{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:26:26Z","timestamp":1760149586213,"version":"build-2065373602"},"reference-count":56,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2023,8,18]],"date-time":"2023-08-18T00:00:00Z","timestamp":1692316800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Linguatula serrata (Fr\u00f6lich, 1789) is a widespread parasite known as the tongue worm belonging to the family Linguatulidae. The adult form of the parasite is usually located in the upper respiratory tract of domestic and wild carnivores while the larval forms are located in the visceral organs of intermediate hosts (various herbivorous mammals). Twenty-four European brown hares (Lepus europaeus) were examined in this study, of which two were positive with L. serrata nymphs. The collected nymphs were examined morphologically using electron-microscopic analysis and molecularly by amplification of 18S rRNA and COX1 genes. Lung tissue samples were also collected and histopathological examination was performed. Histopathological examination revealed the following lesions: generalized inflammatory oedema, granulomas with necrosis, calcification and fibrosis in the bronchial tree. The results of molecular sequencing for L. serrata specimens collected from the European brown hares are deposited in GenBank. This study presents the first report on Linguatula serrata nymphs collected from L. europaeus in Romania, using molecular and morphological characterization simultaneously.<\/jats:p>","DOI":"10.3390\/ijms241612927","type":"journal-article","created":{"date-parts":[[2023,8,18]],"date-time":"2023-08-18T10:14:38Z","timestamp":1692353678000},"page":"12927","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Characterization of the Tongue Worm, Linguatula serrata (Pentastomida), Identified from Hares (Lepus europaeus) in Romania"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1536-9874","authenticated-orcid":false,"given":"Beatrice Ana-Maria","family":"Jitea","sequence":"first","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mirela","family":"Imre","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tiana","family":"Florea","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C\u0103t\u0103lin Bogdan","family":"S\u00eerbu","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Iasmina","family":"Luca","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adrian","family":"Stancu","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexandru C\u0103lin","family":"Cire\u0219an","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gheorghe","family":"D\u0103r\u0103bu\u0219","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Life Sciences \u201cKing Michael I\u201d from Timisoara, Calea Aradului 119, 300645 Timisoara, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"publisher","first-page":"3517","DOI":"10.1007\/s00436-013-3534-9","article-title":"Phylogenetic position of Linguatula arctica and Linguatula serrata (Pentastomida) as inferred from the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I gene","volume":"112","author":"Gjerde","year":"2013","journal-title":"Parasitol. Res."},{"key":"ref_2","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.ijppaw.2017.08.008","article-title":"Occurrence of tongue worm, Linguatula cf. serrata (Pentastomida: Linguatilidae) in wild canids and livestock in south-eastern Australia","volume":"6","author":"Shamsi","year":"2017","journal-title":"Int. J. Parasitol. Parasites. Wildl."},{"key":"ref_3","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1071\/ZO20017","article-title":"First report of nymphs of the introduced pentastomid, Linguatula serrata, in red-necked wallabies (Notamacropus rufogriseus) in Australia","volume":"67","author":"Barton","year":"2019","journal-title":"Aust. J. Zool."},{"key":"ref_4","doi-asserted-by":"publisher","first-page":"1553","DOI":"10.1007\/s00436-020-06670-y","article-title":"Verification of rabbits as intermediate hosts for Linguatula serrata (Pentastomida) in Australia","volume":"119","author":"Barton","year":"2020","journal-title":"Parasitol. Res."},{"key":"ref_5","first-page":"131","article-title":"Nymphal Linguatulosis in Indian Crested Porcupines (Histrix indica) in Southwest of Iran","volume":"9","author":"Rajabloo","year":"2015","journal-title":"J. Arthropod.-Borne Dis."},{"key":"ref_6","unstructured":"Baker, J.R., and Muller, R. (1986). Advances in Parasitology, Academic Press."},{"key":"ref_7","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1093\/clinids\/9.6.1087","article-title":"Pentastomiasis","volume":"9","author":"Drabick","year":"1987","journal-title":"Rev. Infect. Dis."