{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T20:45:24Z","timestamp":1783111524700,"version":"3.54.6"},"reference-count":38,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T00:00:00Z","timestamp":1690416000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science, Technological Development and Innovation of the Republic of Serbia","award":["451-03-47\/2023-01\/200143"],"award-info":[{"award-number":["451-03-47\/2023-01\/200143"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The eight-year study (2015\u20132023) was performed on a large sample of poached European pond turtles infected with Haemogregarina stepanowi and held in a pond that belongs to a quarantine section of Belgrade Zoo. The protected species of European pond turtles have been found in poor health, with general weakness, anorexia, and low motility. Comprehensive cytological, hematological, molecular, and postmortem evaluations have been performed. Initially, Diff Quick staining of the blood smears revealed rounded or elongated erythrocytes, often bearing premeront or U-shaped gamont of the hemogregarines inside. The reduced erythrocyte numbers, hemoglobin, and hematocrit values found in the examined population of infected turtles indicated anemia. Macroscopically, shell necrosis and massive skin hemorrhages were the most prominent findings observed in diseased turtles. Microscopically, the lungs, liver, kidneys, and spleen revealed hyperemia, hemorrhages, and the presence of parasitic stages in tissue samples in 31 of 40 necropsied turtles. Cytological and microscopic examination of the samples proved to be sufficient for establishing the infection, but molecular analyses of the 18S sequence were used for phylogenetic studies. Over the years, the number of diseased and dead turtles has decreased, which could be hypothetically attributed to the elimination of leeches as the definitive host.<\/jats:p>","DOI":"10.3390\/ani13152429","type":"journal-article","created":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T01:56:16Z","timestamp":1690509376000},"page":"2429","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Eight-Year Study of Haemogregarina stepanowi Infection in Poached European Pond Turtles (Emys orbicularis) Held in Belgrade Zoo Quarantine"],"prefix":"10.3390","volume":"13","author":[{"given":"Sanja","family":"Aleksi\u0107-Kova\u010devi\u0107","sequence":"first","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3208-147X","authenticated-orcid":false,"given":"Milo\u0161","family":"Vu\u010di\u0107evi\u0107","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00f3zsef","family":"\u00d6zvegy","sequence":"additional","affiliation":[{"name":"Belgrade Zoo, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Jelisi\u0107","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1705-7615","authenticated-orcid":false,"given":"Biljana","family":"Djurdjevi\u0107","sequence":"additional","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, Department of Epizootiology, Clinical Diagnostics and DDD, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6116-3271","authenticated-orcid":false,"given":"Jasna","family":"Prodanov-Radulovi\u0107","sequence":"additional","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, Department of Epizootiology, Clinical Diagnostics and DDD, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Milan","family":"Do\u0161enovi\u0107","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darko","family":"Marinkovi\u0107","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1556\/avet.2013.060","article-title":"Skin and skeletal system lesions of european pond turtles (Emys orbicularis) from natural habitats","volume":"62","author":"Rusvai","year":"2014","journal-title":"Acta Vet Hung."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"76","DOI":"10.2298\/VETGL181208005V","article-title":"Plasma glutathione peroxidase (gpx 3) activity in the freshwater turtle Trachemys scripta elegans after isoflurane inhalation anesthesia","volume":"75","year":"2021","journal-title":"Vet Glas."},{"key":"ref_3","first-page":"131","article-title":"Hematolog\u00eda y citolog\u00eda sangu\u00ednea en reptiles","volume":"31","author":"Cuenca","year":"2011","journal-title":"Clin. Vet. Peq. Anim."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"421","DOI":"10.17221\/5643-VETMED","article-title":"Haematology and plasma chemistry of Bornean River turtles suffering from shell necrosis and haemogregarine parasites","volume":"50","author":"Knotkova","year":"2005","journal-title":"Vet. Med. Czech"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/j.1550-7408.2011.00607.x","article-title":"Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences","volume":"59","author":"Barta","year":"2012","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1017\/S0031182013001820","article-title":"Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885","volume":"141","author":"Kvicerova","year":"2014","journal-title":"Parasitol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1007\/s00436-023-07814-6","article-title":"Molecular characterization of haemosporidian and haemogregarine diversity in southwestern Iberian amphibians and reptiles","volume":"122","author":"Marzal","year":"2023","journal-title":"Parasitol. