Hostname: page-component-84b7d79bbc-x5cpj Total loading time: 0 Render date: 2024-08-01T06:51:30.092Z Has data issue: false hasContentIssue false
  • English
  • Français

First molecular detection and identification of Leishmania species in small wild rodents from Turkey

Published online by Cambridge University Press:  14 May 2020

Mehmet Karakuş ,
Mehmet Ali Öktem ,
Mustafa Sözen ,
Ferhat Matur ,
Faruk Çolak ,
Muhammed Nalçaci Open the ORCID record for Muhammed Nalçaci [Opens in a new window] ,
Yusuf Özbel Open the ORCID record for Yusuf Özbel [Opens in a new window]  and
Seray Töz Open the ORCID record for Seray Töz [Opens in a new window]
Mehmet Karakuş
Affiliation:
University of Health Sciences, Faculty of Medicine, Department of Medical Microbiology, İstanbul, Turkey
Mehmet Ali Öktem
Affiliation:
Dokuz Eylül University, Faculty of Medicine, Department of Microbiology, İzmir, Turkey
Mustafa Sözen
Affiliation:
Zonguldak Bülent Ecevit University, Faculty of Arts and Sciences, Department of Biology, Zonguldak, Turkey
Ferhat Matur
Affiliation:
Dokuz Eylül University, Faculty of Science, Department of Biology, İzmir, Turkey
Faruk Çolak
Affiliation:
Zonguldak Bülent Ecevit University, Faculty of Arts and Sciences, Department of Biology, Zonguldak, Turkey
Muhammed Nalçaci
Affiliation:
Ege University Graduate School of Natural and Applied Sciences, Department of Biology, Bornova, İzmir, Turkey
Yusuf Özbel*
Affiliation:
Ege University, Faculty of Medicine, Department of Parasitology, Izmir, Turkey
Seray Töz
Affiliation:
Ege University, Faculty of Medicine, Department of Parasitology, Izmir, Turkey
*
Author for correspondence: Yusuf ÖZBEL, E-mail: yusuf.ozbel@ege.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

Leishmaniasis is a parasitic disease infecting animals and humans. Two clinical forms (Visceral and cutaneous leishmaniasis) and four species are reported to be present in Turkey. Several studies have investigated canine and human leishmaniasis in Turkey but no study was performed to screen the infection among wild rodents, so far. The present study aims to investigate the role of small wild rodents as reservoir animals for Leishmania spp. in different regions of Turkey. Formalin-preserved tissue samples (spleen, liver, lung) of 712 rodents from 30 provinces were screened for the presence of Leishmania spp. DNA. Before DNA extraction, tissues were dried, rehydrated, and homogenated. Leishmania screening in rodent tissues and species determination was performed with a combination of real-time kDNA and ITS1 polymerase chain reaction protocols. Eight (1.12%) out of 712 animals were found to be positive for Leishmania spp. DNA and species typing revealed five L. infantum, two L. tropica and one L. major among positives. Leishmania major and L. infantum DNA were detected in Apodemus spp. from Zonguldak province located in the Western Black Sea Region, while L. tropica DNA was found in Meriones sp. and Gerbillus dasyurus from Adana and Hatay provinces located in Eastern Mediterranean Region of Turkey. The present study is first to report natural infection of L. infantum, L. major and L. tropica in small wild rodents in Turkey, suggesting their possible roles as reservoirs. Further studies are needed for planning epidemiological studies and also for developing rodent control measures in risky endemic areas to break the transmission cycle.

