{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T18:43:01Z","timestamp":1783104181958,"version":"3.54.6"},"reference-count":55,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2013,8,12]],"date-time":"2013-08-12T00:00:00Z","timestamp":1376265600000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0070212","type":"journal-article","created":{"date-parts":[[2013,8,12]],"date-time":"2013-08-12T21:07:41Z","timestamp":1376341661000},"page":"e70212","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":69,"title":["Phylogenetic Characterization of \u03b2-Tubulins and Development of Pyrosequencing Assays for Benzimidazole Resistance in Cattle Nematodes"],"prefix":"10.1371","volume":"8","author":[{"given":"Janina","family":"Demeler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nina","family":"Kr\u00fcger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00fcrgen","family":"Kr\u00fccken","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vera C.","family":"von der Heyden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabrina","family":"Ram\u00fcnke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ursula","family":"K\u00fcttler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra","family":"Miltsch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"L\u00f3pez Cepeda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Malcolm","family":"Knox","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jozef","family":"Vercruysse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Geldhof","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Achim","family":"Harder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"von Samson-Himmelstjerna","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2013,8,12]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1016\/0020-7519(88)90175-0","article-title":"The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles","volume":"18","author":"E Lacey","year":"1988","journal-title":"Int J Parasitol"},{"key":"ref2","first-page":"844","article-title":"Variance in the Effectiveness of Thiabendazole against <italic>Haemonchus contortus<\/italic> in Sheep","volume":"25","author":"DP Conway","year":"1964","journal-title":"Am J Vet Res"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.pt.2004.08.001","article-title":"Drug resistance in nematodes of veterinary importance: a status report","volume":"20","author":"RM Kaplan","year":"2004","journal-title":"Trends Parasitol"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1080\/00480169.2006.36711","article-title":"Prevalence of anthelmintic resistance on 62 beef cattle farms in the North Island of New Zealand","volume":"54","author":"TS Waghorn","year":"2006","journal-title":"N Z Vet J"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.vetpar.2009.08.018","article-title":"The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US","volume":"166","author":"LC Gasbarre","year":"2009","journal-title":"Vet Parasitol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/0020-7519(90)90199-W","article-title":"Anthelmintic resistance in nematodes: extent, recent understanding and future directions for control and research","volume":"20","author":"RK Prichard","year":"1990","journal-title":"Int J Parasitol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.pt.2004.07.010","article-title":"Drug resistance in veterinary helminths","volume":"20","author":"AJ Wolstenholme","year":"2004","journal-title":"Trends Parasitol"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"2993","DOI":"10.1083\/jcb.109.6.2993","article-title":"Genetic and molecular analysis of a <italic>Caenorhabditis elegans<\/italic> \u03b2-tubulin that conveys benzimidazole sensitivity","volume":"109","author":"M Driscoll","year":"1989","journal-title":"J Cell Biol"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/0166-6851(94)90066-3","article-title":"Benzimidazole resistance in <italic>Haemonchus contortus<\/italic> is correlated with a conserved mutation at amino acid 200 in \u03b2-tubulin isotype 1","volume":"63","author":"MS Kwa","year":"1994","journal-title":"Mol Biochem Parasitol"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1002\/cm.970170204","article-title":"Identification of an amino acid substitution in the benA, \u03b2-tubulin gene of <italic>Aspergillus nidulans<\/italic> that confers thiabendazole resistance and benomyl supersensitivity","volume":"17","author":"MK Jung","year":"1990","journal-title":"Cell Motil Cytoskeleton"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S0166-6851(01)00455-8","article-title":"Mutation in position 167 of isotype 1 \u03b2-tubulin gene of <italic>Trichostrongylid<\/italic> nematodes: role in benzimidazole resistance?","volume":"120","author":"A Silvestre","year":"2002","journal-title":"Mol Biochem Parasitol"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1645\/GE3305RN","article-title":"Beta-tubulin complementary DNA sequence variations observed between cyathostomins from benzimidazole-susceptible and -resistant populations","volume":"90","author":"M Drogemuller","year":"2004","journal-title":"J Parasitol"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"234","DOI":"10.4269\/ajtmh.2005.73.234","article-title":"Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment","volume":"73","author":"AE Schwab","year":"2005","journal-title":"Am J Trop Med Hyg"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.exppara.2005.10.003","article-title":"The \u03b2-tubulin genes of two <italic>Strongyloides<\/italic> species","volume":"112","author":"LA Melville","year":"2006","journal-title":"Exp Parasitol"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.vetpar.2006.10.003","article-title":"Phenotyping and genotyping of <italic>Haemonchus contortus<\/italic> isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes","volume":"144","author":"M Ghisi","year":"2007","journal-title":"Vet