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1139\/z92-018","article-title":"Prevalence and intensity of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in three turtle species from Ontario, with observations on intraerythrocytic development","volume":"70","author":"Siddall","year":"1992","journal-title":"Can. J. Zool."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1007\/s00436-005-1355-1","article-title":"Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida","volume":"96","author":"Amo","year":"2005","journal-title":"Parasitol. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1136\/vr.155.22.708","article-title":"Haemoparasites from clinical screening of reptiles in South-East Queensland, Australia","volume":"155","author":"Peirce","year":"2004","journal-title":"Vet. Rec."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"324","DOI":"10.2307\/3280826","article-title":"A haemogregarine from the American alligator (Alligator mississippiensis)","volume":"66","author":"Khan","year":"1980","journal-title":"J. Parasitol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1111\/j.1550-7408.1990.tb01257.x","article-title":"Gametogenesis and sporogonic development of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in the leech Placobdella ornata","volume":"37","author":"Siddall","year":"1990","journal-title":"J. Protozool."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"426","DOI":"10.2307\/3283131","article-title":"Merogonic development of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in the leech Placobdella ornata (Glossiphoniidae), its transmission to a chelonian intermediate host and phylogenetic implications","volume":"77","author":"Siddall","year":"1991","journal-title":"J. Parasitol."},{"key":"ref_14","unstructured":"\u00d6zvegy, J. (2016). Morphological Changes of Pond Turtle (Emys orbicularis) Tissues Naturally Infected with the Hemoparasite Haemogregarina stepanowi and Its Molecular and Genetic Identification. [Ph.D. Thesis, University of Belgrade]."},{"key":"ref_15","unstructured":"Telford, S.R. (2009). Hemoparasites of the Reptilia: Color Atlas and Text, CRC Press. [1st ed.]."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1017\/S0031182007004106","article-title":"Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: Evolutionary significance of biological and morphological features","volume":"135","author":"Pakandl","year":"2008","journal-title":"Parasitol."},{"key":"ref_17","first-page":"95","article-title":"BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95\/98\/NT","volume":"41","author":"Hall","year":"1999","journal-title":"Nucleic Acids Symp. Ser."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"637","DOI":"10.7589\/0090-3558-45.3.637","article-title":"Investigation of shell disease in map turtles (Graptemys spp.)","volume":"45","author":"Hensel","year":"2009","journal-title":"J. Wildl. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Muriel, J., Marzal, A., Magallanes, S., Garc\u00eda-Longoria, L., Suarez-Rubio, M., Bates, P.J., and Renner, S.C. (2021). Prevalence and diversity of avian Haemosporidians may vary with anthropogenic disturbance in tropical habitats in Myanmar. Diversity, 13.","DOI":"10.3390\/d13030111"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1645\/GE-1725.1","article-title":"Molecular and morphological description of a Hepatozoon species in reptiles and their ticks in the Northern Territory, Australia","volume":"95","author":"Vilcins","year":"2009","journal-title":"J. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ijppaw.2018.01.008","article-title":"Molecular detection of hemogregarines and haemosporidians in Brazilian free-living testudines","volume":"7","author":"Oliveira","year":"2018","journal-title":"Int. J. Parasitol. Parasites. Wildl."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1730","DOI":"10.1017\/S0031182016001372","article-title":"Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia","volume":"143","author":"Maia","year":"2016","journal-title":"Parasitology"},{"key":"ref_23","first-page":"443","article-title":"Cytological and molecular identification of Haemogregarina Stepanowi in blood samples of the European pond turtle (Emys orbicularis) from quarantine at Belgrade Zoo","volume":"65","year":"2016","journal-title":"Acta Vet."