students with intestinal parasitesin Practical parasitology courses andinfection ARTICLE IN PRESS

Practical parasitology courses and infection with intestinal parasites in students

Sh. Fallahi

^a,b,∗

, A. Rostami

^c

, M. Mohammadi

^d

, F. Ebrahimzadeh

^e

, Y. Pournia

^f

aDepartmentofParasitologyandMycology,FacultyofMedicine, LorestanUniversityofMedicalSciences,Khorramabad,Iran

bRaziHerbalMedicinesResearchCenter,LorestanUniversityofMedicalSciences, Khorramabad,Iran

cDepartmentofParasitologyandMycology,FacultyofMedicine, ShahidBeheshtiUniversityofMedicalSciences,Tehran,Iran

dDepartmentofPharmaceuticalBiotechnology,FacultyofPharmacy, LorestanUniversityofMedicalSciences,Khorramabad,Iran

eDepartmentofBiostatistics,FacultyofMedicine,

LorestanUniversityofMedicalSciences,Khorramabad,Iran

fInstructor,FacultyofMedicine,LorestanUniversityofMedicalSciences, Khorramabad,Iran

Received26July2015 ;receivedinrevisedform11November2015;accepted11December2015

KEYWORDS Intestinalparasites;

Practicalparasitology course;

Students

Summary Studentswhoare working inresearch or educationallaboratories of parasitology,aswellashealthcareworkersprovidingcareforpatients,areatthe risk of becoming infected withparasites through accidental exposure. The main purposeofthisstudywastoidentifypotentialpositivecasesofintestinalparasitic infections amongstudentswhotookpracticalparasitologycoursescomparedwith studentswhodidnottakeanypracticalparasitologycoursesinLorestanUniversityof MedicalSciences,Khorramabad,Iran,in2013—2014.Atotalof310subjectsfromvar- iousmajorswereinvitedtovoluntarilyparticipateinthestudy.Variousdemographic datawerecollectedusingquestionnaires.Threestoolsampleswerecollectedfrom eachindividualonalternatedays.Salinewetmounts(SWM),formalin—ethersedi- mentationtest(FEST),Sheatherfloatationtest(SHFT)andtrichromeandmodified Ziehl—Neelsen stainingmethodswereusedtodiagnose thepresenceof intestinal

∗Correspondingauthorat:DepartmentofMedicalParasitologyandMycology,SchoolofMedicine,LorestanUniversityofMedical Sciences,Khorramabad,Iran.Tel.:+986633120133;fax:+986633120133.

E-mailaddresses:Falahi.Sh@lums.ac.ir,Shfupdate@gmail.com(Sh.Fallahi).

http://dx.doi.org/10.1016/j.jiph.2015.12.010

1876-0341/©2015KingSaudBinAbdulazizUniversityforHealthSciences.PublishedbyElsevierLimited.Allrightsreserved.

parasites.Theprevalence rateofintestinalparasites(IPs)amongthestudentswas 11.93%.TherewasasignificantdifferencebetweenmajorsintheinfectionwithIPs (P<0.05). Themost frequentlyobservedIPswereBlastocystishominis (4.51%)and Giardiaintestinalis(3.54%).Theresultsofthisstudyshowedthatthetransmissionof pathogenicparasitesintheeducationalcourseofpracticalparasitologycouldoccur andmustbetakenintocarefulconsideration.

©2015KingSaudBinAbdulazizUniversityforHealthSciences.PublishedbyElsevier Limited.Allrightsreserved.

Introduction

Parasitic diseases constitute great medical, social andeconomicproblemsworldwide.Parasiticinfec- tions have a high prevalence and it is estimated that more than three billion people are infected by IPs in the world today [1]. The role of IPs in causing morbidity and mortality as well as in the pathogenesis of other infectious diseases differs fromspecies tospecies [2,3]. Similarly,thedistri- butionandprevalenceofvariousspeciesofIPsalso differ from region to region due to several envi- ronmental, social, and geographical factors [4,5].

