{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T13:58:35Z","timestamp":1787579915408,"version":"build-2736575974"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,11,21]],"date-time":"2025-11-21T00:00:00Z","timestamp":1763683200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2025,11,21]],"date-time":"2025-11-21T00:00:00Z","timestamp":1763683200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/501100004156","name":"Mahidol University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004156","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"DOI":"10.1186\/s12917-025-05133-9","type":"journal-article","created":{"date-parts":[[2025,11,21]],"date-time":"2025-11-21T15:20:20Z","timestamp":1763738420000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Hybridization, high genetic diversity, and molecular evidence of drug resistance to albendazole and levamisole in Haemonchus populations infecting goats in Thailand"],"prefix":"10.1186","volume":"21","author":[{"given":"Abigail Hui En","family":"Chan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Urusa","family":"Thaenkham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chanisara","family":"Kaenkaew","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wallop","family":"Pakdee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sivapong","family":"Sungpradit","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,11,21]]},"reference":[{"key":"5133_CR1","doi-asserted-by":"publisher","DOI":"10.3390\/ani11020363","volume":"11","author":"KV Arsenopoulos","year":"2021","unstructured":"Arsenopoulos KV, Fthenakis GC, Katsarou EI, Papadopoulos E. Haemonchosis: a challenging parasitic infection of sheep and goats. Animals. 2021;11:363.","journal-title":"Animals"},{"key":"5133_CR2","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/bs.apar.2016.02.024","volume":"93","author":"RB Besier","year":"2016","unstructured":"Besier RB, Kahn LP, Sargison ND, Van Wyk JA. Diagnosis, treatment and management of Haemonchus contortus in small ruminants. Adv Parasitol. 2016;93:181\u2013238.","journal-title":"Adv Parasitol"},{"key":"5133_CR3","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens13030238","volume":"13","author":"KV Arsenopoulos","year":"2024","unstructured":"Arsenopoulos KV, Minoudi S, Symeonidou I, Triantafyllidis A, Fthenakis GC, Papadopoulos E. Extensive countrywide molecular identification and high genetic diversity of Haemonchus spp. in domestic ruminants in Greece. Pathogens. 2024;13:238.","journal-title":"Pathogens"},{"key":"5133_CR4","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/bs.apar.2016.02.023","volume":"93","author":"DS Zarlenga","year":"2016","unstructured":"Zarlenga DS, Hoberg EP, Tuo W. The identification of Haemonchus species and diagnosis of haemonchosis. Adv Parasitol. 2016;93:145\u201380.","journal-title":"Adv Parasitol"},{"key":"5133_CR5","doi-asserted-by":"publisher","first-page":"1085","DOI":"10.1645\/GE-3309","volume":"90","author":"ER Hoberg","year":"2004","unstructured":"Hoberg ER, Lichtenfels JR, Gibbons L. Phylogeny for species of the genus Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora (Artiodactyla). J Parasitol. 2004;90:1085\u2013102.","journal-title":"J Parasitol"},{"key":"5133_CR6","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1017\/S0022149X18000743","volume":"93","author":"MC Santos","year":"2019","unstructured":"Santos MC, Amarante MRV, Amarante AFT. Establishment of co-infection and hybridization of Haemonchus contortus and Haemonchus placei in sheep. J Helminthol. 2019;93:697\u2013703.","journal-title":"J Helminthol"},{"key":"5133_CR7","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/0020-7519(80)90008-9","volume":"10","author":"LF Le Jambre","year":"1980","unstructured":"Le Jambre LF, Royal WM. Meiotic abnormalities in backcross lines of hybrid Haemonchus. Int J Parasitol. 1980;10:281\u20136.","journal-title":"Int J Parasitol"},{"key":"5133_CR8","doi-asserted-by":"crossref","unstructured":"Le Jambre LF. Hybridization of Australian Haemonchus placei (Place, 1893), Haemonchus contortus cayugensis (Das & Whitlock, 1960) and Haemonchus contortus (Rudolphi, 1803) from Louisiana. Int J Parasitol. 