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Research Article Protozoan Parasites of Rodents and Their Zoonotic Significance in Boyer-Ahmad District, Southwestern Iran Zeinab Seifollahi, Bahador Sarkari, Mohammad Hossein Motazedian, Qasem Asgari, Mohammad Javad Ranjbar, and Samaneh Abdolahi Khabisi Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran Correspondence should be addressed to Bahador Sarkari; [email protected] Received 30 September 2015; Revised 24 January 2016; Accepted 28 January 2016 Academic Editor: Remo Lobetti Copyright © 2016 Zeinab Seifollahi et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Backgrounds. Wild rodents are reservoirs of various zoonotic diseases, such as toxoplasmosis, babesiosis, and leishmaniasis. e current study aimed to assess the protozoan infection of rodents in Boyer-Ahmad district, southwestern Iran. Materials and Methods. A total of 52 rodents were collected from different parts of Boyer-Ahmad district, in Kohgiluyeh and Boyer-Ahmad province, using Sherman live traps. Each rodent was anesthetized with ether, according to the ethics of working with animals, and was dissected. Samples were taken from various tissues and stool samples were collected from the contents of the colon and small intestines. Moreover, 2 to 5mL of blood was taken from each of the rodents and the sera were examined for anti- Leishmania antibodies, by ELISA, or anti-T. gondii antibodies, by modified agglutination test (MAT). DNA was extracted from brain tissue samples of each rodent and PCR was used to identify the DNA of T. gondii. Results. Of the 52 stool samples of rodents studied by parasitological methods, intestinal protozoa infection was seen in 28 cases (53.8%). From 52 rodents, 19 (36.5%) were infected with Trichomonas, 10 (19.2%) with Giardia muris, and 11 (21.2%) with Entamoeba spp. Also, 10 cases (19.2%) were infected with Blastocystis, 3 (5.8%) were infected with Chilomastix, 7 (13.5%) were infected with Endolimax, 1 (1.9%) was infected with Retortamonas, 3 (5.77%) were infected with T. gondii, and 6 (11.54%) were infected with Trypanosoma lewisi. Antibodies to T. gondii were detected in the sera of 5 (9.61%) cases. Results of the molecular study showed T. gondii infection in 3 (5.77%) of the rodents. Findings of this study showed that rodents in Kohgiluyeh and Boyer-Ahmad province, southwestern Iran, are infected with several blood and intestinal parasites; some of them might be potential risks to residents and domestic animals in the region. 1. Introduction Rodents are the most frequent and important mammals on the Earth, because they can adapt themselves to the different locations and environmental changes. ese animals live on almost every continent except Antarctica [1]. Rodents are considered as reservoirs of various zoonotic diseases includ- ing toxoplasmosis, babesiosis, and leishmaniasis [1–4]. Nev- ertheless, rodents cannot directly cause disease in humans and disease is mainly transmitted to humans if human is in contact with rodents’ feces and secretory materials. Transmission of the zoonotic pathogens to humans can occur via rodent’s urine, feces, hair, and saliva [2]. Human activities which change the ecosystem of rodents’ living place have an important role in the epidemiology of zoonotic diseases. Given the damage of rodents to humans and economic loss and due to their health importance, parasitological studies on rodents seem necessary [2]. Several studies have been done on parasitic infections of wild rodent in Iran [5–10]. However, due to ecological differences in different areas of the country, the parasitic fauna of the rodents in each ecological setting might be different. is notion justifies new studies on para- sitic infection of the rodents in other areas of the country. e current study aimed to assess the parasitic protozoan infec- tions of rodents in Boyer-Ahmad district, southwest Iran. 2. Materials and Methods 2.1. e Study Area. Boyer-Ahmad district is located in Kohgiluyeh and Boyer-Ahmad province. e province is located in southwest of Iran with geographical coordinates of 30 40 12 N, 51 36 0 E. e province has two types Hindawi Publishing Corporation Veterinary Medicine International Volume 2016, Article ID 3263868, 5 pages http://dx.doi.org/10.1155/2016/3263868

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Page 1: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

Research ArticleProtozoan Parasites of Rodents and Their ZoonoticSignificance in Boyer-Ahmad District Southwestern Iran

Zeinab Seifollahi Bahador Sarkari Mohammad Hossein Motazedian Qasem AsgariMohammad Javad Ranjbar and Samaneh Abdolahi Khabisi

Department of Parasitology and Mycology School of Medicine Shiraz University of Medical Sciences Shiraz Iran

Correspondence should be addressed to Bahador Sarkari sarkaribsumsacir

Received 30 September 2015 Revised 24 January 2016 Accepted 28 January 2016

Academic Editor Remo Lobetti

Copyright copy 2016 Zeinab Seifollahi et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Backgrounds Wild rodents are reservoirs of various zoonotic diseases such as toxoplasmosis babesiosis and leishmaniasis Thecurrent study aimed to assess the protozoan infection of rodents in Boyer-Ahmad district southwestern Iran Materials andMethods A total of 52 rodents were collected from different parts of Boyer-Ahmad district in Kohgiluyeh and Boyer-Ahmadprovince using Sherman live traps Each rodent was anesthetized with ether according to the ethics of working with animalsand was dissected Samples were taken from various tissues and stool samples were collected from the contents of the colonand small intestines Moreover 2 to 5mL of blood was taken from each of the rodents and the sera were examined for anti-Leishmania antibodies by ELISA or anti-T gondii antibodies by modified agglutination test (MAT) DNA was extracted frombrain tissue samples of each rodent and PCR was used to identify the DNA of T gondii Results Of the 52 stool samples of rodentsstudied by parasitological methods intestinal protozoa infection was seen in 28 cases (538) From 52 rodents 19 (365) wereinfected with Trichomonas 10 (192) with Giardia muris and 11 (212) with Entamoeba spp Also 10 cases (192) were infectedwith Blastocystis 3 (58) were infected with Chilomastix 7 (135) were infected with Endolimax 1 (19) was infected withRetortamonas 3 (577) were infected with T gondii and 6 (1154) were infected with Trypanosoma lewisi Antibodies to Tgondii were detected in the sera of 5 (961) cases Results of the molecular study showed T gondii infection in 3 (577) of therodents Findings of this study showed that rodents in Kohgiluyeh and Boyer-Ahmad province southwestern Iran are infected withseveral blood and intestinal parasites some of them might be potential risks to residents and domestic animals in the region

1 Introduction

Rodents are the most frequent and important mammals onthe Earth because they can adapt themselves to the differentlocations and environmental changes These animals live onalmost every continent except Antarctica [1] Rodents areconsidered as reservoirs of various zoonotic diseases includ-ing toxoplasmosis babesiosis and leishmaniasis [1ndash4] Nev-ertheless rodents cannot directly cause disease in humansand disease is mainly transmitted to humans if humanis in contact with rodentsrsquo feces and secretory materialsTransmission of the zoonotic pathogens to humans can occurvia rodentrsquos urine feces hair and saliva [2] Human activitieswhich change the ecosystem of rodentsrsquo living place havean important role in the epidemiology of zoonotic diseasesGiven the damage of rodents to humans and economic loss

and due to their health importance parasitological studies onrodents seem necessary [2] Several studies have been doneon parasitic infections of wild rodent in Iran [5ndash10] Howeverdue to ecological differences in different areas of the countrythe parasitic fauna of the rodents in each ecological settingmight be different This notion justifies new studies on para-sitic infection of the rodents in other areas of the countryThecurrent study aimed to assess the parasitic protozoan infec-tions of rodents in Boyer-Ahmad district southwest Iran

2 Materials and Methods

21 The Study Area Boyer-Ahmad district is located inKohgiluyeh and Boyer-Ahmad province The province islocated in southwest of Iran with geographical coordinatesof 30∘ 401015840 1210158401015840 N 51∘ 361015840 010158401015840 E The province has two types

Hindawi Publishing CorporationVeterinary Medicine InternationalVolume 2016 Article ID 3263868 5 pageshttpdxdoiorg10115520163263868

2 Veterinary Medicine International

of tropical and cold climate and Boyer-Ahmad district islocated in the cold area The mean of long-term rain andsnow amount is above 600mm in this area and a wide areaof the county is covered with forests of oak wild pistachioand mountain almond The main professions of the peopleare agricultural practice and breeding and raising livestock

22 Rodentsrsquo Collection and Identification Considering themap of the study area 52 rodents were collected from differ-ent parts of Boyer-Ahmad County using Sherman live trapswith roasted almonds as bait in the summer and autumnof 2014 Different areas of the district including villages ofKakan Madvan Tange Sorkh Kal Morgah Mansourabadand Dehno were selected for sampling After transferringto the laboratory the genus and species of rodents wereidentified based on morphological characteristics This wasdone to subsequently find out the rate of protozoan parasitesin each rodentrsquos species