Thus,astudyonthe prevalenceofvariousintesti- nalparasiticinfectionsisaprerequisitenotonlyto formulateappropriatecontrolstrategiesbutalsoto predict risks for communities under consideration [6].Theglobalinfectionratesduetogastrointesti- nalparasitesareonaremarkablescale,particularly in undevelopedordevelopingcountries.Inastudy in Ethiopia, the prevalence rate of IPs among school children was 83.8% [7]. In another survey inTurkey, 31.8%ofthestudiedschoolchildrenhad beeninfectedwithoneormoreIPs[8].Inanother study thatwasperformedon studentsin southern Sudan in 1998, 15 different species of parasites were foundamongthesubjectsafterparasitologi- calexamination[9].TheseasonalprevalenceofIPs in the United States during2000 was 31.62%[10].

The prevalence of IPs among students in various regions ofIran varies, for example, Tehran 18.4%

[11],Kashan9.46%[12],andKouhdasht32.5%[13].

One of the common health indicators in every community is the prevalence ofparasiticdiseases among its people. The capacity toperceive these parasiticdiseasesandtheeffectivecausesintheir establishment and dispersion patterns enhance healthmonitoring[14].Theparasitologylaboratory is one ofthemost common placeswhere contam- ination with parasites could occur. Thus, people

who are working or examining in this place, such as students of the medical sciences, could be at the risk of being infected with parasites. Thus, thiscase-controlledstudywasperformedtodeter- mine the prevalence of IPs in students who took practicalparasitologycoursesinparasitologylabo- ratoriescompared withstudentswho didnottake any practical parasitology courses and had never beenin aparasitology laboratory in LorestanUni- versityofMedicalSciences,Lorestanprovince,west Iran,during2013and2014.

Methods

Studypopulation

The presentstudywas performedin the parasito- logylaboratoryoftheFacultyofMedicine,Lorestan University ofMedicalSciences, Khorramabad City, West Iran, from May 2013 to January 2014. The participantswere175studentswhoweremajoring inMedicine,LaboratorySciences,Nursing,Medical Emergencies and Controlling Diseases Health who tookpracticalparasitologycourses(exposedgroup) and 135 studentsoftheMidwifery, FamilyHealth, HealthInformationTechnologyandOperationRoom majorswho had never beenin a parasitology lab- oratory (unexposed group). Only students with a negativeparasitologyresultbeforethestartofthe coursewereenrolledinthestudy.Allofthepartic- ipants were included in the study voluntarily. For every individual, a questionnaire includingdemo- graphic information was also completed. Three stool sampleswerecollected fromeachindividual inpre-labeled,leak-free,plasticspecimencontain- ers,onalternatedays;andeachsamplearrivedat thelaboratory onthedayofcollectionundercold storageconditions.Accordingtotheparasitological examination results, individuals were assigned to thecase orcontrolgroups.Subjectsinfectedwith

IPs were cases, and uninfected individuals were controls.

Parasitologicalexamination

The stool samples were examined macroscopi- cally toconfirm the consistencyand todetermine the presence of blood, mucus or adult worms.

Moreover, SWM (using 0.85% NaCl solution), were prepared directly from the fecal samples and observedunderamicroscopewitha10×objective lens to demonstrate the presence of worm eggs, larvae, and subsequently with the 40× objective lens to capture the details of protozoan tropho- zoites or cysts. Mounts were also prepared from concentrated specimens using the FEST and SHFT techniques and observed in the same manner.

To identify opportunistic coccidial intestinal par- asite oocysts of Cryptosporidium spp., Isospora belli, Cyclospora cayetanensis, a permanentslide was prepared for each sample, and then stained using the modified Ziehl—Neelsen acid-fast tech- nique, In addition, the prepared smears were stainedwith Trichromestainingmethods andthen

examined microscopically [15]. Findings of the caseandcontrolgroupswerecomparedwith each other. Data analysis was performed using SPSS software version21.The Chi-square testwas per- formed to compare the prevalence of parasites amonggroups. Associations were testedusing the Kruskal—Wallis, Mann—Whitney and Fisher’s exact testsafteradjustments.AP-valueof<0.05wascon- sideredstatisticallysignificant.

Results

Sociodemographicdescription ofthestudy population

Sixtypercentofthe studiedstudentswerefemale and 64.5% of the students were dormitory resi- dents.Themajorityoftheparticipantswas inthe 20—25 age group, and most took practical parasi- tology courses (46.12% and 56.45%, respectively).

