research note the prevalence of intestinal parasitic
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©2020 Institute of Parasitology, SAS, KošiceDOI 10.2478/helm-2020-0033
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HELMINTHOLOGIA, 57, 3: 276 – 279, 2020
Research Note
The prevalence of intestinal parasitic infections among Kosovar and Serbian school-children in Kosovo
K. KORZENIEWSKI1,*, A. LASS2, A. AUGUSTYNOWICZ1, M. KONIOR1
1MilitaryInstituteofMedicine,DepartmentofEpidemiologyandTropicalMedicine,83-103Gdynia,4GrudzińskiegoSt.,Poland,*E-mail: kkorzeniewski@wim.mil.pl; 2MedicalUniversityofGdańsk,InstituteofMaritimeandTropicalMedicine,
DepartmentofTropicalParasitology,81-519Gdynia,9BPowstaniaStyczniowegoSt.,Poland
Article info
ReceivedJuly18,2019AcceptedMay5,2020
Summary
Theaimofthisstudywastoestimatetheprevalenceanddistributionofspeciesofintestinalpara-sitesintheBalkansontheexampleofKosovarandSerbianresidentsfromtheregionofGnjilaneineasternKosovo,wheretheepidemiologyofintestinalparasiticinfectionsremainsunknown.Para-sitologicalexaminationofstoolspecimenswasperformedin2017and2018.Stoolsampleswerecollectedfromasymptomaticschool-childrenaged6–17years:530KosovarsfromthemunicipalityofKaçanikand310SerbsfromthemunicipalitiesofKamenicaandStrpce.Eachpatientprovidedtwostoolsamplescollectedeverysecondday,fixedinSAFpreservativeand70%spiritusvini,transpor-ted to the Department of Epidemiology and Tropical Medicine at the Military Institute of Medicine in Poland,andtestedbylightmicroscopyusingthreediagnosticmethods:directsmearinLugol’ssolu-tion,decantationindistilledwater,andFülleborn’sflotation.Atotalof101Kosovarchildren(19.1%ofthestudygroup)werefoundtobeinfectedwithintestinalparasites:nematodes(n=20),cestodes(n=2),trematodes(n=2),andprotozoa(n=79).Only13Serbianchildren(4.2%)werefoundtobeinfectedwith nematodes (n=4), cestodes (n=3), and protozoa (n=6).Giardia intestinaliswas themostprevalent intestinalparasite inbothgroups (14,9%vs.1.9%children).Theprevalenceofasymptomaticparasitic infectionswassignificantlyhigherinKosovarsincomparisontotheSerbslivinginthesameregionofeasternKosovo.Thisfactshowsthattheremaybesignificantdifferencesinthequalityofhealthcareandsanitationaswellasfeedhygienebetweenthesetwocommunities.Keywords:helminths;protozoa;children;epidemiology;Kosovo
Introduction
Despite a spectacular advance in the diagnosis and management of diseases, intestinal parasitic infections remain amajor publichealth issueglobally(KeiserandUtzinger,2010). It isestimatedthatmore than twobillionpeopleworldwideare infectedwithatleastonespeciesofintestinalparasiteandoverfivebillionpeopleliveincountrieswherehelminthsandprotozoaareendemic(Kuciket al.,2004).Theriskofinfectionisparticularlyhighinareaswithpoorsanitationbecausepoorhygieneand the lackofadequate
sanitationfacilitiesencouragethespreadoffoodandwaterbornediseases(Hotezet al.,2007).Thereareanumberfactorswhichfacilitatethespreadofparasiticinfectionsbothinthedevelopingandtheindustrializedworld;theseincludelowsocioeconomicsta-tus, mass migrations, and the presence of hosts in ecosystems (reservoirsofparasites)(Aliet al.,2014;Ojhaet al.,2014).Thespectrumofclinicalsymptomsinparasiticinfectionsisextremelywideandmayvary fromasymptomaticcases throughdiarrheastocachexialeadingtosevereanemia(KorzeniewskiandKurpas,2016).Microscopicexamination isstill thegoldstandard for the
* – corresponding author
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diagnosisofintestinalhelminthsandprotozoamakingitpossibletodetectparasitesattheirdifferentdevelopmentalstages(cysts,trophozoites, larvae, ova) (Myjak et al., 2011). In Europe, highratesofparasiticinfectionsarereportedfromthecountrieswhichare listed in the third and fourth quartile according to gross domes-ticproductpercapita(GDP$1809–$17630)(HotezandGur-with,2011);Kosovoranksinthe4thquartile.TheexactprevalenceofparasiticinfectionsinKosovoisnotclearbecausethecountrylacksorganizedepidemiologicalscreening.In2001,astudywasconductedtoestablishtheetiologyofdiarrheain45Kosovarchil-dren(KosovskaMitrovica). It revealed that40%of thediarrheacasesinthestudygroupwereassociatedwithGiardia intestina-lis (Quamilèet al.,2011).Anotherstudyaimedatassessing theprevalenceofparasiticinfectionsinKosovowasconductedbytheauthorsofthepresentarticlein2015.Thestudygroupconsistedof632Kosovars(childrenandadults)livinginthemunicipalityofKaҫaniklocatedinsouthernKosovo.Wefoundthat12%ofthestudy population had asymptomatic parasitic infections, mainly Giardia intestinalis infection(10%oftheinfectedindividuals)(Ko-rzeniewskiandAugustynowicz,2017).Kosovohasapopulationofaround2millionpeople.ThemajorityofitsresidentsareAlbanian,but therearealsosomesignificantethnicminorities living in thecountry,ofwhichtheSerbianminorityisthelargest(140,000).Theaimofthisstudywastoassesstheprevalenceanddistribu-tionofspeciesofintestinalparasitesintheBalkansontheexam-pleofKosovarandSerbianresidentsfromtheregionofGnjilaneineasternKosovo,wheretheepidemiologyofintestinalparasiticinfectionsremainsunknown.