Keywords

LeishmaniasisL. infantumL. majorL. tropicareservoir animalwild rodents
Type
Research Article
Information
Parasitology , Volume 147 , Issue 10 , September 2020 , pp. 1088 - 1093
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akhoundi, M, Mohebali, M, Asadi, M, Mahmodi, MR, Amraei, K and Mirzaei, A (2013) Molecular characterization of Leishmania spp. in reservoir hosts in endemic foci of zoonotic cutaneous leishmaniasis in Iran. Folia Parasitologia (Praha) 60, 218–224.CrossRefGoogle ScholarPubMed
Alten, B, Maia, C, Afonso, O, Campino, L, Jimenez, M, Gonzalez, E, Molina, R, Banuls, AL, Prudhomme, J, Vergnes, B, Toty, C, Cassan, C, Thierry, M, Sereno, D, Bongiorno, G, Bianchi, R, Khouty, C, Tsirigotakis, N, Dokianakis, E, Antoniou, M, Christodoulou, V, Mazeris, A, Karakus, M, Ozbel, Y, Arserim, SK, Erisoz Kasap, O, Gunay, F, Oguz, G, Kaynas, S, Tsetsvadze, N, Tskhvaradze, L, Giorgobiani, E, Gramiccia, M, Volf, P and Gradoni, L (2015) Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum. PLOS Neglected Tropical Diseases 10, e0004458.CrossRefGoogle Scholar
Ansari, N and Mofidi, S (1950) Contribution l’étude des forms humides de leishmaniose cutané. Bulletin de la Societe de PathologieExotique 43, 601–607.Google Scholar
Baneth, G, Yasur-Landau, D, Gilad, M and Nachum-Biala, Y (2017) Canine leishmaniosis caused by Leishmania major and Leishmania tropica: comparative findings and serology. Parasites and Vectors 10, 113.CrossRefGoogle ScholarPubMed
Can, H, Döşkaya, M, Özdemir, HG, Şahar, EA, Karakavuk, M, Pektaş, B, Karakuş, M, Töz, S, Caner, A, Döşkaya, AD, İz, SG, Özbel, Y and Gürüz, Y (2016) Seroprevalence of Leishmania infection and molecular detection of Leishmania tropica and Leishmania infantum in stray cats of İzmir, Turkey. Experimental Parasitology 167, 109–114.CrossRefGoogle ScholarPubMed
Çetintaş, O, Matur, F and Sözen, M (2017) Distribution and conservation of Acomys cilicicus (mammalia: rodentia) in Turkey. Turkish Journal of Zoology 41, 1059–1068.CrossRefGoogle Scholar
Di Bella, C, Vitale, F, Russo, G, Greco, A, Milazzo, G, Aloise, G and Cagnin, M (2003) Are rodents a potential reservoir for Leishmania infantum in Italy? Journal of Mountain Ecology 7, 125–129.Google Scholar
Dujardin, JC, Campino, L, Canavate, C, Dedet, JP, Gradoni, L, Soteriadou, K, Mazeris, A, Özbel, Y and Boelaert, M (2008) Spread of vector-borne diseases and neglect of leishmaniasis, Europe. Emerging Infectious Diseases 14, 1013–1018.CrossRefGoogle Scholar
Echchakery, M, Chicharro, C, Boussaa, S, Nieto, J, Carrillo, E, Sheila, O, Moreno, J and Bouzmezzough, A (2017) Molecular detection of Leishmania infantum and Leishmania tropica in rodent species from endemic cutaneous leishmaniasis areas in Morocco. Parasites and Vectors 10, 454.CrossRefGoogle ScholarPubMed
Forotuan, M, Khademvatan, S, Majidiani, H, Khalkhali, H, Hedayati-Rad, F, Khashaveh, S and Mohammadzadeh, H (2017) Prevalence of Leishmania species in rodents: a systematic review and meta-analysis in Iran. ActaTropica 172, 164–172.Google Scholar
Ghawar, W, Toumi, A, Snoussi, MA, Chlif, S, Zaatour, A, Boukthir, A, Hamida, NB, Chemkhi, J, Diouani, MF and Ben-Salah, A (2011) Leishmania major infection among Psammomys obesus and Meriones Shawi: reservoirs of zoonotic cutaneous leishmaniasis in Sidi Bouzid (central Tunisia). Vector Borne and Zoonotic Diseases 11, 1561–1568.CrossRefGoogle Scholar
Gürel, MS, Yeşilova, Y, Olgen, MK and Ozbel, Y (2012) Cutaneous leishmaniasis in Turkey. Türkiye Parazitoloji Dergisi 36, 121–129, Review, in Turkish.Google ScholarPubMed
Helhazar, M, Leitao, J, Duarte, A, Tavares, L and da Fonseca, IP (2013) Natural infection of synathropic rodent species Mus musculus and Rattus norvegicus by Leishmania Infantum in Sesimbra and Sintra – Portugal. Parasites and Vectors 6, 88.CrossRefGoogle ScholarPubMed