},{"key":"ref_8","first-page":"808","article-title":"Prevalence of Linguatula serrata in domestic ruminants in South India","volume":"39","author":"Ravindran","year":"2008","journal-title":"Southeast Asian J. Trop. Med."},{"key":"ref_9","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1007\/s12639-012-0104-5","article-title":"The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran","volume":"36","author":"Rezaei","year":"2012","journal-title":"J. Parasit. Dis."},{"key":"ref_10","doi-asserted-by":"publisher","first-page":"879","DOI":"10.1007\/s11250-018-1768-3","article-title":"Effect of age, sex, and season on the prevalence of Linguatula serrata infestation in mesenteric lymph nodes of goats slaughtered in Tabriz, Iran","volume":"51","author":"Hajipour","year":"2019","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_11","doi-asserted-by":"publisher","first-page":"28","DOI":"10.16988\/iuvfd.266125","article-title":"Prevalence of Linguatula serrata infection in domestic ruminants in west part of Iran: Risk factors and public health implications","volume":"43","author":"Brahmat","year":"2017","journal-title":"IUVFD"},{"key":"ref_12","doi-asserted-by":"publisher","first-page":"197","DOI":"10.22192\/ijarbs.2017.04.08.024","article-title":"Prevalence of Linguatula serrata (Order: Pentastomida) nymphs parasitizing Camels and Goats with experimental infestation of dogs in Egypt","volume":"4","author":"Marwa","year":"2017","journal-title":"Int. J. Adv. Res. Biol. Sci."},{"key":"ref_13","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1016\/S2221-1691(12)60247-0","article-title":"The prevalence of Linguatula serrata nymphs in camels slaughtered in Mashhad slaughterhouse, Northeast, Iran","volume":"2","author":"Fard","year":"2012","journal-title":"Asian Pac. J. Trop. Biomed."},{"key":"ref_14","doi-asserted-by":"publisher","first-page":"870","DOI":"10.3201\/eid1705.100790","article-title":"Linguatula serrata tongue worm in human eye, Austria","volume":"17","author":"Koehsler","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_15","doi-asserted-by":"publisher","first-page":"916120","DOI":"10.1155\/2014\/916120","article-title":"Linguatula serrata (Porocephalida: Linguatulidae) infection among client-owned dogs in Jalingo, North Eastern Nigeria: Prevalence and public health implications","volume":"5","author":"Oluwasina","year":"2014","journal-title":"J. Parasitol. Res."},{"key":"ref_16","doi-asserted-by":"publisher","first-page":"PMC3544120","DOI":"10.4103\/2277-9175.100142","article-title":"A case report of Linguatula serrata infestation from rural area of Isfahan city, Iran","volume":"1","author":"Tabibian","year":"2012","journal-title":"Adv. Biomed. Res."},{"key":"ref_17","unstructured":"Unat, E.K., Y\u00fccel, K., Alta\u015f, K., and Samast\u0131, M. (1995). Unat\u2019\u0131n T\u0131p Parazitolojisi. \u0130nsan\u0131n \u00d6karyonlu Parazitleri ve Bunlarla Olu\u015fan Hastal\u0131klar\u0131, \u0130stanbul \u00dcniversitesi Cerrahpa\u015fa T\u0131p Fak. Vakf\u0131 Yay\u0131nlar\u0131. Yay\u0131n."},{"key":"ref_18","doi-asserted-by":"publisher","first-page":"405","DOI":"10.4269\/ajtmh.1999.60.405","article-title":"Ocular linguatuliasis in Ecuador: Case report and morphometric study of the larva of Linguatula serrata","volume":"60","author":"Lazo","year":"1999","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_19","first-page":"439","article-title":"A case report of Linguatula serrata in human throat from Tehran, central Iran","volume":"55","author":"Maleky","year":"2001","journal-title":"Indian J. Med. Sci."},{"key":"ref_20","doi-asserted-by":"publisher","first-page":"198","DOI":"10.3109\/00313028809066635","article-title":"Hepatic granuloma in a man from North America caused by a nymph of Linguatula serrata","volume":"20","author":"Baird","year":"1988","journal-title":"Pathology"},{"key":"ref_21","doi-asserted-by":"publisher","first-page":"480","DOI":"10.3348\/kjr.2010.11.4.480","article-title":"Imaging features of pediatric pentastomiasis infection: A case report","volume":"11","author":"Lai","year":"2010","journal-title":"Korean J. Radiol."},{"key":"ref_22","first-page":"54","article-title":"A case of concomitant hepatic lesion in a child with cystic hydatid disease and Arthropoda larva (nymph)","volume":"1","author":"Lukmanova","year":"2007","journal-title":"Med. Parazitol."},{"key":"ref_23","first-page":"787","article-title":"Human nasopharyngeal linguatuliasis (Pentasomida) caused by Linguatula serrata","volume":"29","author":"Morsy","year":"1999","journal-title":"J. Egypt. Soc. Parasitol."