23 Evaluation of Rodentsrsquo Protozoan Infection After trans-ferring the rodents to the laboratory they were anesthetizedwith ether and blood samples were taken from their heartDifferent rodent parts were carefully examined and necessarysamples were prepared Smears were prepared from rodentliver spleen and peripheral blood on glass slides fixedwith methanol and stained with Giemsa Then smears werestudied by an optical microscope with 100x magnification

Temporary staining of rodentrsquos stool samples with Lugolrsquossolution was done for detection of any protozoan cystsor trophozoites The samples were also examined withformalin-ethyl acetate sedimentation and zinc sulfate floata-tion techniques and the obtained materials were observedby conventional light microscope Smears were also preparedfrom the rodent stool samples and stained with trichromeMoreover smears were prepared from the stool sediments orfloated materials obtained by concentration methods fixedwith methanol and stained with acid-fast staining to detectcoccidia parasites in fecal samples

24 Serological Assessment of Rodentsrsquo Sera Samples Rodentsrsquosera were examined by indirect ELISA for anti-Leishmaniaantibodies Moreover MAT was performed on rodent serasamples as previously described to assess anti-T gondiiantibodies [11] Sera were studied in two dilutions of 1 20and 1 40 and samples with MAT titer of 1 40 or higher wereconsidered as positive

25 Molecular Analysis of Rodentsrsquo Tissue Samples DNA wasextracted from brain tissue samples of each rodent usingDNA extraction kit based on the manufacturerrsquos (Yekta-Tajhiz Azma Tehran Iran) instructions PCR was performedto amplify a 529 bp gene of T gondii as described by Edvins-son et al [12]The two primers used were TOXOFCAGGGAGGA AGA CGA AAGTTG and TOXOR CAG ACA CAGTGC ATC TGG ATT PCR products were separated in 15agarose gel and stained with ethidium bromide

26 Statistical Analysis The statistical analysis was per-formed with SPSS software (version 16) Chi-square test was

Figure 1 Trypanosoma lewisi in blood smear of the studied rodentsstained with Giemsa (100x)

used to examine the association between rodentrsquos parasiticinfections and related studied factors such as rodentrsquos speciesgender place of collection and weight

3 Results

A total of 52 rodents were captured during the course of thisstudy including 25 (481) Meriones 15 (288) Rattus 10(192)Apodemus 1 (19)Calomyscus and 1 (19)ArvicolaAmong the captured rodents 28 (538) were males and 24(462) were females

Of the 52 feces samples of rodents examined by parasito-logical methods 37 (711) were infected with at least oneprotozoan parasite whereas 15 (288) of the rodents werenot infected with any intestinal protozoan parasites From52 rodents 19 (365) were infected with Trichomonas 10(192) with G muris 11 (212) with Entamoeba 10 (192)with Blastocystis 3 (58) with Chilomastix 7 (135) withEndolimax and 1 (19) was infected with RetortamonasRegarding the rodentsrsquo infection with blood and tissue proto-zoa 3 (577)were infectedwithT gondii and 6 (1154)withTrypanosoma lewisi (Figure 1) Anti-Leishmania antibodieswere detected in the sera of 8 (1534) of the rodentsamong them were 6 rodents which were also infected withTrypanosoma lewisi No Leishmania parasites were observedin the impression smears of liver or spleen of the seropositiverodents Figure 2 shows a few of intestinal protozoa detectedin trichrome-stained samples of rodentsrsquo feces

Multiple infections were seen in 19 out of 52 (365)rodents Simultaneous infection with Trichomonas and Enta-moeba was seen in 58 Trichomonas and G muris in 19G muris and Trypanosoma in 19 Blastocystis and G murisin 19Trichomonas and Blastocystis in 19 and Entamoebaand Blastocystis in 19 of the rodents Also simultaneousinfection with Blastocystis Trypanosoma and Endolimaxwasobserved in 19 of the rodents

In this study 542 of rodents infected with intestinalprotozoa were female and 458 were male Statisticalanalysis showed no significant correlation between variousprotozoa and gender of the rodents (119875 gt 005)

The highest rates of infection with G muris (70) Tri-chomonas (368) Endolimax (714) Trypanosoma (100)and Blastocystis (60) were seen in Rattus genus and thehighest infection with Entamoeba (545) was seen in thegenusMeriones Statistical analysis showed significant corre-lation between protozoa infection and the rodentrsquos genus (119875 lt005) Table 1 shows the distribution of protozoan infectionsaccording to the rodent genus

Veterinary Medicine International 3

(a) (b)

(c)

Figure 2 Protozoa in stool samples of the rodents stained with trichrome (a) Entamoeba trophozoite (b) Trichomonas trophozoite and (c)Endolimax trophozoite (100x)

Table 1 Distribution of protozoan infection according to genus of the studied rodents

Rattus Meriones Calomyscus Apodemus Arvicola TotalNumber Number Number Number Number Number

G muris 7 70 2 20 0 0 1 10 0 0 10 1923Trichomonas 7 368 4 211 1 53 7 368 0 0 19 365Blastocystis 6 60 2 20 1 10 1 10 0 0 10 1923Entamoeba 4 364 6 545 0 0 1 19 0 0 11 211Chilomastix 1 333 1 333 0 0 1 333 0 0 3 58Endolimax 5 714 1 143 0 0 1 333 0 0 7 1346Retortamonas 0 0 0 0 0 0 1 100 0 0 1 192Trypanosoma 6 100 0 0 0 0 0 0 0 0 6 1153T gondii 0 0 1 333 1 333 1 333 0 0 3 508

Findings of the molecular study showed T gondii infec-tion in 3 (577) rodents two male and one female Rodentsinfected with T gondii were from Apodemus Meriones andCalomyscus genus Figure 3 shows PCR products of DNAisolated from rodentsrsquo brain tissue

No cases of coccidial infection were seen in any of thefecal samples when the samples were evaluated by modifiedacid-fast staining method

4 Discussion

Rodents are considered as reservoirs for a few of helminthicand protozoan parasites [1 2] Among the protozoa parasitesof rodents is T gondii which is common in rodents and theseanimals can behave as natural reservoir for this protozoaEvaluation of T gondii infection in rodents as the mainpray for cat with regards to the role of cat in spreadingof T gondii oocyst in the environment is important [13]Rate of Toxoplasma infection in rodents is different based onecological status of a given area In the current study T gondiiinfection was common protozoa of the studied rodents Sakiand Khademvatan reported a prevalence rate of 6 for Tgondii in rodents of Ahvaz district south of Iran [14] Studyof Mercier et al in 2013 assessing 766 rodents in Niameydistrict of Niger revealed Toxoplasma infection in 196

1 2 3 4 65

529bp

Figure 3 The PCR product of the DNA of T gondii isolated fromthe rodents brain tissues Lanes 1ndash3 samples isolated from rodentsrsquobrain tissue lane 4 50 bp DNA Ladder lane 5 negative control lane6 positive control (tachyzoite prepared from mice peritonea)

of the studied rodents [15] In the current study T gondiiinfection was found in ApodemusMeriones and Calomyscusgenus and to the best of our knowledge this is the first report

4 Veterinary Medicine International

of molecular detection of T gondii infection in Calomyscusfrom Iran

Another important parasitic infection that rodents havean important role in its transmission as reservoirs is leish-maniasis A large number of species of rodents have beenidentified as reservoir of cutaneous leishmaniasis in Iran [3ndash5]Mohebali et al reported the infection of different species ofthe rodents including Rhombomys opimusMeriones libycusTatera indica and Meriones hurrianae with L major [16]Rassi et al reported thatMeriones libycus is themain reservoirof cutaneous leishmaniasis in Fars province southern Iran[17] In the present study Leishmania infection was notdetected in any of the studied rodents The reason for this isthat leishmaniasis is mainly seen in tropical and subtropicalareas of Iran while Boyer-Ahmad district is located in coldandmountainous region of the country and is not consideredas an endemic focus of cutaneous leishmaniasis Althoughvisceral leishmaniasis is not uncommon in this district itsreservoirs are dogs carnivores or properly cats rather thanrodents [18ndash20]

Rodents are frequently infected with intestinal protozoaand may act as reservoir for a few of them In the cur-rent study intestinal protozoa including Trichomonas Enta-moeba and G muris were detected in the studied rodentsRate of Giardia infection as the main intestinal protozoa inrodents was found to be 146 in Al Hindi and Abu-Haddafstudy in 2013 in Palestine 963 in Microtus and 483 inApodemus species in Poland 25 in the study by Rasti andcolleagues in 2000 in Kashan Iran and 27 in the study byKia and colleagues in 2001 in Ahvaz south of Iran [7 21ndash23]In the current study rate of G muris infection in the rodentswas relatively high Further study is needed to compare thegenotype of these protozoa isolated from the rodents withthe human isolates