Jimenez, M, Gonzalez, E, Martin-Martin, I, Hernandez, S and Molina, R (2014) Could wild rabbits (Oryctolagus cuniculus) be reservoirs for Leishmania Infantum in the focus of Madrid, Spain. Veterinary Parasitology 202, 296–300.CrossRefGoogle ScholarPubMed
Kahime, K, Boussaa, S, Bounoua, L, Ouanaimi, F, Messouli, M and Boumezzough, A (2014) Leishmaniasis in Morocco: diseases and vectors. Asian Pacific Journal of Tropical Diseases 4, S530–S534.CrossRefGoogle Scholar
Karakuş, M, Töz, S, Ertabaklar, H, Paşa, S, Atasoy, A, Arserim, SK, Ölgen, MK, Alkan, MZ, Durant, C and Özbel, Y (2015) Evaluation of conjunctival swab sampling in the diagnosis of canine leishmaniasis: a two-year follow-up study in Çukurova plain, Turkey. Veterinary Parasitology 214, 295–302.CrossRefGoogle Scholar
Karakuş, M, Arserim, SK, Erişöz Kasap, Ö, Pekağırbaş, M, Aküzüm, D, Alten, B, Töz, S and Özbel, Y (2019) Vector and reservoir surveillance study in a canine and human leishmaniasis endemic area in most western part of Turkey, Karaburun. Acta Tropica 190, 177–182.CrossRefGoogle Scholar
Kassahun, A, Sadlova, J, Dvorak, V, Kostalova, T, Rohousova, I, Frynta, D, Aghova, T, Yasur-Landau, D, Lemma, W, Hailu, A, Baneth, G, Warburg, A, Volf, P and Votypka, J (2015) Detection of L. donovani And L. tropica In Ethiopian wild rodents. Acta Tropica 145, 39–44.CrossRefGoogle ScholarPubMed
Koltas, IS, Eroglu, F, Alabaz, D and Uzun, S (2014) The emergence of Leishmania major and Leishmaniadonovani in southern Turkey. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 154–158.CrossRefGoogle Scholar
Kryštufek, B and Vohralík, V (2005) Mammals of Turkey and Cyprus (Rodentia Volume I: Sciuridae, Dipodidae, Gliridae, Arvicolinae). Koper: Annales Majora, pp. 149–162.Google Scholar
Kryštufek, B and Vohralík, V (2009) Mammals of Turkey and Cyprus (Rodentia Volume II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae), Koper: Annales Majora, pp. 71–252.Google Scholar
Maroli, M, Pennisi, MG, Di Muccio, T, Khoury, C, Gradoni, L and Gramiccia, M (2007) Infection of sandflies by a cat naturally infected with Leishmania infantum. Veterinary Parasitology 145, 357–360.CrossRefGoogle ScholarPubMed
Navea-Perez, HM, Diaz-Saez, V, Corpas-Lopez, V, Merino-Espinosa, G, Morillas-Marquez, F and Martin-Sanchez, J (2015) Leishmania Infantum in wild rodents: reservoirs or just irrelevant incidental hosts? Parasitology Research 114, 2363–2370.CrossRefGoogle ScholarPubMed
Othman, B, Ghawar, W, Chaouch, M, Ayari, C, Chemkhi, J, Cancino-Faure, B, Tomas-Perez, M, Alcover, MM, Riera, C, Ben-Salah, A, Fisa, R, Ben-Ismail, R and Ben-Abderrezzak, S (2018) First detection of leishmania DNA in Psammomys obesus and Psammomys vexillaris: their potential involvement in the epidemiology of leishmaniasis in Tunisia. Infection. Genetics and Evolution 59, 7–15.CrossRefGoogle Scholar
Özbel, Y, Turgay, N, Alkan, MZ, Babaoğlu, A, ÖzensoyTöz, S and Babalıoğlu, N (2002) A focus of zoonotic visceral leishmaniasis in West Black Sea Region of Turkey: Karabuk. Türkiye Parazitoloji Dergisi 26, 362–366.Google Scholar
Özbilgin, A, Çulha, G, Uzun, S, Harman, M, GünaştıTopal, S, Okudan, F, Zeyrek, F, Gündüz, C, Östan, İ, Karakuş, M, Töz, S, Kurt, Ö, Akyar, I, Erat, A, Güngör, D, Kayabaşı, Ç, Çavuş, İ, Bastien, P, Pratlong, F, Kocagöz, T and Özbel, Y (2016) Leishmaniasis in Turkey: first clinical isolation of Leishmania major from 18 autochthonous cases of Cutaneous Leishmaniasis from four geographical regions of Turkey. Tropical Medicine & International Health 21, 783–791.CrossRefGoogle ScholarPubMed
Özbilgin, A, Töz, S, Harman, M, Günaşti Topal, S, Uzun, S, Okudan, F, Güngör, D, Erat, A, Ertabaklar, H, Ertuğ, S, Gündüz, C, Çavuş, İ, Karakuş, M, Östan Ural, İ, Ölgen, MK, Kayabaşi, Ç, Kurt, Ö and Özbel, Y (2019) The current clinical and geographical situation of cutaneous leishmaniasis based on species identification in Turkey. ActaTropica 190, 59–67.Google ScholarPubMed
