{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2024,6,5]],"date-time":"2024-06-05T10:14:35Z","timestamp":1717582475515},"reference-count":22,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"published-print":{"date-parts":[[2013,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Francisellosis, caused by the bacterium <jats:italic>Francisella noatunensis<\/jats:italic> subsp. <jats:italic>noatunensis<\/jats:italic>, remains a serious threat to Atlantic cod (<jats:italic>Gadhus morhua<\/jats:italic>) farming in Norway and potentially in other countries. As outbreak strains appear clonal in population structure, access to highly discriminatory typing tools is critical for understanding the epidemiology of francisellosis infections in aquaculture. In this study, a simplified multiple-locus variable-number of tandem repeat analysis (MLVA) targeting five highly polymorphic variable number of tandem repeat (VNTR) loci in a single multiplex PCR was developed to rapidly discriminate between outbreak strains.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>The assay resulted in identification of at least 13 different allelic profiles or subpopulations among 91\u2009<jats:italic>F. noatunensis<\/jats:italic> isolates from farmed cod in Norway. The VNTR loci appear relatively stable, with isolates originating from individual outbreaks showing identical MLVA profiles following repeated passage. MLVA displayed greater discriminatory power than pulse-field gel electrophoresis (PFGE). Both MLVA and PFGE show good epidemiological concordance by their abilities to separate outbreak strains from epidemiologically unrelated isolates.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>The MLVA method presented here is robust, easy to perform and provides a good alternative to other typing systems for <jats:italic>F. noatunensis<\/jats:italic> subsp. <jats:italic>noatunensis<\/jats:italic> and epidemiological study of francisellosis in cod.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1746-6148-9-252","type":"journal-article","created":{"date-parts":[[2013,12,13]],"date-time":"2013-12-13T02:11:01Z","timestamp":1386900661000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["An improved multiple-locus variable-number of tandem repeat analysis (MLVA) for the fish pathogen Francisella noatunensis using capillary electrophoresis"],"prefix":"10.1186","volume":"9","author":[{"given":"Samuel","family":"Duodu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xihe","family":"Wan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nora Martinussen","family":"Tandstad","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P\u00e4r","family":"Larsson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kerstin","family":"Myrtenn\u00e4s","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andreas","family":"Sj\u00f6din","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mats","family":"Forsman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Duncan J","family":"Colquhoun","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2013,12,13]]},"reference":[{"key":"816_CR1","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1186\/1297-9716-42-47","volume":"42","author":"DJ Colquhoun","year":"2011","unstructured":"Colquhoun DJ, Duodu S: Francisella infections in farmed and wild aquatic organisms. Vet Res. 2011, 42: 47-10.1186\/1297-9716-42-47.","journal-title":"Vet Res"},{"key":"816_CR2","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1007\/s00203-006-0109-5","volume":"185","author":"A Nylund","year":"2006","unstructured":"Nylund A, Ottem KF, Watanabe K, Karlsbakk E, Kross\u00f8y B: Francisella sp. (Family Francisellaceae) causing mortality in Norwegian cod (Gadus morhua) farming. Arch Microbiol. 2006, 185: 383-392. 10.1007\/s00203-006-0109-5.","journal-title":"Arch Microbiol"},{"key":"816_CR3","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1111\/j.1365-2761.2006.00714.x","volume":"29","author":"AB Olsen","year":"2006","unstructured":"Olsen AB, Mikalsen J, Rode M, Alfjorden A, Hoel E, Straum-Lie K, Haldorsen R, Colquhoun DJ: A novel systemic granulomatous inflammatory disease in farmed Atlantic cod Gadus morhua L., associated with a bacterium belonging to the genus Francisella. J Fish Dis. 2006, 29: 307-311. 