Infection with blood protozoa Trypanosoma was com-mon in the studied rodents in our study Lower rate ofinfection (10) with this parasite has been reported in Kiaet al study in Ahvaz south of Iran [7] whereas higher ratesof infection have been reported fromBrazil (217) and India(823) [24 25]

In this study infection with intestinal coccidia was notfound in the rodents while other studies have reportedcoccidia infection in these animals [21]This difference couldbe due to the differences in climatic conditions in the studiedareas and also nutritional or habitat preferences of therodents

Taken together findings of the current study revealedthat rodents in Kohgiluyeh and Boyer-Ahmad province insouthwest of Iran are infectedwithmany intestinal and bloodprotozoa Some of these protozoa may be potential risksto the residents and domestic animals in the region Highprevalence of intestinal protozoan infections in the rodentsmight be linked to the unsafe disposal of human waste andalso use of human and animal fertilizers in the area

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The results described in this paper were part of MSc thesis ofZeinab Seifollahi The study was financially supported by theoffice of vice-chancellor for research of Shiraz University ofMedical Sciences (Grant No 7322-93)

References

[1] B GMeerburg G R Singleton and A Kijlstra ldquoRodent-bornediseases and their risks for public healthrdquo Critical Reviews inMicrobiology vol 35 no 3 pp 221ndash270 2009

[2] B G Meerburg ldquoRodents are a risk factor for the spreading ofpathogens on farmsrdquo Veterinary Microbiology vol 142 no 3-4pp 464ndash465 2010

[3] M H Davami M H Motazedian M Kalantari et al ldquoMolecu-lar survey on detection of Leishmania infection in rodent reser-voirs in Jahrom District Southern Iranrdquo Journal of Arthropod-Borne Diseases vol 8 no 2 pp 139ndash146 2014

[4] B Pourmohammadi M H Motazedian and M KalantarildquoRodent infection with Leishmania in a new focus of humancutaneous leishmaniasis in northern Iranrdquo Annals of TropicalMedicine and Parasitology vol 102 no 2 pp 127ndash133 2008

[5] D Mehrabani M H Motazedian A Oryan Q Asgari GR Hatam and M Karamian ldquoA search for the rodent hostsof Leishmania major in the Larestan region of southern Irandemonstration of the parasite in Tatera indica and Gerbillus spby microscopy culture and PCRrdquo Annals of Tropical Medicineand Parasitology vol 101 no 4 pp 315ndash322 2007

[6] S Gholami H F Motevali E Moabedi and S Shahabi ldquoStudyof helmintic intestinal parasites in the rodents from the ruraland central regions of Mazandaran province in the years 1997to 1999rdquo Journal of Mazandaran University of Medical Sciencesvol 12 no 35 pp 67ndash75 2002

[7] E Kia M Homayouni A Farahnak M Mohebali and SShojai ldquoStudy of endoparasites of rodents and their zoonoticimportance inAhvaz SouthWest Iranrdquo Iranian Journal of PublicHealth vol 30 pp 49ndash52 2001

[8] E B Kia E Shahryary-Rad M Mohebali et al ldquoEndoparasitesof rodents and their zoonotic importance in Germi Dashte-Mogan Ardabil Province Iranrdquo Iranian Journal of Parasitologyvol 5 no 4 pp 15ndash20 2010

[9] S M Sadjjadi and J Massoud ldquoHelminth parasites of wildrodents in Khuzestan province south west of Iranrdquo Journal ofVeterinary Parasitology vol 13 no 1 pp 55ndash56 1999

[10] A Salehabadi G Mowlavi and S M Sadjjadi ldquoHuman infec-tion with Moniliformis moniliformis (Bremser 1811) (Travassos1915) in Iran another case report after three decadesrdquo Vector-Borne and Zoonotic Diseases vol 8 pp 101ndash104 2008

[11] B Sarkari Q Asgari N Bagherian et al ldquoMolecular andSerological evaluation of Toxoplasma gondii infection in rearedturkeys in Fars Province Iranrdquo Jundishapur Journal of Microbi-ology vol 7 no 7 Article ID e11598 2014

[12] B Edvinsson S Jalal C E Nord B S Pedersen and BEvengard ldquoDNA extraction and PCR assays for detection ofToxoplasma gondiirdquo APMIS vol 112 no 6 pp 342ndash348 2004

[13] C Gotteland Y Chaval I Villena et al ldquoSpecies or localenvironment what determines the infection of rodents byToxoplasma gondiirdquo Parasitology vol 141 no 2 pp 259ndash2682014

Veterinary Medicine International 5

[14] J Saki and S Khademvatan ldquoDetection of Toxoplasma gondiiby PCR and mouse bioassay in rodents of Ahvaz DistrictSouthwestern Iranrdquo BioMed Research International vol 2014Article ID 383859 5 pages 2014

[15] A Mercier M Garba H Bonnabau et al ldquoToxoplasmosisseroprevalence in urban rodents a survey in Niamey NigerrdquoMemorias do Instituto Oswaldo Cruz vol 108 no 4 pp 399ndash407 2013

[16] M Mohebali E Javadian M R Yaghoobi-Ershadi A AAkhavan H Hajjaran and M R Abaei ldquoCharacterization ofLeishmania infection in rodents from endemic areas of theIslamicRepublic of IranrdquoEasternMediterraneanHealth Journalvol 10 no 4-5 pp 591ndash599 2004

[17] Y Rassi M Jalali E Javadian and M Moatazedian ldquoConfir-mation ofMeriones libycus (Rodentia Gerbillidae) as the mainreservoir host of zoonotic cutaneous leishmaniasis in arsanjanfars province South of Iran (1999-2000)rdquo Iranian Journal ofPublic Health vol 30 no 3-4 pp 143ndash144 2001

[18] B Sarkari N PedramMMohebali et al ldquoSeroepidemiologicalstudy of visceral leishmaniasis in Booyerahmad district south-west Islamic Republic of Iranrdquo Eastern Mediterranean HealthJournal vol 16 no 11 pp 1133ndash1136 2010

[19] G RHatam S J Adnani QAsgari et al ldquoFirst report of naturalinfection in cats with Leishmania infantum in Iranrdquo Vector-Borne and Zoonotic Diseases vol 10 no 3 pp 313ndash316 2010

[20] B Sarkari G R Hatam S J Adnani andQ Asgari ldquoSeropreva-lence of feline leishmaniasis in areas of Iran where Leishmaniainfantum is endemicrdquoAnnals of TropicalMedicine and Parasitol-ogy vol 103 no 3 pp 275ndash277 2009

[21] A I Al Hindi and E Abu-Haddaf ldquoGastrointestinal parasitesand ectoparasites biodiversity of Rattus rattus trapped fromKhan Younis and Jabalia in Gaza strip Palestinerdquo Journal of theEgyptian Society of Parasitology vol 43 no 1 pp 259ndash268 2013

[22] S Rasti I Moubedi R Dehghani and A Drodgar ldquoThe surveyof gastrointestinal helminths of mice in Kashanrdquo Journal of theFaculty of Veterinary Medicine University of Tehran vol 55 no4 pp 57ndash59 2000

[23] A BajerM BednarskaA Pawełczyk JM Behnke F SGilbertand E Sinski ldquoPrevalence and abundance of Cryptosporidiumparvum andGiardia spp in wild rural rodents from theMazuryLake District region of Polandrdquo Parasitology vol 125 no 1 pp21ndash34 2002

[24] R Laha H Hemaprasanth and D Bhatta-Charya ldquoObserva-tions on prevalence of Trypanosoma lewisi infection in wildrats and a trial on its adaptation in unnatural hostrdquo Journal ofParasitology and Applied Animal Biology vol 6 pp 5ndash8 1997

[25] P M Linardi and J R Botelho ldquoPrevalence of Trypanosomalewisi in Rattus norvegicus from Belo Horizonte State of MinasGerais BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 97 no3 pp 411ndash414 2002

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Page 2: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

2 Veterinary Medicine International

of tropical and cold climate and Boyer-Ahmad district islocated in the cold area The mean of long-term rain andsnow amount is above 600mm in this area and a wide areaof the county is covered with forests of oak wild pistachioand mountain almond The main professions of the peopleare agricultural practice and breeding and raising livestock

