4.8 3.8 0 0.0 0.0 <0.0001 1 1.0 0.1 <0.0001 Ancylostomaduodenale 33 3.9 3.2 0 0.0 0.0 <0.0001 2 1.9 0.3 <0.0001 Hymenolepisnana 15 1.8 1.4 0 0.0 0.0 <0.001 0 0.0 0.0 <0.001 Schistosomamansoni 9 1.1 0.9 0 0.0 0.0 0.01 0 0.0 0.0 0.01 Dicrocoeliumdendriticum 8 1.0 0.8 0 0.0 0.0 0.02 0 0.0 0.0 0.02 Ascarislumbricoides 7 0.8 0.7 1 1.1 0.1 0.02 0 0.0 0.0 0.04 Strongyloidesstercoralis 5 0.6 0.5 0 0.0 0.0 0.08 0 0.0 0.0 0.07 Trichostrongylusspp 4 0.5 0.4 1 1.1 0.1 0.6 0 0.0 0.0 0.1 Enterobiusvermicularis 3 0.4 0.3 2 2.1 0.3 1.0 1 1.0 0.1 0.6 Taeniaspp 2 0.2 0.2 1 1.1 0.1 1.0 1 1.0 0.1 1.0 Pathogenicprotozoa Entamoebahistolytica 52 7.3 5.0 8 8.9 1.1 <0.0001 3 3.0 0.4 <0.0001 Dientamoebafragilis 4 0.5 0.4 2 2.1 0.3 1.0 5 4.8 0.6 0.5 Giardiaduodenalis 35 4.2 3.3 9 9.5 1.3 0.005 5 4.8 0.6 <0.0001 Isosporabelli 2 0.2 0.2 1 1.1 0.1 1.0 1 1.0 0.1 1.0 Cryptosporidiumspp 0 0.0 0.0 1 1.1 0.1 0.4 40 38.1 5.2 <0.0001 Facultativepathogenicprotozoa
Entamoebacoli 130 15.4 12.4 8 8.4 1.1 <0.0001 2 1.9 0.3 <0.0001 Endolimaxnana 107 12.7 10.2 5 5.3 0.7 <0.0001 5 4.8 0.6 <0.0001 Entamoebahartmanni 47 5.6 4.5 1 1.1 0.1 <0.0001 0 0.0 0.0 <0.0001 Entamoebadispar 20 2.4 1.9 3 3.2 0.4 0.1 0 0.0 0.0 0.002 Iodamoebabu¨tschlii 8 1.0 0.8 0 0.0 0.0 0.02 0 0.0 0.0 0.02 Chilomastixmesnili 6 0.7 0.6 5 5.3 0.7 0.7 0 0.0 0.0 0.04
Parasitesofdifferenttaxonomicclassificationc
Blastocystisspp 323 38.4 30.9 50 52.6 6.9 <0.0001 37 35.2 4.8 <0.0001
a
Differencebetweenimmigrantsandcurrentnatives;atwo-sidedp-valueof<0.05wasconsideredstatisticallysignificant.
b
Differencebetweenimmigrantsandhistoricalnatives;atwo-sidedp-valueof<0.05wasconsideredstatisticallysignificant.
c
Blastocystissppisthoughttobeaprotist,belongingtothestramenopiles,abranchoftheChromalveolata.
Table2
Prevalenceofintestinalparasiticinfectionamongimmigrantsaccordingtotheir geographicalareaoforigin
Geographical areasoforigin Tested patients Infected patients Prevalence p-Valuea Native 720 69 9.6 -EastEurope 82 15 18.3 0.27 Central-SouthAmerica 49 10 20.4 0.20 NorthAfrica 165 64 38.8 0.017 CentralAfrica 486 307 63.2 <0.01 Asia 264 111 44.7 <0.01 a
Statisticaldifferenceswerecalculatedusingthegroupofnativepatientsasthe referencecategory.Atwo-sidedp-value of<0.05wasconsideredstatistically significant.
historicalgroupwereexcluded)weresignificantlyhigheramong immigrantsthanamongnativepatientsanalyzedineither2009– 2010or in1996–1997:12% vs. 0.7%and 0.6%, respectively,for helminths(p<0.001),and8.9%vs.2.9%and1.8%,respectively,for protozoa(Figure1).
3.5. Comparisonbetweennativeandimmigrantpatients
Theprevalenceofparasitizedpatientswasloweramongcurrent nativesthanamong eachgroupofdifferentcurrentimmigrants classifiedonthebasisoftheirgeographicalorigin.Inthisrespect, significant differences were found for immigrants from North Africa,CentralAfrica,andtheIndiansub-continent(Table2).The prevalenceofpatientswithmultiplesimultaneousinfectionswas significantlyhigheramongimmigrantsthanamongnativepatients inbothgroups.Inparticular,thesimultaneousdetectionofthreeor more parasites was observed in 20.1%, 10.1%, and 4.5% of immigrants, currentnatives, and historical natives,respectively (p<0.001forimmigrantsvs.currentnatives;p<0.05for immi-grantsvs.historicalnatives;no significantdifferencewasfound betweencurrentandhistoricalnativepatients).