Parasitol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1016\/j.ijpara.2008.02.001","article-title":"The role of polymorphisms at \u03b2 tubulin isotype 1 codons 167 and 200 in benzimidazole resistance in cyathostomins","volume":"38","author":"JE Hodgkinson","year":"2008","journal-title":"Int J Parasitol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1097\/FPC.0b013e3282f4711d","article-title":"Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on <italic>Haemonchus contortus<\/italic>","volume":"18","author":"M de Lourdes Mottier","year":"2008","journal-title":"Pharmacogenet Genomics"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"e397","DOI":"10.1371\/journal.pntd.0000397","article-title":"Assays to detect \u03b2-tubulin codon 200 polymorphism in <italic>Trichuris trichiura<\/italic> and <italic>Ascaris lumbricoides<\/italic>","volume":"3","author":"A Diawara","year":"2009","journal-title":"PLoS Negl Trop Dis"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.pt.2010.11.008","article-title":"Anthelmintic resistance in nematode parasites of cattle: a global issue?","volume":"27","author":"IA Sutherland","year":"2011","journal-title":"Trends Parasitol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1111\/j.1751-0813.1989.tb13578.x","article-title":"Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays","volume":"66","author":"PJ Martin","year":"1989","journal-title":"Aust Vet J"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.vetpar.2005.11.019","article-title":"The detection of anthelmintic resistance in nematodes of veterinary importance","volume":"136","author":"GC Coles","year":"2006","journal-title":"Vet Parasitol"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1007\/s00436-009-1466-1","article-title":"Standardization of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes","volume":"105","author":"G von Samson-Himmelstjerna","year":"2009","journal-title":"Parasitol Res"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1006\/expr.2000.4542","article-title":"A molecular tool for species identification and benzimidazole resistance diagnosis in larval communities of small ruminant parasites","volume":"95","author":"A Silvestre","year":"2000","journal-title":"Exp Parasitol"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1017\/S0031182003004086","article-title":"Cloning two full-length beta-tubulin isotype cDNAs from Cooperia oncophora, and screening for benzimidazole resistance-associated mutations in two isolates","volume":"127","author":"AI Njue","year":"2003","journal-title":"Parasitology"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.vetpar.2003.09.001","article-title":"Benzimidazole-resistant \u03b2-tubulin alleles in a population of parasitic nematodes (<italic>Cooperia oncophora<\/italic>) of cattle","volume":"117","author":"CA Winterrowd","year":"2003","journal-title":"Vet Parasitol"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1017\/S0031182003003974","article-title":"TaqMan minor groove binder real-time PCR analysis of \u03b2-tubulin codon 200 polymorphism in small strongyles (Cyathostomin) indicates that the TAC allele is only moderately selected in benzimidazole-resistant populations","volume":"127","author":"G von Samson-Himmelstjerna","year":"2003","journal-title":"Parasitology"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.vetpar.2005.02.004","article-title":"Real time PCR for the diagnosis of benzimidazole resistance in trichostrongylids of sheep","volume":"129","author":"MA Alvarez-Sanchez","year":"2005","journal-title":"Vet Parasitol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/j.vetpar.2006.10.014","article-title":"Detection and measurement of benzimidazole resistance alleles in <italic>Haemonchus contortus<\/italic> using real-time PCR with locked nucleic acid Taqman probes","volume":"144","author":"TK Walsh","year":"2007","journal-title":"Vet Parasitol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.vetpar.2008.12.001","article-title":"Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the \u03b2-tubulin gene","volume":"161","author":"J Hoglund","year":"2009","journal-title":"Vet Parasitol"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1017\/S003118200800543X","article-title":"Molecular detection of benzimidazole resistance in Haemonchus contortus using real-time PCR and pyrosequencing","volume":"136","author":"G von Samson-Himmelstjerna","year":"2009","journal-title":"Parasitology"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1111\/j.1751-0813.2010.00648.x","article-title":"Anthelmintic resistance in cattle nematodes on 13 south-west Victorian properties","volume":"88","author":"DK Rendell","year":"2010","journal-title":"Aust Vet J"},{"key":"ref32","unstructured":"Cabaret J, Antoine T (2008) INRA website. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/wcentre.tours.inra.fr\/sfpar\/stat.htm\" xlink:type=\"simple\">http:\/\/wcentre.tours.inra.fr\/sfpar\/stat.htm<\/ext-link>. Accessed 2012 July 9."