The general sociodemographic characteristics of the310studiedstudentsincluding,agegroup,sex, major, taking or not taking practical parasitology

Table1 Theprevalenceofintestinalparasitesinstudentsaccordingtodemographiccharacteristics.

Variable Total

(no.=310)(%)

Caseno.

(%)

Controlno.

(%)

Oddsratio (95%CI)

P-value

Sex 0.775

Male 124(40) 14(11.2) 110(88.8) 0.90(0.45,1.83)

Female 186(60) 23(12.3) 163(87.7)

Age^a 0.445

<20 78(25.1) 12(15.3) 66(84.7) 1

20—25 143(46.1) 17(11.8) 126(88.2) 0.74(0.33,1.65)

≥26 89(28.8) 8(8.9) 81(91.1) 0.54(0.21,1.41)

Residence 0.962

Indormitory 200(64.5) 24(12) 176(88) 1.02(0.50,2.09)

Privatehome 110(35.5) 13(11.8) 97(88.2)

Major^a <0.001

Medicine 35(11.2) 8(22.8) 27(77.2) 1

LaboratorySciences 35(11.2) 12(34.2) 23(65.8) 1.76(0.61,5.05)

Nursing 35(11.2) 7(20) 28(80) 0.84(0.27,2.65)

MedicalEmergencies 35(11.2) 4(11.4) 31(88.6) 0.44(0.12,1.61) HealthInformationTechnology 30(9.6) 2(6.6) 28(93.4) 0.24(0.05,1.24)

OperationRoom 35(11.2) 2(5.7) 33(94.3) 0.21(0.04,1.05)

Midwifery 35(11.2) 3(8.5) 32(91.5) 0.32(0.08,1.31)

FamilyHealth 35(11.2) 1(2.8) 34(97.2) 0.10(0.01,0.84)

ControllingDiseasesHealth 35(11.2) 2(5.7) 33(94.3) 0.04(1.05,0.04)

Takingpracticalparasitologycourse 0.271

Yes(Exposed) 175(56.4) 24(13.7) 151(86.3) 1.49(0.73,3.05)

No(Unexposed) 135(43.6) 13(9.6) 122(90.4)

Handwashingafterpractice 0.737

Yes 85(27.4) 11(12.9) 74(87.1) 1.14(0.54,2.42)

No 225(73.6) 26(11.5) 199(88.5)

aFirstlineconsideredasbaseline.

courses,placeofresidenceandhandswashingafter laboratorypractice,whichwerecollectedviaques- tionnaires,areshowninTable1.

Parasitologicalexaminations andprevalence Outofthe310students,thirty-seven(11.93%)stu- dents were infected with intestinal parasites and outofthesestudents,24people(64.86%)tookthe practical parasitologycourses. Onthe basisofthe parasitological examination, the frequency of IPs was13.7%(24/175)intheexposedgroupand9.6%

(13/135) in the unexposed group. However, stu- dentstakingthepracticalparasitologycourseswere more likely to be infected with IPsthan students who had never been in a laboratory of parasi- tology, but there were no significant differences betweentheexposed/unexposedgroups(OR=1.49;

95%CI=0.73—3.05;P<0.271).

According to the Chi-square and Fisher’sexact tests, there were no significant differences in the sex, age and major distributions between case and control groups. Nevertheless, most of the positive cases were strikingly observed in the

20—25 age group (45.94%), particularlyin female students (62.16%), dormitory resident students (64.86%),studentswhotookpracticalparasitology courses(64.86%)andthosewhodidnotwashtheir hands after laboratory practice (70.27%). Among the infected students, the majority of subjects belongedtotheLaboratorySciencesmajor(32.43%) andthefewestinfectedstudentswereintheFamily Healthmajor(2.70%).