Material and Methods
Study population In total, 840 asymptomatic school-children, aged 6 – 17 years,
living in the regionofGnjilane ineasternKosovo (including530KosovarsfromthemunicipalityofKaçanikand310SerbsfromthemunicipalitiesofKamenicaandStrpce)werescreenedforintesti-nalparasitesin2017and2018.TheapprovaltoperformthestudyinvolvingKosovarchildrenhadbeengivenbytheHeadofMedicalServiceandSocialHealthDepartmentMrs.DianaRekaandtheHeadofEducationandCultureDepartmentMr.EnverKamishiandissuedintheKaҫanikmunicipality.Theapprovaltoperformare-searchstudyamongSerbianchildrenhadbeenobtainedfromtheDirectorofMedicalCenterfortheGnjilaneregion,Dr.ZoranPerić.Writteninformedconsentwasprovidedbyparentsorlegalguard-iansofthechildreninvolvedinthestudy(handwrittensignaturesonacollectivelistofallstudyparticipants).ThedetailsofthestudywereexplainedtotheparticipantsinpatientinformationbrochureswrittenintheAlbanianandSerbianlanguages.
Sample collection and laboratory procedures Each patient provided two stool samples collected every sec-ond day at Kosovar and Serbian healthcare facilities and localschools.ThespecimenswerefixedinSAF(sodium-acetate-ace-ticacid-formalin)preservativeand70%spiritusvini,transportedto the Department of Epidemiology and Tropical Medicine at the Military Institute of Medicine in Poland, and tested by light mi-croscopyusingthreediagnosticmethods:directsmearinLugol’ssolution,decantationwithdistilledwater,andFülleborn’sflotation(ClinicalandLaboratoryStandards Institute,2005;Garciaet al., 2003;WHO,1991).Statistical analysis ThestatisticalanalyseshavebeenperformedusingthestatisticalsuiteStatSoftInc.(2014)STATISTICA(dataanalysissoftwaresys-tem)version12.0.www.statsoft.comandExcel.Thequantitativevariableswerecharacterizedbythearithmeticmeanofstandarddeviationormedianormax/min(range).Thequalitativevariables
Intestinal parasites No of infections
(n=103)
% of infections
% of examined patients (n=530)
Nematodes 20 19.5 3.8Ascaris lumbricoides 8 7.8 1.5
hookworm 8 7.8 1.5Trichuris trichiura 3 2.9 0.6
Enterobius vermicularis 1 1.0 0.2Cestodes 2 1.9 0.4
Hymenolepis nana 2 1.9 0.4Trematodes 2 1.9 0.4
Dicrocoelium dendriticum 2 1.9 0.4Protozoa 79 76.7 14.9
Giardia intestinalis 79 76.7 14.9No of infected 101 100.0 19.1
Table1.Intestinalparasiticinfectionsamong530Kosovarschool-childrenresidinginGnjilaneregion(Kaçanikmunicipality).
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werepresentedwiththeuseofcountandpercentage.Astatisticalsignificancelevelof0.05wasusedforallcalculations.
Ethical Approval and/or Informed Consent Theresearchprojectwasapprovedby theBioethicsCommitteeat theMilitary Institute ofMedicine inPoland (DecisionNo. 72/WIM/2017)undertheDeclarationofHelsinkiandinlinewiththeEU provisions on Good Clinical Practice for conducting clinical tri-als and testing medicinal productssignedbythePolishBioethicsCommittee.
Results
Followingthemicroscopicexaminationof1,680stoolspecimens(twosamples taken fromeachof the840subjects)by threedif-ferent light microscopy methods we found that the total preva-lenceof intestinalparasiteswas19.1%inKosovar(n=530)and4.2%inSerbianschool-children(n=310).Thestudyrevealedthat101 Kosovar children were infected with pathogenic intestinalparasites; a total of 103 infectionsweredetected (two casesofco-infections). Themost frequently detected intestinal parasitesincluded Giardia intestinalis (14.9%studysubjects),Ascaris lum-bricoides(1.5%)andhookworm(1.5%)(Table1).A totalof13Serbianchildrenwere found tobe infectedwith in-testinalparasites.Giardia intestinalis (1.9%of thestudygroup)and Ascaris lumbricoides(1.0%)werepredominant(Table2).In-fectionswithnon-pathogenicintestinalparasites,e.g.Enatmoeba coli, Endolimax nana, Chilomastix mesnili(foundinbothexaminedgroups)werenottakenintoconsiderationandarenotdiscussedinthispaper.