10.1111\/j.1365-2761.2006.00714.x.","journal-title":"J Fish Dis"},{"key":"816_CR4","doi-asserted-by":"publisher","first-page":"1960","DOI":"10.1099\/ijs.0.64765-0","volume":"57","author":"J Mikalsen","year":"2007","unstructured":"Mikalsen J, Olsen AB, Tengs T, Colquhoun DJ: Francisella philomiragia subsp. noatunensis subsp. nov., isolated from farmed Atlantic cod (Gadus morhua L.). Int J Syst Evol Microbiol. 2007, 57: 1960-1965. 10.1099\/ijs.0.64765-0.","journal-title":"Int J Syst Evol Microbiol"},{"key":"816_CR5","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1111\/j.1365-2672.2008.04092.x","volume":"106","author":"KF Ottem","year":"2009","unstructured":"Ottem KF, Nylund A, Karlsbakk E, Friis-M\u00f8ller A, Kamaishi T: Elevation of Francisella philomiragia subsp. noatunensis Mikalsen et al. (2007) to Francisella noatunensis comb. nov. [syn. Francisella piscicida Ottem et al. (2008) syn. nov.] and characterization of Francisella noatunensis subsp. orientalis subsp. nov., two important fish pathogens. J Appl Microbiol. 2009, 106: 1231-1243. 10.1111\/j.1365-2672.2008.04092.x.","journal-title":"J Appl Microbiol"},{"key":"816_CR6","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1128\/MMBR.62.2.275-293.1998","volume":"62","author":"A van Belkum","year":"1998","unstructured":"van Belkum A, Scherer S, Van Alphen L, Verbrugh H: Short-sequence repeats in prokaryotic genomes. Microbiol Mol Biol Rev. 1998, 62: 275-293.","journal-title":"Microbiol Mol Biol Rev"},{"key":"816_CR7","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1016\/S1369-5274(99)80053-8","volume":"2","author":"A van Belkum","year":"1999","unstructured":"van Belkum A: The role of short sequence repeats in epidemiologic typing. Curr Opin Microbiol. 1999, 2: 306-311. 10.1016\/S1369-5274(99)80053-8.","journal-title":"Curr Opin Microbiol"},{"key":"816_CR8","doi-asserted-by":"publisher","first-page":"3186","DOI":"10.1128\/JCM.39.9.3186-3192.2001","volume":"39","author":"J Farlow","year":"2001","unstructured":"Farlow J, Smith KL, Wong J, Abrams M, Lytle M, Keim P: Francisella tularensis strain typing using multiple-locus, variable-number tandem repeat analysis. J Clin Microbiol. 2001, 39: 3186-3192. 10.1128\/JCM.39.9.3186-3192.2001.","journal-title":"J Clin Microbiol"},{"key":"816_CR9","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1046\/j.1365-2958.2001.02245.x","volume":"39","author":"D Metzgar","year":"2001","unstructured":"Metzgar D, Thomas E, Davis C, Field D, Wills C: The microsatellites of Escherichia coli: rapidly evolving repetitive DNAs in a non-pathogenic prokaryote. Mol Microbiol. 2001, 39: 183-190. 10.1046\/j.1365-2958.2001.02245.x.","journal-title":"Mol Microbiol"},{"issue":"1\u20132","key":"816_CR10","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.vetmic.2010.02.036","volume":"28","author":"AO Jenkins","year":"2010","unstructured":"Jenkins AO, Venter EH, Hutamo K, Godfroid J: Comparison of the capillary and agarose electrophoresis based multiple locus VNTR (variable number of tandem repeats) analysis (MLVA) on Mycobacterium bovis isolates. Vet Microbiol. 2010, 28 (1\u20132): 172-176.","journal-title":"Vet Microbiol"},{"key":"816_CR11","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/1746-6148-7-5","volume":"7","author":"\u00d8J Brevik","year":"2011","unstructured":"Brevik \u00d8J, Ottem KF, Nylund A: Multiple-locus, variable number of tandem repeat analysis (MLVA) of the fish-pathogen Francisella noatunensis. BMC Vet Res. 2011, 7: 5-10.1186\/1746-6148-7-5.","journal-title":"BMC Vet Res"},{"key":"816_CR12","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1186\/1471-2180-6-33","volume":"6","author":"F Lista","year":"2006","unstructured":"Lista F, Faggioni G, Valjevac S, Ciammaruconi A, Vaissaire J, le Doujet C, Gorg\u00e9 O, De Santis R, Carattoli A, Ciervo A, Fasanella A, Orsini F, D'Amelio R, Pourcel C, Cassone A, Vergnaud G: Genotyping of Bacillus anthracis strains based on automated capillary 25-loci multiple locus variable-number tandem repeats analysis. BMC Microbiol. 