22 Rodentsrsquo Collection and Identification Considering themap of the study area 52 rodents were collected from differ-ent parts of Boyer-Ahmad County using Sherman live trapswith roasted almonds as bait in the summer and autumnof 2014 Different areas of the district including villages ofKakan Madvan Tange Sorkh Kal Morgah Mansourabadand Dehno were selected for sampling After transferringto the laboratory the genus and species of rodents wereidentified based on morphological characteristics This wasdone to subsequently find out the rate of protozoan parasitesin each rodentrsquos species

23 Evaluation of Rodentsrsquo Protozoan Infection After trans-ferring the rodents to the laboratory they were anesthetizedwith ether and blood samples were taken from their heartDifferent rodent parts were carefully examined and necessarysamples were prepared Smears were prepared from rodentliver spleen and peripheral blood on glass slides fixedwith methanol and stained with Giemsa Then smears werestudied by an optical microscope with 100x magnification

Temporary staining of rodentrsquos stool samples with Lugolrsquossolution was done for detection of any protozoan cystsor trophozoites The samples were also examined withformalin-ethyl acetate sedimentation and zinc sulfate floata-tion techniques and the obtained materials were observedby conventional light microscope Smears were also preparedfrom the rodent stool samples and stained with trichromeMoreover smears were prepared from the stool sediments orfloated materials obtained by concentration methods fixedwith methanol and stained with acid-fast staining to detectcoccidia parasites in fecal samples

24 Serological Assessment of Rodentsrsquo Sera Samples Rodentsrsquosera were examined by indirect ELISA for anti-Leishmaniaantibodies Moreover MAT was performed on rodent serasamples as previously described to assess anti-T gondiiantibodies [11] Sera were studied in two dilutions of 1 20and 1 40 and samples with MAT titer of 1 40 or higher wereconsidered as positive

25 Molecular Analysis of Rodentsrsquo Tissue Samples DNA wasextracted from brain tissue samples of each rodent usingDNA extraction kit based on the manufacturerrsquos (Yekta-Tajhiz Azma Tehran Iran) instructions PCR was performedto amplify a 529 bp gene of T gondii as described by Edvins-son et al [12]The two primers used were TOXOFCAGGGAGGA AGA CGA AAGTTG and TOXOR CAG ACA CAGTGC ATC TGG ATT PCR products were separated in 15agarose gel and stained with ethidium bromide

26 Statistical Analysis The statistical analysis was per-formed with SPSS software (version 16) Chi-square test was

Figure 1 Trypanosoma lewisi in blood smear of the studied rodentsstained with Giemsa (100x)

used to examine the association between rodentrsquos parasiticinfections and related studied factors such as rodentrsquos speciesgender place of collection and weight

3 Results

A total of 52 rodents were captured during the course of thisstudy including 25 (481) Meriones 15 (288) Rattus 10(192)Apodemus 1 (19)Calomyscus and 1 (19)ArvicolaAmong the captured rodents 28 (538) were males and 24(462) were females

Of the 52 feces samples of rodents examined by parasito-logical methods 37 (711) were infected with at least oneprotozoan parasite whereas 15 (288) of the rodents werenot infected with any intestinal protozoan parasites From52 rodents 19 (365) were infected with Trichomonas 10(192) with G muris 11 (212) with Entamoeba 10 (192)with Blastocystis 3 (58) with Chilomastix 7 (135) withEndolimax and 1 (19) was infected with RetortamonasRegarding the rodentsrsquo infection with blood and tissue proto-zoa 3 (577)were infectedwithT gondii and 6 (1154)withTrypanosoma lewisi (Figure 1) Anti-Leishmania antibodieswere detected in the sera of 8 (1534) of the rodentsamong them were 6 rodents which were also infected withTrypanosoma lewisi No Leishmania parasites were observedin the impression smears of liver or spleen of the seropositiverodents Figure 2 shows a few of intestinal protozoa detectedin trichrome-stained samples of rodentsrsquo feces

Multiple infections were seen in 19 out of 52 (365)rodents Simultaneous infection with Trichomonas and Enta-moeba was seen in 58 Trichomonas and G muris in 19G muris and Trypanosoma in 19 Blastocystis and G murisin 19Trichomonas and Blastocystis in 19 and Entamoebaand Blastocystis in 19 of the rodents Also simultaneousinfection with Blastocystis Trypanosoma and Endolimaxwasobserved in 19 of the rodents

In this study 542 of rodents infected with intestinalprotozoa were female and 458 were male Statisticalanalysis showed no significant correlation between variousprotozoa and gender of the rodents (119875 gt 005)

The highest rates of infection with G muris (70) Tri-chomonas (368) Endolimax (714) Trypanosoma (100)and Blastocystis (60) were seen in Rattus genus and thehighest infection with Entamoeba (545) was seen in thegenusMeriones Statistical analysis showed significant corre-lation between protozoa infection and the rodentrsquos genus (119875 lt005) Table 1 shows the distribution of protozoan infectionsaccording to the rodent genus

Veterinary Medicine International 3

(a) (b)

(c)

Figure 2 Protozoa in stool samples of the rodents stained with trichrome (a) Entamoeba trophozoite (b) Trichomonas trophozoite and (c)Endolimax trophozoite (100x)

Table 1 Distribution of protozoan infection according to genus of the studied rodents

Rattus Meriones Calomyscus Apodemus Arvicola TotalNumber Number Number Number Number Number

G muris 7 70 2 20 0 0 1 10 0 0 10 1923Trichomonas 7 368 4 211 1 53 7 368 0 0 19 365Blastocystis 6 60 2 20 1 10 1 10 0 0 10 1923Entamoeba 4 364 6 545 0 0 1 19 0 0 11 211Chilomastix 1 333 1 333 0 0 1 333 0 0 3 58Endolimax 5 714 1 143 0 0 1 333 0 0 7 1346Retortamonas 0 0 0 0 0 0 1 100 0 0 1 192Trypanosoma 6 100 0 0 0 0 0 0 0 0 6 1153T gondii 0 0 1 333 1 333 1 333 0 0 3 508

Findings of the molecular study showed T gondii infec-tion in 3 (577) rodents two male and one female Rodentsinfected with T gondii were from Apodemus Meriones andCalomyscus genus Figure 3 shows PCR products of DNAisolated from rodentsrsquo brain tissue

No cases of coccidial infection were seen in any of thefecal samples when the samples were evaluated by modifiedacid-fast staining method

4 Discussion

Rodents are considered as reservoirs for a few of helminthicand protozoan parasites [1 2] Among the protozoa parasitesof rodents is T gondii which is common in rodents and theseanimals can behave as natural reservoir for this protozoaEvaluation of T gondii infection in rodents as the mainpray for cat with regards to the role of cat in spreadingof T gondii oocyst in the environment is important [13]Rate of Toxoplasma infection in rodents is different based onecological status of a given area In the current study T gondiiinfection was common protozoa of the studied rodents Sakiand Khademvatan reported a prevalence rate of 6 for Tgondii in rodents of Ahvaz district south of Iran [14] Studyof Mercier et al in 2013 assessing 766 rodents in Niameydistrict of Niger revealed Toxoplasma infection in 196

1 2 3 4 65

529bp

Figure 3 The PCR product of the DNA of T gondii isolated fromthe rodents brain tissues Lanes 1ndash3 samples isolated from rodentsrsquobrain tissue lane 4 50 bp DNA Ladder lane 5 negative control lane6 positive control (tachyzoite prepared from mice peritonea)

of the studied rodents [15] In the current study T gondiiinfection was found in ApodemusMeriones and Calomyscusgenus and to the best of our knowledge this is the first report

4 Veterinary Medicine International

of molecular detection of T gondii infection in Calomyscusfrom Iran

Another important parasitic infection that rodents havean important role in its transmission as reservoirs is leish-maniasis A large number of species of rodents have beenidentified as reservoir of cutaneous leishmaniasis in Iran [3ndash5]Mohebali et al reported the infection of different species ofthe rodents including Rhombomys opimusMeriones libycusTatera indica and Meriones hurrianae with L major [16]Rassi et al reported thatMeriones libycus is themain reservoirof cutaneous leishmaniasis in Fars province southern Iran[17] In the present study Leishmania infection was notdetected in any of the studied rodents The reason for this isthat leishmaniasis is mainly seen in tropical and subtropicalareas of Iran while Boyer-Ahmad district is located in coldandmountainous region of the country and is not consideredas an endemic focus of cutaneous leishmaniasis Althoughvisceral leishmaniasis is not uncommon in this district itsreservoirs are dogs carnivores or properly cats rather thanrodents [18ndash20]