Discussion
Currentepidemiologicalsituationof intestinalparasitic infections(IPI) inKosovo isunknownandpresentedstudyremainsoneof
fewanalyses in thefieldof intestinalparasitology in this region.Populationscreening toassess theprevalenceof intestinalpar-asiteshavebeencarriedoutintheneighboringcountries,e.g.inAlbania andSerbia.The study of Sejdiniet al. (2011) involving321children(aged7–16years) living in thecountiesofTiranaandElbasan in centralAlbania demonstrated the overall IPI in-cidenceof19.0%, themostprevalentbeingGiardia intestinalis (10.9%),hookworm (5.6%),andAscaris lumbricoides (1.9%).AdifferentscreeningstudyperformedbySpinelliet al. (2006) in277asymptomaticsubjects fromcentralAlbania found that24.2%ofthestudygroupwereinfectedwithpathogenicprotozoaandhelminths, including Trichuris trichiura(12.3%),Giardia intestina-lis(11.2%),Hymenolepis nana(1.8%)andAscaris lumbricoides (1.1%).Theauthors’studyinvolving530asymptomaticKosovarschool-children from theGnjilane regiondemonstrateda similaroverallincidenceofIPI(19.1%),wherethemostcommonlyiden-tifiedparasites includedGiardia intestinalis (14.9%),hookworm(1.5%)andAscaris lumbricoides(1.5%).AccordingtotheresearchstudiesconductedinSerbia,theratesof infectionswith intestinal parasites in the local population arerelatively low. A multicenter screening of 6,645 asymptomaticschool-children, aged 7 – 11 years, from 115 settlements in 20different regions of central Serbia (including Belgrade, Kraguje-vac, Lučani, Bor, Žagubica, Sjenica, Novi Pazar, Valjevo,Alek-sandrovac, Pirot, Bosilegrad, Ivanjica, Golubac, Užice, Klado-vo, Negotin, Kraljevo, Gornji Milanovac, Kruŝevac, and Čačak)found the overall prevalence of Giardia intestinalis infections to be6.1%.(Nikolićet al.,2011).Theauthors’studyconducted intheperiodbetween2017and2018among310asymptomaticSer-bianschool-childrenfromtheGnjilaneregionineasternKosovo,demonstratedtheoverallincidenceofIPIat4.2%,withGiardia in-testinalis(1.9%)andAscaris lumbricoides(1.0%)beingpredom-inant.Examinationof2,440Serbiantravelersreturningfromtropi-calandsubtropicaldestinationsrevealedinfectionswithintestinalparasitesin1.2%patientsonly,mainlyEntamoeba histolytica sen-su lato and Giardia intestinalis(Dakićet al.,2011).Inrecentyears,
Intestinal parasites No of infections
(n=13)
% of infections
% of examined patients (n=310)
Nematodes 4 30.8 1.3 Ascaris lumbricoides 3 23.1 1.0
Enterobius vermicularis 1 7.7 0.3Cestodes 3 23.1 1.0
Hymenolepis nana 2 15.4 0.7Diphyllobothrium latum 1 7.7 0.3
Protozoa 6 46.1 1.9Giardia intestinalis 6 46.1 1.9
No of infected 13 100.0 4.2
Table2.Intestinalparasiticinfectionsamong310Serbianschool-childrenresidingGnjilaneregion(KamenicaandStrpcemunicipality).
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amajorityofstudiesintotheprevalenceofintestinalparasitesinhumans that are carried out in Europe are primarily focused on the incidence of Cryptosporidiumspp.andGiardiaspp.SerbiaisoneofthecountriesparticipatinginIPIsurveillance(thenumberofreportedgiardiasiscasesinthecountryfellfrom4.6/100,000in2005to1.1/100,000in2014)(Plutzeret al.,2018).Unfortunately,thereisnoreliabledataavailableastotheprevalenceofintestinalparasiticinfectionsinKosovo.
Conclusion
Current epidemiology of intestinal parasites in Kosovo is un-known. The study involved asymptomatic Kosovar and Serbianschool-children living in thesameecosystemof theGnjilane re-gion (easternKosovo)anddemonstrated that theprevalenceofintestinalparasiticinfectionsinKosovarsissignificantlyhigherincomparison to Serbian children, whichmay be the evidence ofsome differences in the quality of health care and sanitation as wellasfeedhygienebetweenthesetwocommunities.
Acknowledgements.
Thisstudywassupportedandco-fundedby theMinistryofSci-ence and Higher Education in Poland (project No. 518/2018,2018–2019).Theauthorsaregrateful toMrs.DianaReka,Mr.EnverKamishiandDr.ZoranPerićfortheirexcellenttechnicalas-sistance and supervision in patient recruitment and collection of biologicalsamples.
Declaration of interest
Theauthorsdeclarethattheyhavenoconflictofinterest.
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