{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T03:32:10Z","timestamp":1764991930008,"version":"3.46.0"},"reference-count":29,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T00:00:00Z","timestamp":1761955200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,11,15]],"date-time":"2025-11-15T00:00:00Z","timestamp":1763164800000},"content-version":"vor","delay-in-days":14,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Universit\u00e4tsklinikum Ulm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasitol Res"],"published-print":{"date-parts":[[2025,11]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Alveolar echinococcosis (AE) is a rare but severe zoonosis caused by\n                    <jats:italic>Echinococcus multilocularis<\/jats:italic>\n                    that predominantly affects the liver. While previous studies have focused on single ultrasound patterns, the significance of hepatic double pattern lesions is not yet fully understood. The aim of this study is to investigate the prevalence, characteristics and combinations of sonographic double patterns in AE. Based on data from Germany\u2019s national echinococcosis database (n=825),40 patients with AE and confirmed double pattern were analysed retrospectively. Inclusion criteria were patients with at least two hepatic lesions of different patterns on reference ultrasound (US). US images were evaluated using the Echinococcosis Multilocularis Ulm Classification (EMUC)-US classification, with the analysis conducted by independent, blinded sonographers. Overall, a double pattern was detected in 4.8 % of patients (n=40). Ten different pattern combinations between two different patterns were observed, with the hailstorm and ossification patterns being the most common combination (52.2 %). Pattern combinations of up to four patterns were found in a single patient. A statistically significant correlation between the pattern combination and lesion activity, as determined by\n                    <jats:sup>18<\/jats:sup>\n                    FDG-PET\/CT and serological markers, could not be demonstrated. Sonographic double pattern manifestations of AE are rare. Currently, the occurrence of specific patterns and their combinations does not correlate with lesion activity. Further studies with larger sample sizes are needed to better understand the significance of double patterns and their potential prognostic value.\n                  <\/jats:p>","DOI":"10.1007\/s00436-025-08593-y","type":"journal-article","created":{"date-parts":[[2025,11,15]],"date-time":"2025-11-15T17:05:18Z","timestamp":1763226318000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Sonographic double patterns in hepatic alveolar echinococcosis according to the echinococcosis multilocularis ultrasound classification"],"prefix":"10.1007","volume":"124","author":[{"given":"Nele","family":"Hergesell","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dennis","family":"Skotnik","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wolfgang","family":"Kratzer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2025,11,15]]},"reference":[{"key":"8593_CR1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0003964","volume":"9","author":"RW Ammann","year":"2015","unstructured":"Ammann RW, Stumpe KDM, Grimm F, Deplazes P, Huber S, Bertogg K, Fischer DR, M\u00fcllhaupt B (2015) Outcome after discontinuing long-term benzimidazole treatment in 11 patients with non-resectable alveolar echinococcosis with negative FDG-PET\/CT and anti-EmII\/3\u201310 serology. PLoS Negl Trop Dis 9:e0003964. https:\/\/doi.org\/10.1371\/journal.pntd.0003964","journal-title":"PLoS Negl Trop