2006, 6: 33-10.1186\/1471-2180-6-33.","journal-title":"BMC Microbiol"},{"key":"816_CR13","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1128\/JCM.02136-06","volume":"45","author":"AC Pasqualotto","year":"2007","unstructured":"Pasqualotto AC, Denning DW, Anderson MJ: A cautionary tale: lack of consistency in allele sizes between two laboratories for a published multilocus microsatellite typing system. J Clin Microbiol. 2007, 45: 522-528. 10.1128\/JCM.02136-06.","journal-title":"J Clin Microbiol"},{"key":"816_CR14","doi-asserted-by":"publisher","first-page":"2928","DOI":"10.1128\/JB.182.10.2928-2936.2000","volume":"182","author":"P Keim","year":"2000","unstructured":"Keim P, Price LB, Klevytska AM, Smith KL, Schupp JM, Okinaka R, Jackson PJ, Hugh-Jones ME: Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J Bacteriol. 2000, 182: 2928-2936. 10.1128\/JB.182.10.2928-2936.2000.","journal-title":"J Bacteriol"},{"key":"816_CR15","doi-asserted-by":"crossref","first-page":"2233","DOI":"10.1128\/jcm.33.9.2233-2239.1995","volume":"33","author":"FC Tenover","year":"1995","unstructured":"Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B: Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995, 33: 2233-2239.","journal-title":"J Clin Microbiol"},{"key":"816_CR16","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1469-0691.2007.01786.x","volume":"3","author":"A van Belkum","year":"2007","unstructured":"van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M: Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol. 2007, 3: 1-46. Infect","journal-title":"Clin Microbiol"},{"key":"816_CR17","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1186\/1471-2164-13-268","volume":"13","author":"A Sjodin","year":"2012","unstructured":"Sjodin A, Svensson K, Ohrman C, Ahlinder J, Lindgren P, Duodu S, Johansson A, Colquhoun DJ, Larsson P, Forsman M: Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish. BMC Genomics. 2012, 13: 268-10.1186\/1471-2164-13-268.","journal-title":"BMC Genomics"},{"key":"816_CR18","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1093\/nar\/27.2.573","volume":"27","author":"G Benson","year":"1999","unstructured":"Benson G: Tandem repeats finder:a program to analyze DNA sequences. Nucleic Acids Res. 1999, 27: 573-580. 10.1093\/nar\/27.2.573.","journal-title":"Nucleic Acids Res"},{"key":"816_CR19","first-page":"365","volume-title":"Bioinformatics Methods and Protocols: Methods in Molecular Biology","author":"S Rozen","year":"2000","unstructured":"Rozen S, Skaletsky HJ: Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Edited by: Krawetz S, Misener S. 2000, Totowa, NJ: Humana Press, 365-386."},{"key":"816_CR20","first-page":"181","volume":"101","author":"A Abolmaaty","year":"2000","unstructured":"Abolmaaty A, Vu C, Oliver J, Levin RE: Development of a new lysis solution for releasing genomic DNA from bacterial cells for DNA amplification by polymerase chain reaction. Microbios. 2000, 101: 181-189.","journal-title":"Microbios"},{"key":"816_CR21","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1038\/163688a0","volume":"163","author":"EH Simpson","year":"1949","unstructured":"Simpson EH: Measurement of diversity. Nature. 1949, 163: 688-10.1038\/163688a0.","journal-title":"Nature"},{"key":"816_CR22","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1093\/bioinformatics\/16.9.847","volume":"16","author":"B Haubold","year":"2000","unstructured":"Haubold B, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000, 16: 847-848. 10.1093\/bioinformatics\/16.9.847.","journal-title":"Bioinformatics"}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1746-6148-9-252.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,2]],"date-time":"2021-09-02T02:39:21Z","timestamp":1630550361000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/1746-6148-9-252"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,12]]},"references-count":22,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2013,12]]}},"alternative-id":["816"],"URL":"https:\/\/doi.org\/10.1186\/1746-6148-9-252","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,12]]},"assertion":[{"value":"10 May 2013","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 December 2013","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 December 2013","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"252"}}