1981;11:323\u201330.","DOI":"10.1016\/0020-7519(81)90043-6"},{"key":"5133_CR9","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.ijpara.2014.09.002","volume":"45","author":"U Chaudhry","year":"2015","unstructured":"Chaudhry U, Redman EM, Abbas M, Muthusamy R, Ashraf K, Gilleard JS. Genetic evidence for hybridisation between Haemonchus contortus and Haemonchus placei in natural field populations and its implications for interspecies transmission of anthelmintic resistance. Int J Parasitol. 2015;45:149\u201359.","journal-title":"Int J Parasitol"},{"key":"5133_CR10","doi-asserted-by":"publisher","first-page":"691","DOI":"10.47665\/tb.37.3.691","volume":"37","author":"K Vongnady","year":"2020","unstructured":"Vongnady K, Rucksaken R, Mangkit B. Morphological identification of adult male Haemonchus species in goats from Thailand and Lao PDR. Trop Biomed. 2020;37:691\u2013712.","journal-title":"Trop Biomed"},{"key":"5133_CR11","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-12695-4","volume":"10","author":"G Sall\u00e9","year":"2019","unstructured":"Sall\u00e9 G, Doyle SR, Cortet J, Cabaret J, Berriman M, Holroyd N, et al. The global diversity of Haemonchus contortus is shaped by human intervention and climate. Nat Commun. 2019;10:4811.","journal-title":"Nat Commun"},{"key":"5133_CR12","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.ijpddr.2021.02.004","volume":"15","author":"MM George","year":"2021","unstructured":"George MM, Vatta AF, Howell SB, Storey BE, McCoy CJ, Wolstenholme AJ, et al. Evaluation of changes in drug susceptibility and population genetic structure in Haemonchus contortus following worm replacement as a means to reverse the impact of multiple-anthelmintic resistance on a sheep farm. Int J Parasitol Drugs Drug Resist. 2021;15:134\u201343.","journal-title":"Int J Parasitol Drugs Drug Resist"},{"key":"5133_CR13","doi-asserted-by":"publisher","DOI":"10.3390\/ani11102761","volume":"11","author":"AV Pot\u00e2rniche","year":"2021","unstructured":"Pot\u00e2rniche AV, Mickiewicz M, Olah D, Cerbu C, Sp\u00eenu M, Hari A, et al. First report of anthelmintic resistance in gastrointestinal nematodes in goats in Romania. Animals. 2021;11:2761.","journal-title":"Animals"},{"key":"5133_CR14","doi-asserted-by":"publisher","DOI":"10.1016\/j.parint.2020.102105","volume":"77","author":"AR Dey","year":"2020","unstructured":"Dey AR, Begum N, Anisuzzaman MA, Alam MZ. Multiple anthelmintic resistance in Gastrointestinal nematodes of small ruminants in Bangladesh. Parasitol Int. 2020;77:102105.","journal-title":"Parasitol Int"},{"key":"5133_CR15","doi-asserted-by":"publisher","DOI":"10.1186\/s12917-025-04700-4","volume":"21","author":"AHE Chan","year":"2025","unstructured":"Chan AHE, Kaenkaew C, Pakdee W, Sungpradit S, Thaenkham U. Emergence of dual drug-resistant strongylids in goats: first phenotypic and genotypic evidence from Ratchaburi Province, central Thailand. BMC Vet Res. 2025;21:245.","journal-title":"BMC Vet Res"},{"key":"5133_CR16","doi-asserted-by":"publisher","first-page":"764","DOI":"10.14202\/vetworld.2021.764-768","volume":"14","author":"O Pitaksakulrat","year":"2021","unstructured":"Pitaksakulrat O, Chaiyasaeng M, Artchayasawat A, Eamudomkarn C, Thongsahuan S, Boonmars T. The first molecular identification of benzimidazole resistance in Haemonchus contortus from goats in Thailand. Vet World. 2021;14:764\u20138.","journal-title":"Vet World"},{"key":"5133_CR17","doi-asserted-by":"publisher","first-page":"83","DOI":"10.14202\/vetworld.2022.83-90","volume":"15","author":"N Ratanapob","year":"2022","unstructured":"Ratanapob N, Thuamsuwan N, Thongyuan S. Anthelmintic resistance status of goat gastrointestinal nematodes in Sing Buri Province, Thailand. Vet World. 2022;15:83\u201390.","journal-title":"Vet World"},{"key":"5133_CR18","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1017\/S0031182007000066","volume":"134","author":"JS Gilleard","year":"2007","unstructured":"Gilleard JS, Beech RN. Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology. 2007;134:1133\u201347.","journal-title":"Parasitology"},{"key":"5133_CR19","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1011285","volume":"19","author":"AO Shaver","year":"2023","unstructured":"Shaver AO, Wit J, Dilks CM, Crombie TA, Li H, Aroian RV, et al. Variation in anthelmintic responses are driven by genetic differences among diverse C. elegans wild strains. PLoS Pathog. 2023;19:e1011285.","journal-title":"PLoS Pathog"},{"key":"5133_CR20","doi-asserted-by":"publisher","DOI":"10.1186\/s13071-016-1864-z","volume":"9","author":"F Yin","year":"2016","unstructured":"Yin F, Gasser RB, Li F, Bao M, Huang W, Zou F, et al. Population structure of Haemonchus contortus from seven geographical regions in China, determined on the basis of microsatellite markers. Parasit Vectors. 2016;9:586.","journal-title":"Parasit Vectors"},{"key":"5133_CR21","doi-asserted-by":"publisher","DOI":"10.1016\/j.meegid.2021.105021","volume":"95","author":"O Pitaksakulrat","year":"2021","unstructured":"Pitaksakulrat O, Chaiyasaeng M, Artchayasawat A, Eamudomkarn C, Boonmars T, Kopolrat KY, et al. Genetic diversity and population structure of Haemonchus contortus in goats from Thailand. Infect Genet Evol. 2021;95:105021.","journal-title":"Infect Genet Evol"},{"key":"5133_CR22","doi-asserted-by":"publisher","first-page":"104030","DOI":"10.1016\/j.sjbs.2024.104030","volume":"31","author":"S Parvin","year":"2024","unstructured":"Parvin S, Dey AR, Shohana NN, Anisuzzaman, Talukder MH, Alam MZ. Haemonchus contortus, an obligatory haematophagus worm infection in small ruminants: population genetics and genetic diversity. Saudi J Biol Sci. 2024;31:104030.","journal-title":"Saudi J Biol Sci"},{"key":"5133_CR23","unstructured":"Mangkit B, Thaenkham U, Adisakwattana P, Watthanakulpanich D, Jantasuriyarat C, Komalamisra C. Molecular characterization of Haemonchus contortus (Nematoda: Trichostrongylidae) from small ruminants in Thailand based on the second internal transcribed spacer of ribosomal DNA. ANRES. 2014;48(5):740-58."},{"key":"5133_CR24","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1016\/0020-7519(94)00156-I","volume":"25","author":"LA Stevenson","year":"1995","unstructured":"Stevenson LA, Chilton NB, Gasser RB. Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. Int J Parasitol. 1995;25:483\u20138.","journal-title":"Int J Parasitol"},{"key":"5133_CR25","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.vetpar.2014.10.026","volume":"206","author":"T Hussain","year":"2014","unstructured":"Hussain T, Periasamy K, Nadeem A, Babar M, Pichler R, Diallo A. Sympatric species distribution, genetic diversity and population structure of Haemonchus isolates from domestic ruminants in Pakistan. Vet Parasitol. 2014;206:188\u201399.","journal-title":"Vet Parasitol"},{"key":"5133_CR26","first-page":"95","volume":"41","author":"TA Hall","year":"1999","unstructured":"Hall TA, BioEdit. A user-friendly biological sequence alignment editor and analysis program for windows 95\/98\/NT. Nucl Acids Symp Ser. 1999;41:95\u20138.","journal-title":"Nucl Acids Symp Ser"},{"key":"5133_CR27","doi-asserted-by":"crossref","unstructured":"Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinf. 2002;Chap. 2:Unit 2.3.","DOI":"10.1002\/0471250953.bi0203s00"},{"key":"5133_CR28","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1093\/molbev\/msy096","volume":"35","author":"S Kumar","year":"2018","unstructured":"Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547\u20139.","journal-title":"Mol Biol Evol"},{"key":"5133_CR29","unstructured":"Rambaut A. FigTree v1.3.1. 2010. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http:\/\/tree.bio.ed.ac.uk\/software\/figtree\/."