Dis"},{"key":"8593_CR2","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1007\/s15010-019-01325-2","volume":"47","author":"S Baumann","year":"2019","unstructured":"Baumann S, Shi R, Liu W, Bao H, Schmidberger J, Kratzer W, Li W (2019) Worldwide literature on epidemiology of human alveolar echinococcosis: a systematic review of research published in the twenty-first century. Infection 47:703\u201327. https:\/\/doi.org\/10.1007\/s15010-019-01325-2","journal-title":"Infection"},{"key":"8593_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.actatropica.2009.11.001","volume":"114","author":"E Brunetti","year":"2010","unstructured":"Brunetti E, Kern P, Vuitton DA (2010) Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114:1\u201316. https:\/\/doi.org\/10.1016\/j.actatropica.2009.11.001","journal-title":"Acta Trop"},{"key":"8593_CR4","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s13244-022-01190-y","volume":"8","author":"P Calame","year":"2022","unstructured":"Calame P, Weck A, Busse-Cote A, Brumpt E, Richou C, Turco C, Doussot A, Bresson-Hadni S, Delabrousse E (2022) Role of the radiologist in the diagnosis and management of the two forms of hepatic echinococcosis. Insights Imaging 8:13. https:\/\/doi.org\/10.1186\/s13244-022-01190-y","journal-title":"Insights Imaging"},{"key":"8593_CR5","doi-asserted-by":"publisher","first-page":"358","DOI":"10.2967\/jnumed.112.109942","volume":"54","author":"C Caoduro","year":"2013","unstructured":"Caoduro C, Porot C, Vuitton DA, Bresson-Hadni S, Grenouillet F, Richou C, Boulahdour H, Blagosklonov O (2013) The role of delayed 18F-FDG PET imaging in the follow-up of patients with alveolar echinococcosis. J Nucl Med 54:358\u2013363. https:\/\/doi.org\/10.2967\/jnumed.112.109942","journal-title":"J Nucl Med"},{"key":"8593_CR6","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(25)00283-X","author":"A Casulli","year":"2025","unstructured":"Casulli A, Abela B, Petrone D, Soba B, Dezs\u00e9nyi B, Karamon J, Millon L, Saarma U, Antolov\u00e1 D, Chappuis F, Gloor S, Stoeckle M, M\u00fcllhaupt B, Beck R, Lagler H, L\u00f6tsch F, Auer H, Hayette M-P, Kol\u00e1\u0159ov\u00e1 L, Laivacuma S, \u0160ark\u016bnas M, Sokolovas V, Marcinkut\u0117 A, Troell K, Deibel A, Jokelainen P, Sulima M, Krankowska D, Roman S, Joliat G-R, Halkic N, Bresson-Hadni S, Bednarek J, Za\u0142\u0119ski A, Paul M, Yaqub S, Jensenius M, van der Giessen J, Nabarro L, Chiodini P, Demonmerot F, Knapp J, Gr\u00fcner B, Kern P, Peters L, Santolamazza F, Santoro A (2025) Unveiling the incidences and trends of alveolar echinococcosis in europe: a systematic review from the KNOW-PATH project. Lancet Infect Dis. https:\/\/doi.org\/10.1016\/S1473-3099(25)00283-X","journal-title":"Lancet Infect Dis"},{"key":"8593_CR7","doi-asserted-by":"publisher","first-page":"441","DOI":"10.3390\/pathogens11040441","volume":"11","author":"A Deibel","year":"2022","unstructured":"Deibel A, Zu Schwabedissen CM, Husmann L, Grimm F, Deplazes P, Reiner CS, M\u00fcllhaupt B (2022) Characteristics and clinical course of alveolar echinococcosis in patients with Immunosuppression-Associated conditions: A retrospective cohort study. Pathogens 11:441. https:\/\/doi.org\/10.3390\/pathogens11040441","journal-title":"Pathogens"},{"key":"8593_CR8","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.vetpar.2005.03.034","volume":"130","author":"P Deplazes","year":"2005","unstructured":"Deplazes P, Grimm F, Sydler T, Tanner I, Kapel CMO (2005) Experimental alveolar echinococcosis in pigs, lesion development and serological follow up. Vet Parasitol 130:213\u2013222. https:\/\/doi.org\/10.1016\/j.vetpar.2005.03.034","journal-title":"Vet