{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T06:03:45Z","timestamp":1791266625821,"version":"4.1.0"},"reference-count":47,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2025,4,3]],"date-time":"2025-04-03T00:00:00Z","timestamp":1743638400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"European Union (NextGenerationEU)"},{"name":"Ministry of Science and Education of the Republic of Croatia"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>The tapeworms Echinococcus granulosus and Echinococcus multilocularis cause two different clinical manifestations in humans: cystic echinococcosis (CE) and alveolar echinococcosis (AE), respectively. Both forms of echinococcosis manifest primarily in the liver, while other organs or tissues are less frequently affected. Simultaneous occurrence of CE and AE is extremely rare, and all previously reported patients exhibited affected livers, while simultaneous infection without liver involvement has not yet been described. Herein, we present an exclusively extrahepatic E. granulosus and E. multilocularis coinfection localized between the calf muscles of a patient. Due to progressive painful local swelling, an abscess was suspected, but there was no improvement after the administration of multiple courses of antibiotics. When imaging diagnostics suggested a parasitic origin of the two identified cystic lesions, positive serology for both species indicated a dual infection. Albendazole therapy was started, and extensive surgical excision was performed. Both species were confirmed using PCR and sequencing from intraoperative samples. The current case shows that coinfection without liver involvement can occur, even in patients from low-incidence regions, which should be considered in the differential diagnosis of patients with unusual clinical presentation.<\/jats:p>","DOI":"10.3390\/pathogens14040343","type":"journal-article","created":{"date-parts":[[2025,4,3]],"date-time":"2025-04-03T04:33:43Z","timestamp":1743654823000},"page":"343","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Double Trouble on the Lower Leg\u2014Unique Human Coinfection with Echinococcus granulosus and Echinococcus multilocularis Without Liver Involvement"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-7901-3835","authenticated-orcid":false,"given":"David","family":"Beck","sequence":"first","affiliation":[{"name":"School of Medicine, University of Zagreb, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4717-7212","authenticated-orcid":false,"given":"Mirjana","family":"Balen Topi\u0107","sequence":"additional","affiliation":[{"name":"School of Medicine, University of Zagreb, 10000 Zagreb, Croatia"},{"name":"University Hospital for Infectious Diseases \u201cDr. Fran Mihaljevi\u0107\u201d, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5927-3201","authenticated-orcid":false,"given":"Klaudija","family":"Vi\u0161kovi\u0107","sequence":"additional","affiliation":[{"name":"University Hospital for Infectious Diseases \u201cDr. Fran Mihaljevi\u0107\u201d, 10000 Zagreb, Croatia"},{"name":"Faculty of Health Studies, University of Rijeka, 51000 Rijeka, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5784-1343","authenticated-orcid":false,"given":"Neven","family":"Papi\u0107","sequence":"additional","affiliation":[{"name":"School of Medicine, University of Zagreb, 10000 Zagreb, Croatia"},{"name":"University Hospital for Infectious Diseases \u201cDr. Fran Mihaljevi\u0107\u201d, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rado","family":"\u017dic","sequence":"additional","affiliation":[{"name":"School of Medicine, University of Zagreb, 10000 Zagreb, Croatia"},{"name":"Department of Plastic, Reconstructive and Aesthetic Surgery, Dubrava University Hospital, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Sviben","sequence":"additional","affiliation":[{"name":"School of Medicine, University of Zagreb, 10000 Zagreb, Croatia"},{"name":"Microbiology Service, Parasitology Department, Croatian National Institute of Public Health, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8751-8149","authenticated-orcid":false,"given":"Tomislav","family":"Me\u0161trovi\u0107","sequence":"additional","affiliation":[{"name":"University Centre Vara\u017edin, University North, 42000 Vara\u017edin, Croatia"},{"name":"Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA 98195, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrijana","family":"Bakovi\u0107 Kova\u010devi\u0107","sequence":"additional","affiliation":[{"name":"Department of Health Ecology, Teaching Institute of Public Health \u201cDr. Andrija \u0160tampar\u201d, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Relja","family":"Beck","sequence":"additional","affiliation":[{"name":"Department for Bacteriology and Parasitology, Croatian Veterinary Institute, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,4,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Conraths, F.J., Probst, C., Possenti, A., Boufana, B., Saulle, R., La Torre, G., Busani, L., and Casulli, A. (2017). Potential risk factors associated with human alveolar echinococcosis: Systematic review and meta-analysis. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005801"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/bs.apar.2016.11.001","article-title":"Global distribution of alveolar and cystic echinococcosis","volume":"95","author":"Deplazes","year":"2017","journal-title":"Adv. Parasitol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/bs.apar.2016.11.002","article-title":"Ecology and life cycle patterns of Echinococcus species","volume":"95","author":"Romig","year":"2017","journal-title":"Adv. Parasitol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1186\/s13071-016-1746-4","article-title":"The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: A systematic review and meta-analysis","volume":"9","author":"Oksanen","year":"2016","journal-title":"Parasit. Vectors"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e00075-18","DOI":"10.1128\/CMR.00075-18","article-title":"Echinococcosis: Advances in the 21st Century","volume":"32","author":"Wen","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/bs.apar.2016.09.006","article-title":"The echinococcoses","volume":"96","author":"Kern","year":"2017","journal-title":"Adv. Parasitol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1017\/S0022149X15000656","article-title":"Human cystic and alveolar echinococcosis in the Tibet Autonomous Region (TAR), China","volume":"89","author":"Feng","year":"2015","journal-title":"J. Helminthol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/0035-9203(92)90314-3","article-title":"A rare case of mixed cystic and alveolar hydatidosis","volume":"86","author":"Wen","year":"1992","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1017\/S0950268897007760","article-title":"Human hydatidosis in Dalmatia, Croatia","volume":"119","year":"1997","journal-title":"Epidemiol. Infect."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1007\/s00436-017-5732-3","article-title":"First detection of Echinococcus multilocularis in Croatia","volume":"117","author":"Beck","year":"2017","journal-title":"Parasitol. Res."},{"key":"ref_11","first-page":"364","article-title":"Human alveolar echinococcosis, Croatia","volume":"26","author":"Vince","year":"2019","journal-title":"Emerg. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Topi\u0107, M.B., Papi\u0107, N., Vi\u0161kovi\u0107, K., Sviben, M., Kani\u017eaj, T.F., Jadrijevi\u0107, S., Jurkovi\u0107, D., and Beck, R. (2023). Emergence of Echinococcus multilocularis in Central Continental Croatia: A Human Case Series and Update on Prevalence in Foxes. Life, 13.","DOI":"10.3390\/life13061402"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/0166-6851(92)90109-W","article-title":"Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing","volume":"54","author":"Bowles","year":"1992","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1017\/S0031182007002235","article-title":"Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA","volume":"134","author":"Trachsel","year":"2007","journal-title":"Parasitology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1017\/S0031182002001749","article-title":"Spatial and temporal aspects of urban transmission of Echinococcus multilocularis","volume":"124","author":"Stieger","year":"2002","journal-title":"Parasitology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1017\/S0031182001008976","article-title":"Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus","volume":"124","author":"Le","year":"2002","journal-title":"Parasitology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1016\/j.ijpara.2005.01.003","article-title":"Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China","volume":"35","author":"Xiao","year":"2005","journal-title":"Int. J. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/s150100050079","article-title":"Extrahepatic Alveolar Echinococcosis without Liver Involvement: A Rare Manifestation","volume":"28","author":"Reuter","year":"2000","journal-title":"Infection"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e80","DOI":"10.1017\/S0022149X19000385","article-title":"Simultaneous occurrence of hepatic alveolar and cystic echinococcosis","volume":"94","author":"Ran","year":"2019","journal-title":"J. Helminthol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.ijscr.2019.06.042","article-title":"Hydatid cyst of the calf presenting as painless mass: A case report","volume":"60","author":"Mohammed","year":"2019","journal-title":"Int. J. Surg. Case Rep."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/s12306-009-0031-5","article-title":"Case report of a primary multiloculate muscular cystic hydatidosis","volume":"93","author":"Notarnicola","year":"2009","journal-title":"Musculoskelet. Surg."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.ijscr.2021.01.087","article-title":"A case report of primary isolated extrahepatic hydatid cyst of the soft tissues of the breast and thigh","volume":"79","author":"Samsami","year":"2021","journal-title":"Int. J. Surg. Case Rep."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e6664","DOI":"10.1002\/ccr3.6664","article-title":"Primary hydatid cyst in the adductor muscles of thigh: A case report","volume":"10","author":"Arian","year":"2022","journal-title":"Clin. Case Rep."},{"key":"ref_24","first-page":"e67929","article-title":"Hydatid cyst in the thigh: An unusual extra-hepatic site","volume":"16","author":"Shetty","year":"2024","journal-title":"Cureus"},{"key":"ref_25","first-page":"123","article-title":"An unusual cause of insidious back and shoulder pain in a man: A case report","volume":"19","author":"Kaya","year":"2024","journal-title":"Iran. J. Parasitol."},{"key":"ref_26","first-page":"e60312","article-title":"A rare presentation of hydatid cyst: A case report of uncommon localization in the pelvic region and a review of current literature","volume":"16","author":"Gurcan","year":"2024","journal-title":"Cureus"},{"key":"ref_27","first-page":"487","article-title":"Gluteal hydatid cyst: A case report","volume":"14","author":"Seyedsadeghi","year":"2019","journal-title":"Iran. J. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Ciobotaru, O.C., Duca, O.-M., Ciobotaru, O.R., Stamate, E., Piraianu, A.I., Dumitrascu, A.G., Constantin, G.B., Matei, M.N., Voinescu, D.C., and Luchian, S.