The frequency of detected parasites changed among immi-grants dependingon their length of stayin Italy. Asshown in
Table3,thefrequency ofdetected parasitesin immigrantswas significantlyinverselyrelatedtotheamountoftimespentinItaly (p-value for trend <0.0001, for all and each of the groups of parasites analyzedin Table3). Thus, amongimmigrantswitha lengthof stayin Italy of>5 years, thepercentage of parasites
detectedtendedtobesimilartotherateobservedinthenative population.
3.6. Inter-humantransmissibilityofparasites
Ofthehouseholdsofthe48parasitizedimmigrantsanalyzed,all butthreewereentirelyconstitutedbyimmigrants,mainlyfromthe samegeographicalarea.Inoneofthesethreegroupsthatwasnot entirelycomposedofimmigrants,aTrichostrongylussppthatisvery rareinourterritory29wasidentifiedinanativeelderlyperson.This
person likelyacquired the infectionfrom a Pakistanhome care nurse,whoharbouredthesameparasite.Inalltheotherhousehold groups,nocaseofparasite/parasitestransmissionfromtheindex casetoahouseholdcontactwasidentified.Inthehouseholds,the overallprevalenceofparasitizedindividualsdidnotdiffer signifi-cantlyfromthatobservedinthegeneralimmigrantpopulation. 3.7. Clinicalsymptoms
The clinical symptoms, mainly chronic, were extremely heterogeneous for both the spectrum of manifestations and intensity.
Diarrhoea,sometimeshematic andvery profuse,wasmostly associatedwithprotozoainfections,andfeverwaspresentmainly in amoebiasis and schistosomiasis. Signs of malabsorption, abdominalcramps,anaemia,andurticarialreactionswithitching and eosinophilia were associated particularly with helminth infestations. It should be noted that these symptoms, even if
Figure1.Prevalenceofparasitizedindividualsamongimmigrantsandcurrentandhistoricalnativesaccordingtotheprincipalgroupsofparasitesdetected.
Note:Alldifferencesinprevalencebetweenimmigrantsandeachgroupofnativeswerestatisticallysignificant(p<0.01);alldifferencesinprevalencebetweenthetwo groupsofnativeswerenotsignificant;inthegroupofhistoricalnativesCryptosporidiumsppcaseswereexcluded;Blastocystissppcaseswereincludedinprotozoa.
Table3
PrevalenceofintestinalparasiticinfectionsamongimmigrantsaccordingtotheirlengthofstayinItaly LengthofstayinItaly
<2years (478patientstested) 2–5years (362patientstested) >5yearsa (206patientstested) n(%) n(%) n(%) Parasitizedpatientsb 317(62.5) 165(32.6) 25(4.9) Parasitizedby Helminths 79(62.7) 41(32.5) 6(4.8) Pathogenicprotozoa 86(76.1) 22(19.5) 5(4.4)
Facultativepathogenicprotozoa 468(75.1) 133(21.3) 22(3.5)
a
p-Valuefortrend<0.0001,forallandeachofthegroupsofparasitesanalyzed.
b
mild,werepresenteven inthosesubjectsparasitizedbyagents consideredsimplyparasites.
4. Discussion
Inourstudy,theconcentrationofstoolspecimensinthemore recentseriesofpatientswasperformedwithboththetraditional andtheFLOTACsystems.Someauthorshavereporteda slightly improved sensitivity using this latter method.25–27 In our
experience, FLOTAC increases the sensitivity only minimally (0.2%)comparedtotheothermethodofconcentrationused.Thus, evenifthemethodologytodetecttheparasitesispartiallydifferent in the two groups of patients, the overall sensitivity is not substantiallychanged.
About10%ofournativepatients, irrespectiveofthedateon whichthey wereinvestigated,showedan intestinalparasite in theirstool.Inthevastmajorityofcasesitwasaprotozoan,largely representedbyfacultativepathogens,whilehelminthswerefound inlessthan1%ofcasesandwererepresentedbyonlyafewspecies, suchasAscarides,Taenia,andE.vermicularis.Mostavailabledataon theepidemiologyofintestinalparasitosisinItalyarefromstudies focusingonselectedgroupsofpatients(e.g.children,HIV-infected individuals,andinstitutionalizedpsychiatricpatients)orspecific pathogens.30–32Veryfewepidemiologicalstudiesdealingwiththe
prevalenceofintestinalparasitosisinthegeneralpopulationhave beenperformed sofar.Amongthese,ofparticularnotearetwo extensivesurveys,alsoincludingimmigrants,carriedoutrecently innorthern and centralItaly.8,9In the studyby Masucciet al., prevalenceratesof8.9%and26.8%werefoundamongItalianand non-Italian patients, respectively.8 Peruzzi et al. reported very
similardata, showing prevalence rates of 10% and 31% among Italians and foreigners, respectively.9 The results of these two
studiesarecomparabletothosefoundinoursurvey,alsoregarding thespectrumofparasitesinvolved,thussuggestingasubstantial homogeneousepidemiologicalpicturethroughoutourcountry.