Parasitol"},{"key":"8593_CR9","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens11030348","volume":"11","author":"N Eberhardt","year":"2022","unstructured":"Eberhardt N, Peters L, Kapp-Schwoerer S, Beer M, Beer AJ, Gr\u00fcner B, Thaiss WM (2022) 18F-FDG-PET\/MR in alveolar echinococcosis: multiparametric imaging in a real-world setting. Pathogens 11:348. https:\/\/doi.org\/10.3390\/pathogens11030348","journal-title":"Pathogens"},{"key":"8593_CR10","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1051\/parasite\/2014063","volume":"21","author":"B Gottstein","year":"2014","unstructured":"Gottstein B, Wang J, Blagosklonov O, Grenouillet F, Million L, Vuitton DA, M\u00fcller N (2014) Echinococcus metacestode: in search of viability markers. Parasit 21:63. https:\/\/doi.org\/10.1051\/parasite\/2014063","journal-title":"Parasit"},{"key":"8593_CR11","doi-asserted-by":"publisher","first-page":"102356","DOI":"10.1016\/j.parint.2021.102356","volume":"83","author":"L Husmann","year":"2021","unstructured":"Husmann L, Muehlematter UJ, Grimm F, Ledergerber B, Messerli M, Kudura K, Gr\u00fcnig H, M\u00fcllhaupt B, Hasse B, Huellner MW (2021) PET\/CT helps to determine treatment duration in patients with resected as well as inoperable alveolar echinococcosis. Parasitol Int 83:102356. https:\/\/doi.org\/10.1016\/j.parint.2021.102356","journal-title":"Parasitol Int"},{"key":"8593_CR12","doi-asserted-by":"publisher","first-page":"e37","DOI":"10.1055\/a-1996-3603","volume":"148","author":"N Joos","year":"2023","unstructured":"Joos N, Schmidberger J, Schlingeloff J, Kratzer W (2023) Diagnostic delaying factors in hepatic alveolar echinococcosis. Dtsch Med Wochenschr 148:e37\u2013e43. https:\/\/doi.org\/10.1055\/a-1996-3603","journal-title":"Dtsch Med Wochenschr"},{"key":"8593_CR13","doi-asserted-by":"publisher","DOI":"10.1159\/000545080","author":"W Kratzer","year":"2025","unstructured":"Kratzer W (2025) Ultrasound diagnostics in alveolar echinococcosis: an update. Visc Med. https:\/\/doi.org\/10.1159\/000545080","journal-title":"Visc Med"},{"key":"8593_CR14","doi-asserted-by":"publisher","unstructured":"Kratzer W, Gruener, Kaltenbach TEM, Ansari-Bitzenberger S, Kern P, Fuchs M, Mason RA, Barth TEF, Haenle MM, Hillenbrand A, Oeztuerk S, Graeter T (2015) Proposal of an ultrasonographic classification for hepatic alveolar echinococcosis: Echinococcosis multilocularis Ulm classification-ultrasound. World J Gastroenterol. 21:12392-12402. https:\/\/doi.org\/10.3748\/wjg.v21.i43.12392","DOI":"10.3748\/wjg.v21.i43.12392"},{"key":"8593_CR15","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1055\/a-1694-5552","volume":"43","author":"W Kratzer","year":"2022","unstructured":"Kratzer W, Weimer H, Schmidberger J (2022) Echinococcosis: a challenge for liver sonography. Ultraschall Med 43:120\u2013145. https:\/\/doi.org\/10.1055\/a-1694-5552","journal-title":"Ultraschall Med"},{"key":"8593_CR16","doi-asserted-by":"publisher","DOI":"10.1051\/parasite\/2014072","volume":"21","author":"W Liu","year":"2014","unstructured":"Liu W, Delabrousse E, Blagosklonov O, Wang J, Zeng H, Jiang Y, Wang J, Qin Y, Vuitton DA, Wen H (2014) Innovation in hepatic alveolar echinococcosis imaging: best use of old tools, and necessary evaluation of new ones. Parasite 21:74. https:\/\/doi.org\/10.1051\/parasite\/2014072","journal-title":"Parasite"},{"issue":"1","key":"8593_CR17","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1007\/s15010-022-01866-z","volume":"51","author":"J Philipp","year":"2023","unstructured":"Philipp J, Schmidberger J, Schlingeloff P, Kratzer W (2023) Differentiation of hepatic alveolar echinococcosis with a