-A. (2024). Hydatid Cysts of the Psoas Muscle: Insights from the Past Five Years. Life, 14.","DOI":"10.3390\/life14101331"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Nell, M., Burgkart, R.H., Gradl, G., Von Eisenhart-Rothe, R., Schaeffeler, C., Trappe, D., Da Costa, C.P., Gradinger, R., and Kirchhoff, C. (2011). Primary extrahepatic alveolar echinococcosis of the lumbar spine and the psoas muscle. Ann. Clin. Microbiol. Antimicrob., 10.","DOI":"10.1186\/1476-0711-10-13"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1007\/s002560050237","article-title":"Bone and soft tissue manifestations of alveolar echinococcosis","volume":"26","author":"Merkle","year":"1997","journal-title":"Skelet. Radiol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Song, T., Peng, S., Zhou, X., Jiang, L., and Zhang, J. (2022). Case Report: Diagnosis of vertebral alveolar echinococcosis upon next-generation sequencing in a suspected tuberculosis. Front. Surg., 9.","DOI":"10.3389\/fsurg.2022.984640"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Koppen, T., Barth, T.F.E., Eichhorn, K.W., Gabrielpillai, J., Kader, R., Bootz, F., and Send, T. (2021). Alveolar Echinococcosis of the Parotid Gland\u2014An Ultra Rare Location Reported from Western Europe. Pathogens, 10.","DOI":"10.3390\/pathogens10040426"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1128\/JCM.01906-12","article-title":"Fatal alveolar echinococcosis of the lumbar spine","volume":"51","author":"Keutgens","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_34","first-page":"168","article-title":"Co-Occurrence of cystic and alveolar echinococcosis in the liver: A case report","volume":"16","author":"Wang","year":"2021","journal-title":"Iran. J. Parasitolog."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"279","DOI":"10.4254\/wjh.v16.i2.279","article-title":"Coinfection with hepatic cystic and alveolar echinococcosis with abdominal wall abscess and sinus tract formation: A case report","volume":"16","author":"Wang","year":"2024","journal-title":"World J. Hepatol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"300060519851651","DOI":"10.1177\/0300060519851651","article-title":"Diagnosis and treatment of a case of hepatic mixed echinococcosis infection combined with distant organ metastasis","volume":"48","author":"Xu","year":"2019","journal-title":"J. Int. Med. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3911","DOI":"10.12998\/wjcc.v8.i17.3911","article-title":"Diagnosis and treatment of mixed infection of hepatic cystic and alveolar echinococcosis: Four case reports","volume":"8","author":"A","year":"2020","journal-title":"World J. Clin. Cases"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Me\u0161trovi\u0107, T., Sviben, M., Juri\u0161i\u0107, A., Stevanovski, F., Beck, R., and Balen Topi\u0107, M. (Clin. Microbiol. Infect., 2025). A ticking time bomb? A position paper on the rising and neglected threat of alveolar echinococcosis in the Republic of Croatia, Clin. Microbiol. Infect., online ahead of print.","DOI":"10.1016\/j.cmi.2025.01.017"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijpara.2005.08.012","article-title":"Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats","volume":"36","author":"Kapel","year":"2006","journal-title":"Int. J. Parasitol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.3201\/eid2808.212514","article-title":"Dog ownership and risk for alveolar echinococcosis, Germany","volume":"28","author":"Schmidberger","year":"2022","journal-title":"Emerg. Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"102214","DOI":"10.1016\/j.parint.2020.102214","article-title":"The occurrence of Echinococcus spp. in golden jackal (Canis aureus) in southwestern Hungary: Should we need to rethink its expansion?","volume":"80","author":"Balog","year":"2020","journal-title":"Parasitol. Int."},{"key":"ref_42","first-page":"e01707","article-title":"Population genetic structure in a rapidly expanding mesocarnivore: Golden jackals in the Dinaric-Pannonian region","volume":"28","author":"Stronen","year":"2021","journal-title":"Glob. Ecol. Conserv."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1515\/ap-2018-0076","article-title":"First identification of Echinococcus multilocularis in golden jackals in Croatia","volume":"63","year":"2018","journal-title":"Acta Parasitol."},{"key":"ref_44","first-page":"1","article-title":"Immunology of Alveolar and Cystic echinococcosis (AE and CE)","volume":"96","author":"Gottstein","year":"2016","journal-title":"Adv. Parasitol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/bs.apar.2016.09.003","article-title":"Laboratory Diagnosis of Echinococcus spp. in Human Patients and Infected Animals","volume":"96","author":"Casulli","year":"2017","journal-title":"Adv. Parasitol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Guo, H., Liu, W., Wang, J., and Xing, Y. (2021). Extrahepatic alveolar echinococcus on multi-slice computed tomography and magnetic resonance imaging. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-89101-x"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e02552021","DOI":"10.1590\/0037-8682-0255-2021","article-title":"Intramuscular hydatid cyst in the lower extremity: Report of three cases","volume":"54","year":"2021","journal-title":"Rev. Soc. Bras. Med. Trop."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/14\/4\/343\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:09:06Z","timestamp":1760029746000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/14\/4\/343"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,3]]},"references-count":47,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2025,4]]}},"alternative-id":["pathogens14040343"],"URL":"https:\/\/doi.org\/10.3390\/pathogens14040343","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,4,3]]}}}