Paşa, S, Tetik Vardarlı, A, Erol, N, Karakuş, M, Töz, S, Atasoy, A, Balcıoğlu, İC, Emek Tuna, G, Ermiş, ÖV, Ertabaklar, H and Özbel, Y (2015) Detection of Leishmania major and Leishmania tropica in domestic cats in the Ege region of Turkey. Veterinary Parasitology 212, 389–395.CrossRefGoogle ScholarPubMed
Pourmohammadi, B, Mohammadi-Azni, S and Kalantari, M (2017) Natural infection of Nesokia indica with leishmania major and Leishmania infantum parasites in Damghan city, Northern Iran. Acta Tropica 170, 134–139.CrossRefGoogle ScholarPubMed
Saliba, EK and Oumeish, OY (1999) Reservoir hosts of cutaneous leishmaniasis. Clinics in Dermatology 7, 275–277.CrossRefGoogle Scholar
Sarı, B, Limoncu, ME, Balcıoğlu, İC, Aldemir, A, Tasçı, GT, Kiliç, Y, Toz, S, Demirci, B, Demir, S, Erisoz Kasap, O, Olgen, MK and Ozbel, Y (2015) Seroepidemiological and entomological survey in a new focus of zoonotic visceral leishmaniasis in Kars province, northeastern Turkey. Veterinary Parasitology 209, 179–187.CrossRefGoogle Scholar
Serin, MS, Daglioglu, K, Bagirova, M, Allahverdiyev, A, Uzun, S, Vural, Z, Kayar, B, Tezcan, S, Yetkin, M, Aslan, G, Emekdas, G and Koksal, F (2005) Rapid diagnosis and genotyping of Leishmania Isolates from cutaneous and visceral leishmaniasis by microcapillary cultivation and polymerase chain reaction-restriction fragment length polymorphism of Miniexon region. Diagnostic Microbiology and Infectious Diseases 53, 209–214.CrossRefGoogle ScholarPubMed
Toz, SO, Nasereddin, A, Ozbel, Y, Ertabaklar, H, Culha, G, Sevil, N, Alkan, MZ and Jaffe, CL (2009) Leishmaniasis in Turkey: molecular characterization of Leishmania From human and canine clinical samples. Tropical Medicine and International Health 14, 1401–1406.CrossRefGoogle ScholarPubMed
Toz, SO, Culha, G, Zeyrek, FY, Ertabaklar, H, Alkan, MZ, Vardarlı, AT, Gunduz, C and Ozbel, Y (2013) A real-time ITS1-PCR based method in the diagnosis and species identification of leishmania parasite from human and dog clinical samples in Turkey. PLOS Neglected Tropical Diseases 7, e2205.CrossRefGoogle ScholarPubMed
Tsakmakidis, Ι, Angelopoulou, K, Dovas, CI, Dokianakis, Ε, Tamvakis, Α, Symeonidou, I, Antoniou, Μ and Diakou, Α (2017) Leishmania infection in rodents in Greece. Tropical Medicine and International Health 22, 1523–1532.CrossRefGoogle Scholar
Wilson, DE, Lacher, TE Jr. and Mittermeier, RA (2016) Handbook of the Mammals of the World, vol 6. Barcelona: Lagomorphs and Rodents I. Lynx Edicion.Google Scholar
Wilson, DE, Lacher, TE Jr. and Mittermeier, RA (2017) Handbook of the Mammals of the World, vol 7. Barcelona: Rodents II. Lynx Edicion.Google Scholar
Yiğit, N, Çolak, E, Sözen, M and Karataş, A (2006). Rodents of Türkiye: Türkiye Kemiricileri, 1st Edn. Ankara: Meteksan Yayınevi. [In Turkish].Google Scholar
Yiğit, N, Çolak, E and Sözen, M (2016) A new species of voles, Microtus elbeyli sp. nov., from Turkey with taxonomic overview of social voles distributed in southeastern Anatolia. Turkish Journal of Zoology 40, 73–79.CrossRefGoogle Scholar
Zanet, S, Sposimo, P, Trisciuoglio, A, Giannini, F, Strumia, F and Ferroglio, E (2014) Epidemiology of Leishmania Infantum, Toxoplasma Gondii, and Neospora caninum in Rattus Rattus in absence of domestic reservoir and definitive hosts. Veterinary Parasitology 199, 247–249.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Karakuş et al. supplementary material

Karakuş et al. supplementary material 1

Download Karakuş et al. supplementary material(Image)
Image 735.3 KB
Supplementary material: Image

Karakuş et al. supplementary material

Karakuş et al. supplementary material 2

Download Karakuş et al. supplementary material(Image)
Image 523.7 KB