hemangioma-like pattern compared to typical liver hemangioma using contrast-enhanced ultrasound: a pilot study. Infection 51(1):159\u2013168. https:\/\/doi.org\/10.1007\/s15010-022-01866-z","journal-title":"Infection"},{"key":"8593_CR18","doi-asserted-by":"publisher","first-page":"576","DOI":"10.4269\/ajtmh.1987.36.576","volume":"36","author":"RL Rausch","year":"1987","unstructured":"Rausch RL, Wilson JF, Schantz PM, McMahonet BJ (1987) Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2 ELISA) and clinical significance. Am J Trop Med Hyg 36:576\u2013585. https:\/\/doi.org\/10.4269\/ajtmh.1987.36.576","journal-title":"Am J Trop Med Hyg"},{"key":"8593_CR19","doi-asserted-by":"publisher","unstructured":"Reuter S, Schirrmeister H, Kratzer W, Dreweck C, Reske SN, Kern P (1999) Pericystic metabolic activity in alveolar echinococcosis: assessment and follow-up positron emission tomography. Clin Infect Dis. 29:1157-1163. https:\/\/doi.org\/10.1086\/313438","DOI":"10.1086\/313438"},{"key":"8593_CR20","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1007\/s15010-017-1094-0","volume":"46","author":"J Schmidberger","year":"2018","unstructured":"Schmidberger J, Kratzer W, Stark K, Gr\u00fcner B (2018) Alveolar echinococcosis in Germany, 1992\u20132016. An update based on the newly established National AE database. Infection 46:187\u2013206. https:\/\/doi.org\/10.1007\/s15010-017-1094-0","journal-title":"Infection"},{"key":"8593_CR21","doi-asserted-by":"publisher","first-page":"6939","DOI":"10.3748\/wjg.v27.i40.6939","volume":"27","author":"J Schuhbaur","year":"2021","unstructured":"Schuhbaur J, Schweizer M, Philipp J, Schmidberger J, Schlingeloff P, Kratzer W (2021) Long-term follow-up of liver alveolar echinococcosis using echinococcosis multilocularis ultrasound classification. World J Gastroenterol 27:6939. https:\/\/doi.org\/10.3748\/wjg.v27.i40.6939","journal-title":"World J Gastroenterol"},{"key":"8593_CR22","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s40477-022-00688-x","volume":"26","author":"M Schweizer","year":"2023","unstructured":"Schweizer M, Schmidberger J, Schlingeloff P, Kratzer W (2023) Contrast-enhanced ultrasound (CEUS) in patients with metastasis-like hepatic alveolar echinococcosis: a cohort study. J Ultrasound 26:129\u2013136. https:\/\/doi.org\/10.1007\/s40477-022-00688-x","journal-title":"J Ultrasound"},{"key":"8593_CR23","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s15010-007-6133-9","volume":"35","author":"KDM Stumpe","year":"2007","unstructured":"Stumpe KDM, Renner-Schneiter EC, Kuenzle AK, Grimm F, Kadry Z, Clavien PA, Deplazes P, von Schulthess GK, Muellhaupt B, RWAmmann, Renner EL (2007) F-18-Fluorodeoxyglucose (FDG) Positron-Emission tomography of Echinococcus multilocularis liver lesions: prospective evaluation of its value for diagnosis and Follow-up during benzimidazole therapy. Infection 35:11\u201318. https:\/\/doi.org\/10.1007\/s15010-007-6133-9","journal-title":"Infection"},{"key":"8593_CR24","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1016\/j.advms.2019.04.002","volume":"64","author":"M Sulima","year":"2019","unstructured":"Sulima M, Nahorski W, Gorycki T, Wo\u0142yniec W, W\u0105\u017c P, Felczak-Korzybska I, Szostakowska B, Sikorska K (2019) Ultrasound images in hepatic alveolar echinococcosis and clinical stage of the disease. Adv Med Sci 64:324\u201330. https:\/\/doi.org\/10.1016\/j.advms.2019.04.002","journal-title":"Adv Med Sci"},{"key":"8593_CR25","doi-asserted-by":"publisher","first-page":"4115","DOI":"10.3748\/wjg.v30.i37.4115","volume":"30","author":"Y Tao","year":"2024","unstructured":"Tao Y, Wang Y-F, Wang J, Long S, Seyler BC, Zhong