Rodents are frequently infected with intestinal protozoaand may act as reservoir for a few of them In the cur-rent study intestinal protozoa including Trichomonas Enta-moeba and G muris were detected in the studied rodentsRate of Giardia infection as the main intestinal protozoa inrodents was found to be 146 in Al Hindi and Abu-Haddafstudy in 2013 in Palestine 963 in Microtus and 483 inApodemus species in Poland 25 in the study by Rasti andcolleagues in 2000 in Kashan Iran and 27 in the study byKia and colleagues in 2001 in Ahvaz south of Iran [7 21ndash23]In the current study rate of G muris infection in the rodentswas relatively high Further study is needed to compare thegenotype of these protozoa isolated from the rodents withthe human isolates

Infection with blood protozoa Trypanosoma was com-mon in the studied rodents in our study Lower rate ofinfection (10) with this parasite has been reported in Kiaet al study in Ahvaz south of Iran [7] whereas higher ratesof infection have been reported fromBrazil (217) and India(823) [24 25]

In this study infection with intestinal coccidia was notfound in the rodents while other studies have reportedcoccidia infection in these animals [21]This difference couldbe due to the differences in climatic conditions in the studiedareas and also nutritional or habitat preferences of therodents

Taken together findings of the current study revealedthat rodents in Kohgiluyeh and Boyer-Ahmad province insouthwest of Iran are infectedwithmany intestinal and bloodprotozoa Some of these protozoa may be potential risksto the residents and domestic animals in the region Highprevalence of intestinal protozoan infections in the rodentsmight be linked to the unsafe disposal of human waste andalso use of human and animal fertilizers in the area

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The results described in this paper were part of MSc thesis ofZeinab Seifollahi The study was financially supported by theoffice of vice-chancellor for research of Shiraz University ofMedical Sciences (Grant No 7322-93)

References

[1] B GMeerburg G R Singleton and A Kijlstra ldquoRodent-bornediseases and their risks for public healthrdquo Critical Reviews inMicrobiology vol 35 no 3 pp 221ndash270 2009

[2] B G Meerburg ldquoRodents are a risk factor for the spreading ofpathogens on farmsrdquo Veterinary Microbiology vol 142 no 3-4pp 464ndash465 2010

[3] M H Davami M H Motazedian M Kalantari et al ldquoMolecu-lar survey on detection of Leishmania infection in rodent reser-voirs in Jahrom District Southern Iranrdquo Journal of Arthropod-Borne Diseases vol 8 no 2 pp 139ndash146 2014

[4] B Pourmohammadi M H Motazedian and M KalantarildquoRodent infection with Leishmania in a new focus of humancutaneous leishmaniasis in northern Iranrdquo Annals of TropicalMedicine and Parasitology vol 102 no 2 pp 127ndash133 2008

[5] D Mehrabani M H Motazedian A Oryan Q Asgari GR Hatam and M Karamian ldquoA search for the rodent hostsof Leishmania major in the Larestan region of southern Irandemonstration of the parasite in Tatera indica and Gerbillus spby microscopy culture and PCRrdquo Annals of Tropical Medicineand Parasitology vol 101 no 4 pp 315ndash322 2007

[6] S Gholami H F Motevali E Moabedi and S Shahabi ldquoStudyof helmintic intestinal parasites in the rodents from the ruraland central regions of Mazandaran province in the years 1997to 1999rdquo Journal of Mazandaran University of Medical Sciencesvol 12 no 35 pp 67ndash75 2002

[7] E Kia M Homayouni A Farahnak M Mohebali and SShojai ldquoStudy of endoparasites of rodents and their zoonoticimportance inAhvaz SouthWest Iranrdquo Iranian Journal of PublicHealth vol 30 pp 49ndash52 2001

[8] E B Kia E Shahryary-Rad M Mohebali et al ldquoEndoparasitesof rodents and their zoonotic importance in Germi Dashte-Mogan Ardabil Province Iranrdquo Iranian Journal of Parasitologyvol 5 no 4 pp 15ndash20 2010

[9] S M Sadjjadi and J Massoud ldquoHelminth parasites of wildrodents in Khuzestan province south west of Iranrdquo Journal ofVeterinary Parasitology vol 13 no 1 pp 55ndash56 1999

[10] A Salehabadi G Mowlavi and S M Sadjjadi ldquoHuman infec-tion with Moniliformis moniliformis (Bremser 1811) (Travassos1915) in Iran another case report after three decadesrdquo Vector-Borne and Zoonotic Diseases vol 8 pp 101ndash104 2008

[11] B Sarkari Q Asgari N Bagherian et al ldquoMolecular andSerological evaluation of Toxoplasma gondii infection in rearedturkeys in Fars Province Iranrdquo Jundishapur Journal of Microbi-ology vol 7 no 7 Article ID e11598 2014

[12] B Edvinsson S Jalal C E Nord B S Pedersen and BEvengard ldquoDNA extraction and PCR assays for detection ofToxoplasma gondiirdquo APMIS vol 112 no 6 pp 342ndash348 2004

[13] C Gotteland Y Chaval I Villena et al ldquoSpecies or localenvironment what determines the infection of rodents byToxoplasma gondiirdquo Parasitology vol 141 no 2 pp 259ndash2682014

Veterinary Medicine International 5

[14] J Saki and S Khademvatan ldquoDetection of Toxoplasma gondiiby PCR and mouse bioassay in rodents of Ahvaz DistrictSouthwestern Iranrdquo BioMed Research International vol 2014Article ID 383859 5 pages 2014

[15] A Mercier M Garba H Bonnabau et al ldquoToxoplasmosisseroprevalence in urban rodents a survey in Niamey NigerrdquoMemorias do Instituto Oswaldo Cruz vol 108 no 4 pp 399ndash407 2013

[16] M Mohebali E Javadian M R Yaghoobi-Ershadi A AAkhavan H Hajjaran and M R Abaei ldquoCharacterization ofLeishmania infection in rodents from endemic areas of theIslamicRepublic of IranrdquoEasternMediterraneanHealth Journalvol 10 no 4-5 pp 591ndash599 2004

[17] Y Rassi M Jalali E Javadian and M Moatazedian ldquoConfir-mation ofMeriones libycus (Rodentia Gerbillidae) as the mainreservoir host of zoonotic cutaneous leishmaniasis in arsanjanfars province South of Iran (1999-2000)rdquo Iranian Journal ofPublic Health vol 30 no 3-4 pp 143ndash144 2001

[18] B Sarkari N PedramMMohebali et al ldquoSeroepidemiologicalstudy of visceral leishmaniasis in Booyerahmad district south-west Islamic Republic of Iranrdquo Eastern Mediterranean HealthJournal vol 16 no 11 pp 1133ndash1136 2010

[19] G RHatam S J Adnani QAsgari et al ldquoFirst report of naturalinfection in cats with Leishmania infantum in Iranrdquo Vector-Borne and Zoonotic Diseases vol 10 no 3 pp 313ndash316 2010

[20] B Sarkari G R Hatam S J Adnani andQ Asgari ldquoSeropreva-lence of feline leishmaniasis in areas of Iran where Leishmaniainfantum is endemicrdquoAnnals of TropicalMedicine and Parasitol-ogy vol 103 no 3 pp 275ndash277 2009

[21] A I Al Hindi and E Abu-Haddaf ldquoGastrointestinal parasitesand ectoparasites biodiversity of Rattus rattus trapped fromKhan Younis and Jabalia in Gaza strip Palestinerdquo Journal of theEgyptian Society of Parasitology vol 43 no 1 pp 259ndash268 2013

[22] S Rasti I Moubedi R Dehghani and A Drodgar ldquoThe surveyof gastrointestinal helminths of mice in Kashanrdquo Journal of theFaculty of Veterinary Medicine University of Tehran vol 55 no4 pp 57ndash59 2000

[23] A BajerM BednarskaA Pawełczyk JM Behnke F SGilbertand E Sinski ldquoPrevalence and abundance of Cryptosporidiumparvum andGiardia spp in wild rural rodents from theMazuryLake District region of Polandrdquo Parasitology vol 125 no 1 pp21ndash34 2002

[24] R Laha H Hemaprasanth and D Bhatta-Charya ldquoObserva-tions on prevalence of Trypanosoma lewisi infection in wildrats and a trial on its adaptation in unnatural hostrdquo Journal ofParasitology and Applied Animal Biology vol 6 pp 5ndash8 1997

[25] P M Linardi and J R Botelho ldquoPrevalence of Trypanosomalewisi in Rattus norvegicus from Belo Horizonte State of MinasGerais BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 97 no3 pp 411ndash414 2002

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

AnimalsJournal of

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Agronomy

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

InsectsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Case Reports in Veterinary Medicine

Page 3: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

Veterinary Medicine International 3

(a) (b)