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Mari\u010di\u0107, M., Danon, G., Faria, J.F., and Harris, D.J. (2023). Molecular Screening of Haemogregarine Hemoparasites (Apicomplexa: Adeleorina: Haemogregarinidae) in Populations of Native and Introduced Pond Turtles in Eastern Europe. Microorganisms, 11.","DOI":"10.3390\/microorganisms11041063"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"825","DOI":"10.7589\/JWD-D-21-00084","article-title":"Prevalence and parasite intensity of haemogregarines in African bell hinge-back (Kinixys belliana) and african home\u2019s hinge-back (Kinixys homeana) tortoises in Ibadan, Nigeria","volume":"58","author":"Adetunji","year":"2022","journal-title":"J. Wildl. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1645\/0022-3395(2001)087[1217:TOHBFP]2.0.CO;2","article-title":"Transmission of Haemogregarina balli from painted turtles to snapping turtles through the leech Placobdella ornata","volume":"87","author":"Siddall","year":"2001","journal-title":"J. Parasitol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"173","DOI":"10.14411\/fp.2009.021","article-title":"A redescription of Haemogregarina fitzsimonsi Dias, 1953 and some comments on Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) from southern African tortoises (Cryptodira: Testudinidae), with new host data and distribution records","volume":"56","author":"Cook","year":"2009","journal-title":"Folia Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"118","DOI":"10.5152\/tpd.2013.27","article-title":"On the Occurrence of a Haemogregarinae (Apicomplexa) Parasite from freshwater Turtles of South 24 Parganas, West Bengal, India. Turkiye","volume":"37","author":"Molla","year":"2013","journal-title":"Parazitol. Derg."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1656\/1528-7092(2007)6[191:AAOLPO]2.0.CO;2","article-title":"An assessment of leech parasitism on semi aquatic turtles in the Western Piedmont of North Carolina","volume":"6","author":"McCoy","year":"2007","journal-title":"South. Nat."},{"key":"ref_30","first-page":"281","article-title":"Plasma biochemistry of chelonians of the Geochelone group","volume":"31","author":"Knotkova","year":"2000","journal-title":"Proc. Annu. Meet. Eur. Assoc. Zoo- Wildl. Vet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"361","DOI":"10.2478\/acve-2021-0031","article-title":"Fatal Disseminated Pseudomonas Aeruginosa Infection in a Captive Green Iguana (Iguana Iguana)","volume":"71","author":"Koro","year":"2021","journal-title":"Acta Vet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"490","DOI":"10.2478\/acve-2021-0040","article-title":"Pathoanatomical findings of a green turtle (Chelonia mydas) victim of collision with a motorboat","volume":"71","author":"Attademo","year":"2021","journal-title":"Acta Vet."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"100013","DOI":"10.24072\/pci.ecology.100013","article-title":"Limited dispersal in a vector on territorial hosts","volume":"1","author":"Mennerat","year":"2019","journal-title":"PCI Ecol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s00580-007-0715-x","article-title":"Hematological reference intervals in argentine lizard Tupinambis merianae (Sauria\u2014Teiidae)","volume":"17","author":"Troiano","year":"2008","journal-title":"Comp. Clin. Pathol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.ijppaw.2022.01.004","article-title":"Fatal spirorchiidosis in European pond turtles (Emys orbicularis) in Switzerland","volume":"17","author":"Olias","year":"2022","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_36","first-page":"159","article-title":"Health assessment of captive and free-living european pond turtles (Emys orbicularis) in Switzerland","volume":"53","author":"Segner","year":"2022","journal-title":"J. Zoo Wildl. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"16","DOI":"10.5818\/1529-9651.19.1.16","article-title":"Absence of ranavirus and herpesvirus in a survey of two aquatic turtle species in Illinois","volume":"19","author":"Allender","year":"2009","journal-title":"J. Herpetol. Med. Surg."},{"key":"ref_38","first-page":"68","article-title":"Granulomatous hepatitis associated with Hepatozoon sp. meronts in a southern water snake (Nerodia fasciata pictiventris)","volume":"29","author":"Wozniak","year":"1998","journal-title":"J. Zoo Wildl. Med."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/15\/2429\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:20:43Z","timestamp":1760127643000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/15\/2429"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,27]]},"references-count":38,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ani13152429"],"URL":"https:\/\/doi.org\/10.3390\/ani13152429","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,27]]}}}