Since all patients investigated in this study had chronic intestinal symptoms, the influence of a positive selection bias on prevalence estimates is possible.Nevertheless, our findings showthatawidevarietyofintestinalparasitesarestillpresentin Campaniaand their possibleetiological involvement had tobe consideredinthediagnosisofchronicintestinaldisease.
Nosignificantdifferenceswerefoundinthedistributionofthe differentparasitesbetweenthetwogroupsofnativesexceptfor thefrequentidentificationofCryptosporidiumsppinthehistorical HIV-positivepatients, which was significantly decreased in the morerecentcases.Howeverthisexceptioncannotbeascribedto themigrationflowsandismorelikelyduetotheimprovedcontrol ofthis,aswellasotheropportunisticinfections,inducedbyHAART inthelast decade.33Thus, it appearsthat therecentand more
intensemigration flowsfromdevelopingcountriestoItalyhave notaffectedthespreadofparasitesamongthenativepopulationof Campania.Our datademonstrateinsteadthattraveltoendemic geographical areas significantly influenced the prevalence of parasites amongthe nativepopulation of Campania.Indeed, in both thecurrent and historical native groups, thedetection of parasites was significantly associated with a history of recent travelintheseareas,whichhavebecomeincreasinglypopularand fashionableinthelastfewyearsinourcountry.
As in othersurveys, Blastocystis spp wasthe most common parasiteisolatedinourstudyandwasdetectedatasignificantly higherfrequencyamongimmigrantsthanamongbothgroupsof nativepatients.Blastocystisisanentericmicroorganismfoundin humansandinmanyanimals,ubiquitousandlargelypresentin our territory as well, and with a taxonomic position that has remainedelusiveformany years.Atpresent,onthebasisofits molecularfeatures,itisthoughttobeaprotistbelongingtothe
stramenopiles,a branchoftheChromalveolata.34,35Itisusually
considered a non-pathogenic agent. However, recent evidence suggests that in particular conditions Blastocystis spp may be responsiblefor enteric disease;this appears tobelinkedto its geneticvariabilityand totheemergenceofpossiblepathogenic genotypes.36–40
Indeed,therole ofmanyparasitesconsidered saprophytesis controversial and should be revised in order to identify their possiblepathogenicityinsomecircumstances.1Eveninourstudy,
some were detected in patients with intestinal symptoms but without any other possible cause of illness. Moreover, the intestinal symptomstended toresolve afterspecifictherapy in thesepatients.
As already reported by others,12,13 both helminths and
facultativeorpathogenicprotozoawereidentifiedatasignificantly higherfrequencyamongimmigrantsthaninthenativepopulation. In particular, the highest prevalence rates were observed in immigrantsfromequatorialAfricaandtheIndiansub-continent, who also harboured pathogens usually not detectable in our country,suchasschistosomes.Also,nearlyhalfoftheimmigrant patients were positive for at leastone parasite and theywere affectedbymultiplesimultaneousinfectionswithasignificantly higherfrequencythannatives.
Weobservedthatthefrequencyofparasitedetectionamong immigrantsdecreasedinverselytothelengthofstayinItaly;thus after5yearsthepositivedetectionrateamongimmigrantstended tobesimilartotherateobservedinthenativepopulation.This finding, in addition to thelack of effects of the recent intense immigrationflowsupontheepidemiologicalprofileofintestinal parasitosisamongthenativepopulationofourareaandthelackof parasite circulation among household contacts of parasitized subjects,demonstratesthatmigrationfromendemiccountrieshas notinducedanadditionalriskofparasiticinfectionorre-infection among people living in our geographical area. A possible explanationisthatthebiologicalprerequisitesforthemaintenance of a self-sustaining cycle of these agents are missing in Italy; outbreaks arenot possible becauseof the lack of intermediate hosts(e.g.,forschistosomes),orbecauseofthelackoffavourable environmentalandclimateconditionsrequiredbyotherparasites thataredirectlytransmittedfrommantoman(e.g.,E.histolytica andE.nana).
However, in Italynot all parasites are extinct,also because manyofthemarezoonoticagents.41Thus,intheroutineprotocol
for theevaluationof patients withbowelsymptoms,especially thosewithahistoryoftraveltoanat-riskarea,aparasitesearch shouldalwaysbeconsidered.Inaddition,giventhefrequencyof parasitesfoundinimmigrants,especiallyinthosefromhigh-risk areasandthoseexpatriatedinparticularlydifficultcircumstances, a cycle of anti-parasitic therapy with albendazole would be advisable,withouttakingacoprologictest,assuggestedbysome publichealthprograms.42Thisshouldbeviewedinthecontextofa
first impact health care service and hospitality offered by our country, reserving further evaluationsonlyfor those casesthat showpersistenceofsymptomsandpeculiarclinicalfeatures.
Funding:Theentirestudywasconductedwithoutanysponsor. Ethical approval: The study was approved by the Ethics CommitteeofCotugnoHospital.
Conflict of interest: Allof the authorsdeclare no conflicts of interest.
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