(c)

Figure 2 Protozoa in stool samples of the rodents stained with trichrome (a) Entamoeba trophozoite (b) Trichomonas trophozoite and (c)Endolimax trophozoite (100x)

Table 1 Distribution of protozoan infection according to genus of the studied rodents

Rattus Meriones Calomyscus Apodemus Arvicola TotalNumber Number Number Number Number Number

G muris 7 70 2 20 0 0 1 10 0 0 10 1923Trichomonas 7 368 4 211 1 53 7 368 0 0 19 365Blastocystis 6 60 2 20 1 10 1 10 0 0 10 1923Entamoeba 4 364 6 545 0 0 1 19 0 0 11 211Chilomastix 1 333 1 333 0 0 1 333 0 0 3 58Endolimax 5 714 1 143 0 0 1 333 0 0 7 1346Retortamonas 0 0 0 0 0 0 1 100 0 0 1 192Trypanosoma 6 100 0 0 0 0 0 0 0 0 6 1153T gondii 0 0 1 333 1 333 1 333 0 0 3 508

Findings of the molecular study showed T gondii infec-tion in 3 (577) rodents two male and one female Rodentsinfected with T gondii were from Apodemus Meriones andCalomyscus genus Figure 3 shows PCR products of DNAisolated from rodentsrsquo brain tissue

No cases of coccidial infection were seen in any of thefecal samples when the samples were evaluated by modifiedacid-fast staining method

4 Discussion

Rodents are considered as reservoirs for a few of helminthicand protozoan parasites [1 2] Among the protozoa parasitesof rodents is T gondii which is common in rodents and theseanimals can behave as natural reservoir for this protozoaEvaluation of T gondii infection in rodents as the mainpray for cat with regards to the role of cat in spreadingof T gondii oocyst in the environment is important [13]Rate of Toxoplasma infection in rodents is different based onecological status of a given area In the current study T gondiiinfection was common protozoa of the studied rodents Sakiand Khademvatan reported a prevalence rate of 6 for Tgondii in rodents of Ahvaz district south of Iran [14] Studyof Mercier et al in 2013 assessing 766 rodents in Niameydistrict of Niger revealed Toxoplasma infection in 196

1 2 3 4 65

529bp

Figure 3 The PCR product of the DNA of T gondii isolated fromthe rodents brain tissues Lanes 1ndash3 samples isolated from rodentsrsquobrain tissue lane 4 50 bp DNA Ladder lane 5 negative control lane6 positive control (tachyzoite prepared from mice peritonea)

of the studied rodents [15] In the current study T gondiiinfection was found in ApodemusMeriones and Calomyscusgenus and to the best of our knowledge this is the first report

4 Veterinary Medicine International

of molecular detection of T gondii infection in Calomyscusfrom Iran

Another important parasitic infection that rodents havean important role in its transmission as reservoirs is leish-maniasis A large number of species of rodents have beenidentified as reservoir of cutaneous leishmaniasis in Iran [3ndash5]Mohebali et al reported the infection of different species ofthe rodents including Rhombomys opimusMeriones libycusTatera indica and Meriones hurrianae with L major [16]Rassi et al reported thatMeriones libycus is themain reservoirof cutaneous leishmaniasis in Fars province southern Iran[17] In the present study Leishmania infection was notdetected in any of the studied rodents The reason for this isthat leishmaniasis is mainly seen in tropical and subtropicalareas of Iran while Boyer-Ahmad district is located in coldandmountainous region of the country and is not consideredas an endemic focus of cutaneous leishmaniasis Althoughvisceral leishmaniasis is not uncommon in this district itsreservoirs are dogs carnivores or properly cats rather thanrodents [18ndash20]

Rodents are frequently infected with intestinal protozoaand may act as reservoir for a few of them In the cur-rent study intestinal protozoa including Trichomonas Enta-moeba and G muris were detected in the studied rodentsRate of Giardia infection as the main intestinal protozoa inrodents was found to be 146 in Al Hindi and Abu-Haddafstudy in 2013 in Palestine 963 in Microtus and 483 inApodemus species in Poland 25 in the study by Rasti andcolleagues in 2000 in Kashan Iran and 27 in the study byKia and colleagues in 2001 in Ahvaz south of Iran [7 21ndash23]In the current study rate of G muris infection in the rodentswas relatively high Further study is needed to compare thegenotype of these protozoa isolated from the rodents withthe human isolates

Infection with blood protozoa Trypanosoma was com-mon in the studied rodents in our study Lower rate ofinfection (10) with this parasite has been reported in Kiaet al study in Ahvaz south of Iran [7] whereas higher ratesof infection have been reported fromBrazil (217) and India(823) [24 25]

In this study infection with intestinal coccidia was notfound in the rodents while other studies have reportedcoccidia infection in these animals [21]This difference couldbe due to the differences in climatic conditions in the studiedareas and also nutritional or habitat preferences of therodents

Taken together findings of the current study revealedthat rodents in Kohgiluyeh and Boyer-Ahmad province insouthwest of Iran are infectedwithmany intestinal and bloodprotozoa Some of these protozoa may be potential risksto the residents and domestic animals in the region Highprevalence of intestinal protozoan infections in the rodentsmight be linked to the unsafe disposal of human waste andalso use of human and animal fertilizers in the area

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The results described in this paper were part of MSc thesis ofZeinab Seifollahi The study was financially supported by theoffice of vice-chancellor for research of Shiraz University ofMedical Sciences (Grant No 7322-93)

References

[1] B GMeerburg G R Singleton and A Kijlstra ldquoRodent-bornediseases and their risks for public healthrdquo Critical Reviews inMicrobiology vol 35 no 3 pp 221ndash270 2009

[2] B G Meerburg ldquoRodents are a risk factor for the spreading ofpathogens on farmsrdquo Veterinary Microbiology vol 142 no 3-4pp 464ndash465 2010

[3] M H Davami M H Motazedian M Kalantari et al ldquoMolecu-lar survey on detection of Leishmania infection in rodent reser-voirs in Jahrom District Southern Iranrdquo Journal of Arthropod-Borne Diseases vol 8 no 2 pp 139ndash146 2014

[4] B Pourmohammadi M H Motazedian and M KalantarildquoRodent infection with Leishmania in a new focus of humancutaneous leishmaniasis in northern Iranrdquo Annals of TropicalMedicine and Parasitology vol 102 no 2 pp 127ndash133 2008

[5] D Mehrabani M H Motazedian A Oryan Q Asgari GR Hatam and M Karamian ldquoA search for the rodent hostsof Leishmania major in the Larestan region of southern Irandemonstration of the parasite in Tatera indica and Gerbillus spby microscopy culture and PCRrdquo Annals of Tropical Medicineand Parasitology vol 101 no 4 pp 315ndash322 2007

[6] S Gholami H F Motevali E Moabedi and S Shahabi ldquoStudyof helmintic intestinal parasites in the rodents from the ruraland central regions of Mazandaran province in the years 1997to 1999rdquo Journal of Mazandaran University of Medical Sciencesvol 12 no 35 pp 67ndash75 2002

[7] E Kia M Homayouni A Farahnak M Mohebali and SShojai ldquoStudy of endoparasites of rodents and their zoonoticimportance inAhvaz SouthWest Iranrdquo Iranian Journal of PublicHealth vol 30 pp 49ndash52 2001

[8] E B Kia E Shahryary-Rad M Mohebali et al ldquoEndoparasitesof rodents and their zoonotic importance in Germi Dashte-Mogan Ardabil Province Iranrdquo Iranian Journal of Parasitologyvol 5 no 4 pp 15ndash20 2010

[9] S M Sadjjadi and J Massoud ldquoHelminth parasites of wildrodents in Khuzestan province south west of Iranrdquo Journal ofVeterinary Parasitology vol 13 no 1 pp 55ndash56 1999

[10] A Salehabadi G Mowlavi and S M Sadjjadi ldquoHuman infec-tion with Moniliformis moniliformis (Bremser 1811) (Travassos1915) in Iran another case report after three decadesrdquo Vector-Borne and Zoonotic Diseases vol 8 pp 101ndash104 2008

[11] B Sarkari Q Asgari N Bagherian et al ldquoMolecular andSerological evaluation of Toxoplasma gondii infection in rearedturkeys in Fars Province Iranrdquo Jundishapur Journal of Microbi-ology vol 7 no 7 Article ID e11598 2014

[12] B Edvinsson S Jalal C E Nord B S Pedersen and BEvengard ldquoDNA extraction and PCR assays for detection ofToxoplasma gondiirdquo APMIS vol 112 no 6 pp 342ndash348 2004