},{"key":"ref_24","first-page":"105","article-title":"A nodular pulmonary lesion due to Linguatula serrata in an HIV-positive man","volume":"43","author":"Pampiglione","year":"2001","journal-title":"Parassitologia"},{"key":"ref_25","doi-asserted-by":"publisher","first-page":"762","DOI":"10.4269\/ajtmh.1962.11.762","article-title":"The occurrence of Linguatula serrata, Pentastomid, within the Human Eye","volume":"11","author":"Rendtorff","year":"1962","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_26","doi-asserted-by":"publisher","first-page":"85","DOI":"10.15654\/TPK-170651","article-title":"Linguatula serrata (Pentastomida: Linguatulidae) infection in dog, Romania: A case report","volume":"5","author":"Mitrea","year":"2016","journal-title":"AgroLife Sci. J."},{"key":"ref_27","first-page":"694","article-title":"Diagnosis epidemiologic observations in dog linguatulosis","volume":"52","author":"Negrea","year":"2009","journal-title":"Lucr. \u0218tiin\u021bif. Med. Vet. USAMV Ion Ionescu Brad Ia\u0219i."},{"key":"ref_28","first-page":"17","article-title":"Helminthic zoonoses in wild carnivours species from Romanian fauna","volume":"2","author":"Gherman","year":"2002","journal-title":"Scient Parasitol."},{"key":"ref_29","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1002\/vrc2.281","article-title":"Tongue worm (Linguatula serrata) infection in a dog imported into the United Kingdom from Romania","volume":"10","author":"Macrelli","year":"2022","journal-title":"Vet. Rec. Case Rep."},{"key":"ref_30","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1136\/vr.m4207","article-title":"Threat of exotic worms in dogs imported from Romania","volume":"187","author":"Wright","year":"2020","journal-title":"Vet. Rec."},{"key":"ref_31","doi-asserted-by":"publisher","first-page":"100717","DOI":"10.1016\/j.vprsr.2022.100717","article-title":"Linguatula serrata in an imported dog in Germany: Single-case or emerging disease?","volume":"30","author":"Berberich","year":"2022","journal-title":"Vet. Parasitol. Reg. Stud. Rep."},{"key":"ref_32","doi-asserted-by":"publisher","first-page":"1385","DOI":"10.1007\/s00436-008-0951-2","article-title":"Histological evidence of inoculative action of immature Linguatula serrata \u00een lymph nodes of intermediate host","volume":"102","author":"Mihalca","year":"2008","journal-title":"Parasitol. Res."},{"key":"ref_33","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1292\/jvms.16-0508","article-title":"Molecular characterization and phylogeny of Linguatula serrata (Pentastomida: Linguatulidae) based on the nuclear 18S rDNA and mitochondrial cytochrome c oxidase I gene","volume":"79","author":"Mohanta","year":"2017","journal-title":"J. Vet. Med. Sci."},{"key":"ref_34","first-page":"61","article-title":"Prevalence and morphological characterizations of Linguatula serrata nymphs in camels in Isfahan Province, Iran","volume":"3","author":"Rezaei","year":"2012","journal-title":"Vet. Res. Forum."},{"key":"ref_35","doi-asserted-by":"publisher","first-page":"2379","DOI":"10.1007\/s00436-022-07566-9","article-title":"Characterization of tongue worms, Linguatula spp. (Pentastomida) in Romania, with the first record of an unknown adult Linguatula from roe deer (Capreolus jamdani, Linnaeus)","volume":"121","author":"Barton","year":"2022","journal-title":"Parasitol. Res."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Raele, D.A., Petrella, A., Troiano, P., and Cafiero, M.A. (2022). Linguatula serrata (Fr\u00f6hlich, 1789) in Gray Wolf (Canis lupus) from Italy: A Neglected Zoonotic Parasite. Pathogens, 11.","DOI":"10.3390\/pathogens11121523"},{"key":"ref_37","doi-asserted-by":"publisher","first-page":"687","DOI":"10.12681\/jhvms.16077","article-title":"The first report of Linguatula serrata in grey wolf (Canis lupus) from Central Balkans","volume":"68","year":"2017","journal-title":"J. Hell. Vet. Med. Soc."},{"key":"ref_38","doi-asserted-by":"publisher","first-page":"220","DOI":"10.3389\/fvets.2017.00220","article-title":"Endoparasites of wild mammals sheltered in wildlife hospitals and rehabilitation centres in Greece","volume":"4","author":"Liatis","year":"2017","journal-title":"Front. Vet. Sci."},{"key":"ref_39","unstructured":"Diakou, A., Karaiosif, R., Petridou, M., and Iliopoulos, Y. (2014, January 25). Endoparasites of the wolf (Canis lupus) in central Greece. Poster No 113. Proceedings of the EWDA 2014\u201411th European Wildlife Disease Association Conference, Edinburgh, UK."},{"key":"ref_40","doi-asserted-by":"publisher","first-page":"206","DOI":"10.15547\/bjvm.1040","article-title":"Incidence of Linguatula serrata nymphs and pathological lesions of mesenteric lymph nodes in cattle from Urmia","volume":"21","author":"Tavassoli","year":"2018","journal-title":"Iran. Bulg. J. Vet. Med."},{"key":"ref_41","first-page":"282","article-title":"Human Linguatulosis caused by Linguatula serrata in the city of Kerman, South-Eastern Iran-Case Report","volume":"9","author":"Yazdani","year":"2014","journal-title":"Iran. J. Parasitol."