},{"key":"5133_CR30","doi-asserted-by":"publisher","first-page":"3299","DOI":"10.1093\/molbev\/msx248","volume":"34","author":"J Rozas","year":"2017","unstructured":"Rozas J, Ferrer-Mata A, S\u00e1nchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299\u2013302.","journal-title":"Mol Biol Evol"},{"key":"5133_CR31","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1111\/2041-210X.12410","volume":"6","author":"JW Leigh","year":"2015","unstructured":"Leigh JW, Bryant D, PopART. Full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110\u20136.","journal-title":"Methods Ecol Evol"},{"key":"5133_CR32","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1006\/expr.2000.4542","volume":"95","author":"A Silvestre","year":"2000","unstructured":"Silvestre A, Humbert JF. A molecular tool for species identification and benzimidazole resistance diagnosis in larval communities of small ruminant parasites. Exp Parasitol. 2000;95:271\u20136.","journal-title":"Exp Parasitol"},{"key":"5133_CR33","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.ijpddr.2023.02.002","volume":"21","author":"P Baltrusis","year":"2023","unstructured":"Baltrusis P, Halvarsson P, Charvet C, Hoglund J. The presence and relative frequency detection of the levamisole-resistance-associated S168T substitution in hco-acr-8 in Haemonchus contortus. Int J Parasitol Drugs Drug Resist. 2023;21:91\u20135.","journal-title":"Int J Parasitol Drugs Drug Resist"},{"key":"5133_CR34","first-page":"280","volume":"27","author":"FA Almeida","year":"2018","unstructured":"Almeida FA, Bassetto CC, Amarante MRV, Albuquerque ACA, Starling RZC, Amarante AFTD. Helminth infections and hybridization between Haemonchus contortus and Haemonchus placei in sheep from Santana do Livramento, Brazil. Rev Bras Parasitol Vet. 2018;27:280\u20138.","journal-title":"Rev Bras Parasitol Vet"},{"key":"5133_CR35","doi-asserted-by":"publisher","first-page":"3101","DOI":"10.1007\/s00436-023-08000-4","volume":"122","author":"MA Mannan","year":"2023","unstructured":"Mannan MA, Chowdhury S, Hossain MA, Kabir MHB. Genetic variability of Haemonchus contortus isolates in small ruminants from slaughterhouses in Bangladesh. Parasitol Res. 2023;122:3101\u20137.","journal-title":"Parasitol Res"},{"key":"5133_CR36","unstructured":"Department of Livestock Development. Annual Report 2016. Department of Livestock Development, Ministry of Agricultural and Cooperatives, Bangkok, Thailand.\u00a02017. https:\/\/planning.dld.go.th\/th\/images\/stories\/section-10\/Annual-2559.pdf."},{"key":"5133_CR37","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2020.109054","volume":"279","author":"MC Santos","year":"2020","unstructured":"Santos MC, Amarante M, Amarante A. Is there competition between Haemonchus contortus and Haemonchus placei in pasture grazed by only sheep. Vet Parasitol. 2020;279:109054.","journal-title":"Vet Parasitol"}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-025-05133-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12917-025-05133-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-025-05133-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,21]],"date-time":"2025-11-21T15:20:22Z","timestamp":1763738422000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/s12917-025-05133-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,21]]},"references-count":37,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["5133"],"URL":"https:\/\/doi.org\/10.1186\/s12917-025-05133-9","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,21]]},"assertion":[{"value":"24 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 October 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 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 Ethical Committee (Approved code: MUVS-2025-04-18) and the Institutional Biosafety Committee (Approval No. IBC\/MUVS-B-012\/2568) of the Faculty of Veterinary Science, Mahidol University. In this study, parasites were collected post-mortem from goats at two private, commercial slaughterhouses. Informed consent was obtained from the slaughterhouses. It is important to note that no animals were sacrificed specifically for this research. One slaughterhouse, located in Nakhon Pathom province, sourced its animals from Nakhon Pathom itself and the neighboring provinces of Ratchaburi, Kanchanaburi, Suphanburi, and Ang Thong. The other slaughterhouse involved in the study was in Satun province.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"679"}}