[13] C Gotteland Y Chaval I Villena et al ldquoSpecies or localenvironment what determines the infection of rodents byToxoplasma gondiirdquo Parasitology vol 141 no 2 pp 259ndash2682014

Veterinary Medicine International 5

[14] J Saki and S Khademvatan ldquoDetection of Toxoplasma gondiiby PCR and mouse bioassay in rodents of Ahvaz DistrictSouthwestern Iranrdquo BioMed Research International vol 2014Article ID 383859 5 pages 2014

[15] A Mercier M Garba H Bonnabau et al ldquoToxoplasmosisseroprevalence in urban rodents a survey in Niamey NigerrdquoMemorias do Instituto Oswaldo Cruz vol 108 no 4 pp 399ndash407 2013

[16] M Mohebali E Javadian M R Yaghoobi-Ershadi A AAkhavan H Hajjaran and M R Abaei ldquoCharacterization ofLeishmania infection in rodents from endemic areas of theIslamicRepublic of IranrdquoEasternMediterraneanHealth Journalvol 10 no 4-5 pp 591ndash599 2004

[17] Y Rassi M Jalali E Javadian and M Moatazedian ldquoConfir-mation ofMeriones libycus (Rodentia Gerbillidae) as the mainreservoir host of zoonotic cutaneous leishmaniasis in arsanjanfars province South of Iran (1999-2000)rdquo Iranian Journal ofPublic Health vol 30 no 3-4 pp 143ndash144 2001

[18] B Sarkari N PedramMMohebali et al ldquoSeroepidemiologicalstudy of visceral leishmaniasis in Booyerahmad district south-west Islamic Republic of Iranrdquo Eastern Mediterranean HealthJournal vol 16 no 11 pp 1133ndash1136 2010

[19] G RHatam S J Adnani QAsgari et al ldquoFirst report of naturalinfection in cats with Leishmania infantum in Iranrdquo Vector-Borne and Zoonotic Diseases vol 10 no 3 pp 313ndash316 2010

[20] B Sarkari G R Hatam S J Adnani andQ Asgari ldquoSeropreva-lence of feline leishmaniasis in areas of Iran where Leishmaniainfantum is endemicrdquoAnnals of TropicalMedicine and Parasitol-ogy vol 103 no 3 pp 275ndash277 2009

[21] A I Al Hindi and E Abu-Haddaf ldquoGastrointestinal parasitesand ectoparasites biodiversity of Rattus rattus trapped fromKhan Younis and Jabalia in Gaza strip Palestinerdquo Journal of theEgyptian Society of Parasitology vol 43 no 1 pp 259ndash268 2013

[22] S Rasti I Moubedi R Dehghani and A Drodgar ldquoThe surveyof gastrointestinal helminths of mice in Kashanrdquo Journal of theFaculty of Veterinary Medicine University of Tehran vol 55 no4 pp 57ndash59 2000

[23] A BajerM BednarskaA Pawełczyk JM Behnke F SGilbertand E Sinski ldquoPrevalence and abundance of Cryptosporidiumparvum andGiardia spp in wild rural rodents from theMazuryLake District region of Polandrdquo Parasitology vol 125 no 1 pp21ndash34 2002

[24] R Laha H Hemaprasanth and D Bhatta-Charya ldquoObserva-tions on prevalence of Trypanosoma lewisi infection in wildrats and a trial on its adaptation in unnatural hostrdquo Journal ofParasitology and Applied Animal Biology vol 6 pp 5ndash8 1997

[25] P M Linardi and J R Botelho ldquoPrevalence of Trypanosomalewisi in Rattus norvegicus from Belo Horizonte State of MinasGerais BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 97 no3 pp 411ndash414 2002

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

AnimalsJournal of

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Agronomy

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

InsectsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Case Reports in Veterinary Medicine

Page 4: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

4 Veterinary Medicine International

of molecular detection of T gondii infection in Calomyscusfrom Iran

Another important parasitic infection that rodents havean important role in its transmission as reservoirs is leish-maniasis A large number of species of rodents have beenidentified as reservoir of cutaneous leishmaniasis in Iran [3ndash5]Mohebali et al reported the infection of different species ofthe rodents including Rhombomys opimusMeriones libycusTatera indica and Meriones hurrianae with L major [16]Rassi et al reported thatMeriones libycus is themain reservoirof cutaneous leishmaniasis in Fars province southern Iran[17] In the present study Leishmania infection was notdetected in any of the studied rodents The reason for this isthat leishmaniasis is mainly seen in tropical and subtropicalareas of Iran while Boyer-Ahmad district is located in coldandmountainous region of the country and is not consideredas an endemic focus of cutaneous leishmaniasis Althoughvisceral leishmaniasis is not uncommon in this district itsreservoirs are dogs carnivores or properly cats rather thanrodents [18ndash20]

Rodents are frequently infected with intestinal protozoaand may act as reservoir for a few of them In the cur-rent study intestinal protozoa including Trichomonas Enta-moeba and G muris were detected in the studied rodentsRate of Giardia infection as the main intestinal protozoa inrodents was found to be 146 in Al Hindi and Abu-Haddafstudy in 2013 in Palestine 963 in Microtus and 483 inApodemus species in Poland 25 in the study by Rasti andcolleagues in 2000 in Kashan Iran and 27 in the study byKia and colleagues in 2001 in Ahvaz south of Iran [7 21ndash23]In the current study rate of G muris infection in the rodentswas relatively high Further study is needed to compare thegenotype of these protozoa isolated from the rodents withthe human isolates

Infection with blood protozoa Trypanosoma was com-mon in the studied rodents in our study Lower rate ofinfection (10) with this parasite has been reported in Kiaet al study in Ahvaz south of Iran [7] whereas higher ratesof infection have been reported fromBrazil (217) and India(823) [24 25]

In this study infection with intestinal coccidia was notfound in the rodents while other studies have reportedcoccidia infection in these animals [21]This difference couldbe due to the differences in climatic conditions in the studiedareas and also nutritional or habitat preferences of therodents

Taken together findings of the current study revealedthat rodents in Kohgiluyeh and Boyer-Ahmad province insouthwest of Iran are infectedwithmany intestinal and bloodprotozoa Some of these protozoa may be potential risksto the residents and domestic animals in the region Highprevalence of intestinal protozoan infections in the rodentsmight be linked to the unsafe disposal of human waste andalso use of human and animal fertilizers in the area

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The results described in this paper were part of MSc thesis ofZeinab Seifollahi The study was financially supported by theoffice of vice-chancellor for research of Shiraz University ofMedical Sciences (Grant No 7322-93)

References

[1] B GMeerburg G R Singleton and A Kijlstra ldquoRodent-bornediseases and their risks for public healthrdquo Critical Reviews inMicrobiology vol 35 no 3 pp 221ndash270 2009

[2] B G Meerburg ldquoRodents are a risk factor for the spreading ofpathogens on farmsrdquo Veterinary Microbiology vol 142 no 3-4pp 464ndash465 2010

[3] M H Davami M H Motazedian M Kalantari et al ldquoMolecu-lar survey on detection of Leishmania infection in rodent reser-voirs in Jahrom District Southern Iranrdquo Journal of Arthropod-Borne Diseases vol 8 no 2 pp 139ndash146 2014

[4] B Pourmohammadi M H Motazedian and M KalantarildquoRodent infection with Leishmania in a new focus of humancutaneous leishmaniasis in northern Iranrdquo Annals of TropicalMedicine and Parasitology vol 102 no 2 pp 127ndash133 2008

[5] D Mehrabani M H Motazedian A Oryan Q Asgari GR Hatam and M Karamian ldquoA search for the rodent hostsof Leishmania major in the Larestan region of southern Irandemonstration of the parasite in Tatera indica and Gerbillus spby microscopy culture and PCRrdquo Annals of Tropical Medicineand Parasitology vol 101 no 4 pp 315ndash322 2007

[6] S Gholami H F Motevali E Moabedi and S Shahabi ldquoStudyof helmintic intestinal parasites in the rodents from the ruraland central regions of Mazandaran province in the years 1997to 1999rdquo Journal of Mazandaran University of Medical Sciencesvol 12 no 35 pp 67ndash75 2002

[7] E Kia M Homayouni A Farahnak M Mohebali and SShojai ldquoStudy of endoparasites of rodents and their zoonoticimportance inAhvaz SouthWest Iranrdquo Iranian Journal of PublicHealth vol 30 pp 49ndash52 2001

[8] E B Kia E Shahryary-Rad M Mohebali et al ldquoEndoparasitesof rodents and their zoonotic importance in Germi Dashte-Mogan Ardabil Province Iranrdquo Iranian Journal of Parasitologyvol 5 no 4 pp 15ndash20 2010