The prevalence rates of different IPs in the exposed/unexposedgroupsarepresentedinFig.1;

Table 2. The most prevalent parasites in the subjects were Blastocystis hominis (4.51%), Giar- dia intestinalis (3.54%), Entamoeba coli (2.25%) andHymenolepisnana(1.29%),respectively.Other parasites were detected as the following: Ascaris lumbricoides,Iodamoebabutcheli,Entamoebahis- tolytica/dispar and Endolimax nana (Fig. 1). No significantdifferenceswereobservedforthepreva- lence of IPs between the exposed/unexposed groups. The prevalence of IPs among students according to the diagnostic method is shown in Table 3. Most of the positive samples for intesti- nal parasites were detected using FEST (83.87%)

Figure1 Frequencyoftheintestinalparasitesdetectedintheexposedandunexposedgroups.

Table2 Prevalenceofintestinalparasitesintheexposedandunexposedgroups.

Variable Total Exposedgroup

(n=175)no.(%)

Unexposedgroup (n=135)no.(%)

Oddsratio(95%CI) P-value

Giardiaintestinalis 11 8(4.5) 3(2.2) 2.11(0.55,8.10) 0.360

Entamoebacoli 7 5(2.8) 2(1.4) 1.96(0.37,10.24) 0.703

Blastocystishominis 14 9(5.1) 5(3.7) 1.41(0.46,4.31) 0.545

Entamoebahistolytica/dispar 1 0(0.0) 1(0.7) 0.26(0.01,6.32) 0.435

Ascarislumbricoides 2 1(0.5) 1(0.7) 0.77(0.05,12.42) 1

Hymenolepisnana 4 3(1.7) 1(0.7) 2.34(0.24,22.72) 0.635

Iodamoebabutcheli 2 1(0.5) 1(0.7) 0.77(0.05,12.42) 1

Endolimaxnana 1 1(0.5) 0(0.0) 2.33(0.09,57.63) 1

Table3 Theprevalenceofintestinalparasitesinthestudentswithrespecttothediagnosticmethods.

Variable Total(No.=310)

Infectedno.(%) Uninfectedno.(%)

Salinewetmounts 18(5.8) 292(94.2)

Formalin—ethersedimentationtest 31(10) 279(90)

Sheatherfloatationtest 4(1.2) 306(98.8)

Trichromestainingmethod 26(8.3) 284(91.7)

ModifiedZiehl—Neelsenstainingmethod 0(0.0) 310(100.0)

However, any species of opportunistic coccidial intestinalparasitewasdetectedusingthemodified Ziehl—Neelsenacid-faststainingmethod.

Discussion

Many studies on the prevalence of intestinal par- asiticinfections have been performedin Asiaand Iran, dueto itswide distribution in this continent and this country, respectively [8,11—13,23—26].

However, there is little information about the prevalence of intestinal parasites in students of medical sciences universities in Iran. Thus, the present study was performed on 310 students of variousmajorsinLorestanUniversityofMedicalSci- ences, fromMay2013to January2014.This study providedthefirstestimationofparasiteprevalence among medical science students of Lorestan Uni- versity ofMedical Sciences, Lorestanprovince, in westIran.Inthepresentsurvey,11.93%ofthesub- jects had been infected with at least one of the intestinal parasites.The infectionratein the stu- dentswho took practical the parasitology courses and had a negative parasitology result beforethe start ofthe course was 13.71%. In the unexposed groupwho had never beenin a parasitology labo- ratory,this ratewas9.62%. Ourfindingwashigher thanthefindingsin thepreviousstudiesinvarious regions of Iran, suchas, 9.46% in the students of Kashan University ofMedical Sciences [12], 5.63%

inArakstudents[16],5.78%inAhvazstudentswith lowIQ[17]and4.51%inRobatkarimstudents[18].

Moreover,theprevalenceofthepresentstudywas higher than that of another study in Turkey that was8.31%[8]aswellasinmedicalstudentsofone college in Africa at 6% [19]. However, our preva- lence rate was lowerthan the prevalence rateof intestinalparasitesinstudentsofTabrizUniversity of Medical Sciences in 1992, which was 53% [20].