},{"key":"ref_42","doi-asserted-by":"publisher","first-page":"47","DOI":"10.5152\/tpd.2011.12","article-title":"A nasopharyngeal human infestation caused by Linguatula serrata nymphs in Van Province: A Case Report","volume":"35","author":"Cengiz","year":"2011","journal-title":"Turk. Parazitol. Derg."},{"key":"ref_43","first-page":"2","article-title":"A case report of Linguatula serrata in human pharynx from Shiraz, Southern Iran","volume":"12","author":"Sadjjadi","year":"1998","journal-title":"MJIRI"},{"key":"ref_44","doi-asserted-by":"publisher","first-page":"3045","DOI":"10.1007\/s00436-021-07272-y","article-title":"Global status of neglected human Linguatula infection: A systematic review of published case reports","volume":"120","author":"Tabaripour","year":"2021","journal-title":"Parasitol. Res."},{"key":"ref_45","doi-asserted-by":"publisher","first-page":"100465","DOI":"10.1016\/j.vprsr.2020.100465","article-title":"Linguatula serrata in cattle in southeastern Iran: Epidemiological, histopathological and phylogenetic profile and its zoonotic importance","volume":"22","author":"Mohammadi","year":"2020","journal-title":"Vet. Parasitol. Reg. Stud. Rep."},{"key":"ref_46","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.vprsr.2018.06.001","article-title":"Linguatula serrata, a food-borne zoonotic parasite, in livestock in Bangladesh: Some pathologic and epidemiologic aspects","volume":"13","author":"Islam","year":"2018","journal-title":"Vet. Parasitol. Reg. Stud. Rep."},{"key":"ref_47","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.ijppaw.2020.01.010","article-title":"Characterisation of the tongue worm, Linguatula serrata (Pentastomida: Linguatulidae), in Australia","volume":"11","author":"Shamsi","year":"2020","journal-title":"Int. J. Parasitol. Parasites. Wildl."},{"key":"ref_48","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1515\/ap-2015-0027","article-title":"Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial cox1 gene sequences","volume":"61","author":"Ghorashi","year":"2016","journal-title":"Acta Parasitol."},{"key":"ref_49","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1007\/BF00926962","article-title":"Scanning electron microscopy examination of larval Linguatula serrata Fr\u00f6lich (Linguatulidae: Pentastomida)","volume":"69","author":"Banaja","year":"1983","journal-title":"Z. Parasitenkd."},{"key":"ref_50","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1080\/00222938700770401","article-title":"A new species of pentastomid from the nasal passages of the reindeer (Rangifer tarandus) in northern Norway, with speculation about its life-cycle","volume":"21","author":"Riley","year":"1987","journal-title":"J. Nat. Hist."},{"key":"ref_51","doi-asserted-by":"publisher","first-page":"104781","DOI":"10.1016\/j.prevetmed.2019.104781","article-title":"Pathological characteristics of Linguatula serrata (aberrant arthropod) infestation in sheep and factors associated with prevalence in Iran","volume":"172","author":"Hajipour","year":"2019","journal-title":"Prev. Vet. Med."},{"key":"ref_52","doi-asserted-by":"publisher","first-page":"574","DOI":"10.1016\/j.apjtb.2015.04.006","article-title":"Infestation and pathological lesions of some lymph nodes induced by Linguatula serrata nymphs in sheep slaughtered in Shahrekord Area (Southwest Iran), Asian Pac","volume":"5","author":"Hamidreza","year":"2015","journal-title":"J. Trop. Biomed."},{"key":"ref_53","unstructured":"Maxie, G. (2015). Pathology of Domestic Animals, Sunders LTD. [6th ed.]."},{"key":"ref_54","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/0035-9203(68)90134-X","article-title":"A note on the occurrence of Linguatula serrata (frohlich, 1789) in domesticated animals","volume":"62","author":"Gill","year":"1968","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_55","doi-asserted-by":"publisher","first-page":"19","DOI":"10.4067\/S0719-81322020000100104","article-title":"Histopathological lesions compatible with nymphs of Linguatula serrata in bovine liver","volume":"52","year":"2020","journal-title":"AJVS"},{"key":"ref_56","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.4103\/0301-4738.149145","article-title":"Linguatula serrata in the anterior chamber of the eye","volume":"62","author":"Bhende","year":"2014","journal-title":"Indian J. Ophthalmol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/16\/12927\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:36:47Z","timestamp":1760128607000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/16\/12927"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,18]]},"references-count":56,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ijms241612927"],"URL":"https:\/\/doi.org\/10.3390\/ijms241612927","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2023,8,18]]}}}