X-F, Lu Q (2024) Pictorial review of hepatic echinococcosis: ultrasound imaging and differential diagnosis. World J Gastroenterol 30:4115\u201331. https:\/\/doi.org\/10.3748\/wjg.v30.i37.4115","journal-title":"World J Gastroenterol"},{"key":"8593_CR26","unstructured":"Tiao-Ying L, Jia-Min Q, Craig PS, Ito A, Yang W, Vuitton DA, Ning X, Xingwang C, Wen Y and Schantz PM (2004) Review of 311 cases of alveolar echinococcosis and criteria for classification of hepatic ultrasound images. Southeast Asian J Trop Med Public Health 35(1)"},{"key":"8593_CR27","doi-asserted-by":"publisher","first-page":"e00075","DOI":"10.1128\/CMR.00075-18","volume":"32","author":"H Wen","year":"2019","unstructured":"Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP (2019) Echinococcosis: advances in the 21st century. Clin Microbiol Rev 32:e00075\u2013e00018. https:\/\/doi.org\/10.1128\/CMR.00075-18","journal-title":"Clin Microbiol Rev"},{"key":"8593_CR28","doi-asserted-by":"publisher","DOI":"10.1016\/S2589-7500(23)00091-2","volume":"5","author":"Y Yang","year":"2023","unstructured":"Yang Y, Cairang Y, Jiang T, Zhou J, Zhang L, Qi B, Ma S, Tang L, Xu D, Bu L, Bu R, Jing X, Wang H, Zhou Z, Zhao C, Luo B, Liu L, Guo J, Nima Y, Hua G, Wa Z, Zhang Y, Zhou G, Jiang W, Wang C, De Y, Yu X, Cheng Z, Han Z, Liu F, Dou J, Feng H, Wu C, Wang R, Hu J, Yang Q, Luo Y, Wu J, Fan H, Liang P, Yu J (2023) Ultrasound identification of hepatic echinococcosis using a deep convolutional neural network model in China: a retrospective, large-scale, multicentre, diagnostic accuracy study. Lancet Digit Health 5:e503\u2013e514. https:\/\/doi.org\/10.1016\/S2589-7500(23)00091-2","journal-title":"Lancet Digit Health"},{"key":"8593_CR29","doi-asserted-by":"publisher","first-page":"3077","DOI":"10.1007\/s00436-021-07262-0","volume":"120","author":"C-R Yangdan","year":"2021","unstructured":"Yangdan C-R, Wang C, Zhang L-Q (2021) Recent advances in ultrasound in the diagnosis and evaluation of the activity of hepatic alveolar echinococcosis. Parasitol Res 120:3077\u201382. https:\/\/doi.org\/10.1007\/s00436-021-07262-0","journal-title":"Parasitol Res"}],"container-title":["Parasitology Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00436-025-08593-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00436-025-08593-y\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00436-025-08593-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T02:29:04Z","timestamp":1764988144000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00436-025-08593-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11]]},"references-count":29,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2025,11]]}},"alternative-id":["8593"],"URL":"https:\/\/doi.org\/10.1007\/s00436-025-08593-y","relation":{},"ISSN":["0932-0113","1432-1955"],"issn-type":[{"type":"print","value":"0932-0113"},{"type":"electronic","value":"1432-1955"}],"subject":[],"published":{"date-parts":[[2025,11]]},"assertion":[{"value":"4 September 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 November 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 November 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was approved by the Ethics Committee from the University of Ulm (reference no.166\/13) and conducted in accordance with the Declaration of Helsinki. Personalized consent was not required for the retrospective study. All patients gave their written consent to be included in the national Echi registry and agreed to the anonymized analysis of their respective data.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Clinical trial number"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"129"}}