},{"key":"ref33","first-page":"1941","article-title":"Characterisation of the beta-tubulin gene of <italic>Cylicocyclus nassatus<\/italic>?","volume":"29","author":"M Pape","year":"1999","journal-title":"Int J Parasitol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1093\/molbev\/msn083","article-title":"jModelTest: phylogenetic model averaging","volume":"25","author":"D Posada","year":"2008","journal-title":"Mol Biol Evol"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1080\/10635150390235520","article-title":"A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood","volume":"52","author":"S Guindon","year":"2003","journal-title":"Syst Biol"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods","volume":"28","author":"K Tamura","year":"2011","journal-title":"Mol Biol Evol"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.vetpar.2010.01.032","article-title":"Adaptation and evaluation of three different in vitro tests for the detection of resistance to anthelmintics in gastro intestinal nematodes of cattle","volume":"170","author":"J Demeler","year":"2010","journal-title":"Vet Parasitol"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1136\/vr.149.2.58","article-title":"Avermectin resistance in <italic>Cooperia pectinata<\/italic> in cattle in Argentina","volume":"149","author":"OS Anziani","year":"2001","journal-title":"Vet Rec"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1080\/00480169.2003.36353","article-title":"Probable multigeneric resistance to macrocyclic lactone anthelmintics in cattle in New Zealand","volume":"51","author":"B Loveridge","year":"2003","journal-title":"N Z Vet J"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1051\/vetres:2003018","article-title":"Multispecies and multiple anthelmintic resistance on cattle nematodes in a farm in Argentina: the beginning of high resistance?","volume":"34","author":"ME Mejia","year":"2003","journal-title":"Vet Res"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.vetpar.2004.05.018","article-title":"Resistance to benzimidazole and macrocyclic lactone anthelmintics in cattle nematodes in Argentina","volume":"122","author":"OS Anziani","year":"2004","journal-title":"Vet Parasitol"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.vetpar.2007.06.023","article-title":"Anthelmintic resistance in cattle nematodes in northwestern Sao Paulo State, Brazil","volume":"148","author":"RG Soutello","year":"2007","journal-title":"Vet Parasitol"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.vetpar.2008.10.030","article-title":"Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe","volume":"160","author":"J Demeler","year":"2009","journal-title":"Vet Parasitol"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.vetpar.2009.01.031","article-title":"Moxidectin-resistant nematodes in cattle in Brazil","volume":"161","author":"GK Condi","year":"2009","journal-title":"Vet Parasitol"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1051\/vetres:2002034","article-title":"Cattle nematodes resistant to anthelmintics: why so few cases?","volume":"33","author":"GC Coles","year":"2002","journal-title":"Vet Res"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"e91","DOI":"10.1093\/nar\/gkm435","article-title":"DNA bar coding and pyrosequencing to identify rare HIV drug resistance mutations","volume":"35","author":"C Hoffmann","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s10096-007-0261-0","article-title":"Use of pyrosequencing to identify point mutations in domain V of 23S rRNA genes of linezolid-resistant <italic>Staphylococcus aureus<\/italic> and <italic>Staphylococcus epidermidis<\/italic>","volume":"26","author":"W Zhu","year":"2007","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"3900","DOI":"10.1128\/JCM.01209-06","article-title":"Pyrosequencing, a high-throughput method for detecting single nucleotide polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes of <italic>Plasmodium falciparum<\/italic>","volume":"44","author":"Z Zhou","year":"2006","journal-title":"J Clin Microbiol"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.pt.2010.04.003","article-title":"Nematode parasite genes: what&apos;s in a name?","volume":"26","author":"RN Beech","year":"2010","journal-title":"Trends Parasitol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1006\/bbrc.1993.1233","article-title":"Effect of selection for benzimidazole resistance in <italic>Haemonchus contortus<\/italic> on \u03b2-tubulin isotype 1 and isotype 2 genes","volume":"191","author":"MS Kwa","year":"1993","journal-title":"Biochem Biophys Res Commun"},{"key":"ref51","article-title":"Characterization and comparative analysis of the complete <italic>Haemonchus contortus<\/italic> \u03b2-tubulin gene family and implications for benzimidazole resistance in strongylid nematodes","author":"GI Saunders","year":"2013","journal-title":"Int J Parasitol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.vetpar.2011.11.068","article-title":"Relationship between increased albendazole systemic exposure and changes in single nucleotide polymorphisms on the \u03b2-tubulin isotype 1 encoding gene in <italic>Haemonchus contortus<\/italic>","volume":"186","author":"V Barrere","year":"2012","journal-title":"Vet Parasitol"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1007\/s00436-011-2426-0","article-title":"beta-Tubulin genotypes in six species of cyathostomins from anthelmintic-naive Przewalski and benzimidazole-resistant brood horses in Ukraine","volume":"109","author":"WJ Blackhall","year":"2011","journal-title":"Parasitol Res"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1007\/s004360000326","article-title":"Novel small strongyle (Cyathostominae) beta-tubulin sequences","volume":"87","author":"G von Samson-Himmelstjerna","year":"2001","journal-title":"Parasitol Res"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1645\/0022-3395(2002)088[0254:ASPFTB]2.0.CO;2","article-title":"Allele-specific PCR for the beta-tubulin codon 200 TTC\/TAC polymorphism using single adult and larval small strongyle (Cyathostominae) stages","volume":"88","author":"G von Samson-Himmelstjerna","year":"2002","journal-title":"J Parasitol"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0070212","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,7,20]],"date-time":"2019-07-20T21:31:39Z","timestamp":1563658299000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0070212"}},"subtitle":[],"editor":[{"given":"Bernhard","family":"Kaltenboeck","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2013,8,12]]},"references-count":55,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2013,8,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0070212","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,8,12]]}}}