There was no significant association between age group and the resultsofthe parasitological tests, namely infection with IPs in the students could occurin everyage group. The infection ratewith

IPsinfemalestudentswashigherthanthatinmale students.Mostoftheinfectedstudentsweredormi- toryresidents,andthisfindingispresumablydueto the hygienic and socioeconomicconditions ofthis location. Under these conditions, more crowded populations, low hygiene, and high contact rate resultedin anincrease in the risk oftransmission ofparasiticinfections. Accordingtothe resultsof the presentstudy, parasiticinfections in students whotookpracticalparasitologycoursesweremore commonthaninthestudentsunexposedtotherisk factor.However,becauseofthedirectcontactwith contaminatedsamplesorspecimensandlaboratory apparatuses,working orpracticing in parasitology laboratories increased the risk of infection with parasites.Nevertheless,theprevalencerateofIPs intheunexposedgroupswasrelativelyhighdespite thefactthattheyhadneverworkedinorneverhad physicalpresence in parasitology laboratories and thisindicatedthatallofthestudentsofmedicalsci- encesuniversitiesareattheriskofbeinginfected withIPs.Becausethemajorityoftheinfectedstu- dents do not wash their hands after laboratory practice, this finding suggests that hand washing aftercourseworkorbeforeeatinganythingingen- eral is an important factor for the prevention of infectionwithIPs.AsshowninTable3,mostofthe parasiticinfectionsweredetectedamongstudents who have beendiagnosed by FEST, which reflects thefactthatthismethodisaconvenientandhigh- performanceassayinthediagnosisofIPs.

UnliketotheresultsofArbabietal.’sstudy,2005 [12], in our survey, the most common pathogenic andnonpathogenicIPswereB.hominis,G.intesti- nalis, E. coli and H. nana while, in their study, GiardiaintestinalisandE.coliwerethemostcom- mon parasites. Importantly, similar to a previous studyperformedintheruralregionsofKouhdasht, Lorestanprovince [13], the resultsof the current study indicated that protozoan parasites had a higher rate of infection and 10.0% of the studied students were infected with intestinal protozoa.

This contradiction is mainly due to the rapid and high reproduction rates, high compatibility with

theenvironmentandfeasibilityinthetransmission of protozoan parasites during laboratory practice [21,22].Somepotentialsourcesofbiasinthisstudy could be the self-reporting of hand washing, and the sensitivityofthediagnosticmethodsandsam- ple size; however, we resolved these issues via an adjustment for these factors in the statistical analyses.

Thereweresomelimitationstoourstudy.First, wehadalimitedsamplesizebecausewehadaccess toonlythisnumberofstudents.Second,thereisa possibilityofself-treatingwithanti-parasiticdrugs with someoftheparticipantsinourstudypriorto oursamplingbecauseMetronidazole,Mebendazole andAlbendazoleareavailablewithoutprescription in Iran. Third, due to the lack of facilities and financial funding,we couldnot use ofalloftech- niques,suchasthe Baermantechnique,whichhas beenusedtoidentifythelarvae ofworms,includ- ing Strongyloides strongyloides or adhesive tape for Entrobius vermicularies. Thismaybe one rea- sonforthelowprevalenceofhelminthicinfections in our study. Another limitation of our study was thelackofmolecularmethods,suchaspolymerase chain reaction (PCR) to provide a more accurate andspecificassessmentofinfectionwithintestinal parasites amongthestudiedstudents. Ifthis were the case, there may be a higher rate of positive resultsamongthesubjects.

Conclusions

Accordingto ourresults, itcan be concludedthat there was a relatively high prevalence of intesti- nal parasitic infections in students of Lorestan University of Medical Sciences in 2013—2014. The screening and treatment process of infected stu- dents as well as improving the sanitation and preventionprogramswillreducetheinfectionrate.

In addition, thehigh prevalence rateofintestinal parasitesamongthestudiedstudentssuggeststhat infectionwith theseparasitescouldoccurinallof the laboratory and educational centers aswell as acrosstheentiresociety.Additionally,aninterven- tion strategyshouldbedesignedand implemented tocontrolandreducetheseinfections.

Funding

ThisresearchwasfinanciallysupportedbytheVice Chancellors for ResearchofLorestanUniversity of Medical Sciences and approved by Ethical Com- mitteeofLorestanUniversityofMedicalSciences, Khorramabad,Iran.

Competing interests

Nonedeclared.

Ethical approval

Notrequired.

Acknowledgments

Theauthorswishtothankthestudentsofdifferent majorsfromLorestanUniversityofMedicalSciences in2013fortheirgreatassistance.

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