[9] S M Sadjjadi and J Massoud ldquoHelminth parasites of wildrodents in Khuzestan province south west of Iranrdquo Journal ofVeterinary Parasitology vol 13 no 1 pp 55ndash56 1999

[10] A Salehabadi G Mowlavi and S M Sadjjadi ldquoHuman infec-tion with Moniliformis moniliformis (Bremser 1811) (Travassos1915) in Iran another case report after three decadesrdquo Vector-Borne and Zoonotic Diseases vol 8 pp 101ndash104 2008

[11] B Sarkari Q Asgari N Bagherian et al ldquoMolecular andSerological evaluation of Toxoplasma gondii infection in rearedturkeys in Fars Province Iranrdquo Jundishapur Journal of Microbi-ology vol 7 no 7 Article ID e11598 2014

[12] B Edvinsson S Jalal C E Nord B S Pedersen and BEvengard ldquoDNA extraction and PCR assays for detection ofToxoplasma gondiirdquo APMIS vol 112 no 6 pp 342ndash348 2004

[13] C Gotteland Y Chaval I Villena et al ldquoSpecies or localenvironment what determines the infection of rodents byToxoplasma gondiirdquo Parasitology vol 141 no 2 pp 259ndash2682014

Veterinary Medicine International 5

[14] J Saki and S Khademvatan ldquoDetection of Toxoplasma gondiiby PCR and mouse bioassay in rodents of Ahvaz DistrictSouthwestern Iranrdquo BioMed Research International vol 2014Article ID 383859 5 pages 2014

[15] A Mercier M Garba H Bonnabau et al ldquoToxoplasmosisseroprevalence in urban rodents a survey in Niamey NigerrdquoMemorias do Instituto Oswaldo Cruz vol 108 no 4 pp 399ndash407 2013

[16] M Mohebali E Javadian M R Yaghoobi-Ershadi A AAkhavan H Hajjaran and M R Abaei ldquoCharacterization ofLeishmania infection in rodents from endemic areas of theIslamicRepublic of IranrdquoEasternMediterraneanHealth Journalvol 10 no 4-5 pp 591ndash599 2004

[17] Y Rassi M Jalali E Javadian and M Moatazedian ldquoConfir-mation ofMeriones libycus (Rodentia Gerbillidae) as the mainreservoir host of zoonotic cutaneous leishmaniasis in arsanjanfars province South of Iran (1999-2000)rdquo Iranian Journal ofPublic Health vol 30 no 3-4 pp 143ndash144 2001

[18] B Sarkari N PedramMMohebali et al ldquoSeroepidemiologicalstudy of visceral leishmaniasis in Booyerahmad district south-west Islamic Republic of Iranrdquo Eastern Mediterranean HealthJournal vol 16 no 11 pp 1133ndash1136 2010

[19] G RHatam S J Adnani QAsgari et al ldquoFirst report of naturalinfection in cats with Leishmania infantum in Iranrdquo Vector-Borne and Zoonotic Diseases vol 10 no 3 pp 313ndash316 2010

[20] B Sarkari G R Hatam S J Adnani andQ Asgari ldquoSeropreva-lence of feline leishmaniasis in areas of Iran where Leishmaniainfantum is endemicrdquoAnnals of TropicalMedicine and Parasitol-ogy vol 103 no 3 pp 275ndash277 2009

[21] A I Al Hindi and E Abu-Haddaf ldquoGastrointestinal parasitesand ectoparasites biodiversity of Rattus rattus trapped fromKhan Younis and Jabalia in Gaza strip Palestinerdquo Journal of theEgyptian Society of Parasitology vol 43 no 1 pp 259ndash268 2013

[22] S Rasti I Moubedi R Dehghani and A Drodgar ldquoThe surveyof gastrointestinal helminths of mice in Kashanrdquo Journal of theFaculty of Veterinary Medicine University of Tehran vol 55 no4 pp 57ndash59 2000

[23] A BajerM BednarskaA Pawełczyk JM Behnke F SGilbertand E Sinski ldquoPrevalence and abundance of Cryptosporidiumparvum andGiardia spp in wild rural rodents from theMazuryLake District region of Polandrdquo Parasitology vol 125 no 1 pp21ndash34 2002

[24] R Laha H Hemaprasanth and D Bhatta-Charya ldquoObserva-tions on prevalence of Trypanosoma lewisi infection in wildrats and a trial on its adaptation in unnatural hostrdquo Journal ofParasitology and Applied Animal Biology vol 6 pp 5ndash8 1997

[25] P M Linardi and J R Botelho ldquoPrevalence of Trypanosomalewisi in Rattus norvegicus from Belo Horizonte State of MinasGerais BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 97 no3 pp 411ndash414 2002

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

AnimalsJournal of

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Agronomy

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

InsectsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Case Reports in Veterinary Medicine

Page 5: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

Veterinary Medicine International 5

[14] J Saki and S Khademvatan ldquoDetection of Toxoplasma gondiiby PCR and mouse bioassay in rodents of Ahvaz DistrictSouthwestern Iranrdquo BioMed Research International vol 2014Article ID 383859 5 pages 2014

[15] A Mercier M Garba H Bonnabau et al ldquoToxoplasmosisseroprevalence in urban rodents a survey in Niamey NigerrdquoMemorias do Instituto Oswaldo Cruz vol 108 no 4 pp 399ndash407 2013

[16] M Mohebali E Javadian M R Yaghoobi-Ershadi A AAkhavan H Hajjaran and M R Abaei ldquoCharacterization ofLeishmania infection in rodents from endemic areas of theIslamicRepublic of IranrdquoEasternMediterraneanHealth Journalvol 10 no 4-5 pp 591ndash599 2004

[17] Y Rassi M Jalali E Javadian and M Moatazedian ldquoConfir-mation ofMeriones libycus (Rodentia Gerbillidae) as the mainreservoir host of zoonotic cutaneous leishmaniasis in arsanjanfars province South of Iran (1999-2000)rdquo Iranian Journal ofPublic Health vol 30 no 3-4 pp 143ndash144 2001

[18] B Sarkari N PedramMMohebali et al ldquoSeroepidemiologicalstudy of visceral leishmaniasis in Booyerahmad district south-west Islamic Republic of Iranrdquo Eastern Mediterranean HealthJournal vol 16 no 11 pp 1133ndash1136 2010

[19] G RHatam S J Adnani QAsgari et al ldquoFirst report of naturalinfection in cats with Leishmania infantum in Iranrdquo Vector-Borne and Zoonotic Diseases vol 10 no 3 pp 313ndash316 2010

[20] B Sarkari G R Hatam S J Adnani andQ Asgari ldquoSeropreva-lence of feline leishmaniasis in areas of Iran where Leishmaniainfantum is endemicrdquoAnnals of TropicalMedicine and Parasitol-ogy vol 103 no 3 pp 275ndash277 2009

[21] A I Al Hindi and E Abu-Haddaf ldquoGastrointestinal parasitesand ectoparasites biodiversity of Rattus rattus trapped fromKhan Younis and Jabalia in Gaza strip Palestinerdquo Journal of theEgyptian Society of Parasitology vol 43 no 1 pp 259ndash268 2013

[22] S Rasti I Moubedi R Dehghani and A Drodgar ldquoThe surveyof gastrointestinal helminths of mice in Kashanrdquo Journal of theFaculty of Veterinary Medicine University of Tehran vol 55 no4 pp 57ndash59 2000

[23] A BajerM BednarskaA Pawełczyk JM Behnke F SGilbertand E Sinski ldquoPrevalence and abundance of Cryptosporidiumparvum andGiardia spp in wild rural rodents from theMazuryLake District region of Polandrdquo Parasitology vol 125 no 1 pp21ndash34 2002

[24] R Laha H Hemaprasanth and D Bhatta-Charya ldquoObserva-tions on prevalence of Trypanosoma lewisi infection in wildrats and a trial on its adaptation in unnatural hostrdquo Journal ofParasitology and Applied Animal Biology vol 6 pp 5ndash8 1997

[25] P M Linardi and J R Botelho ldquoPrevalence of Trypanosomalewisi in Rattus norvegicus from Belo Horizonte State of MinasGerais BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 97 no3 pp 411ndash414 2002

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

AnimalsJournal of

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Agronomy

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

InsectsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Case Reports in Veterinary Medicine

Page 6: Research Article Protozoan Parasites of Rodents …downloads.hindawi.com/journals/vmi/2016/3263868.pdfRodents are considered as reservoirs for a few of helminthic and protozoan parasites

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

AnimalsJournal of

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Agronomy

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

InsectsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Case Reports in Veterinary Medicine