{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T13:04:36Z","timestamp":1787317476085,"version":"build-2736575974"},"reference-count":20,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,12,1]],"date-time":"2019-12-01T00:00:00Z","timestamp":1575158400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,12,3]],"date-time":"2019-12-03T00:00:00Z","timestamp":1575331200000},"content-version":"vor","delay-in-days":2,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program","doi-asserted-by":"crossref","award":["2016YFD0500702"],"award-info":[{"award-number":["2016YFD0500702"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Major Science and Technology Projects of Hubei Province","award":["66"],"award-info":[{"award-number":["66"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"published-print":{"date-parts":[[2019,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Haemophilus parasuis<\/jats:italic>\n                      is a commensal pathogen in the swine upper respiratory tract and causes Gl\u00e4sser\u2019s disease. Surveillance, screening for infection, and vaccination response of\n                      <jats:italic>H. parasuis<\/jats:italic>\n                      is hindered by the lack of a rapid antibody detection method.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      In the present study, a monomeric autotransporter was identified as a novel antigen for developing an indirect ELISA. The autotransporter passenger domain (Apd) was expressed, purified, and demonstrated to be specific in ELISA and western blotting. Mouse antiserum of recombinant Apd (rApd) recognized native Apd in the 15 serotype reference strains and five non-typeable isolate stains, but showed no reaction with seven other bacterial pathogens. The rApd ELISA was optimized and validated using 67 serum samples with known background, including 27 positive sera from experimentally infected and vaccinated pigs along with 40 negative sera that had been screened with\n                      <jats:italic>H. parasuis<\/jats:italic>\n                      whole cell ELISA from clinically healthy herds. The rApd ELISA provided positive and negative percent agreements of 96.4 and 94.9%, respectively, and an AUC value of 0.961, indicating that the assay produced accurate results.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>\n                      Apd was a universal antigen component among 15 serotype and non-typeable strains of\n                      <jats:italic>H. parasuis<\/jats:italic>\n                      and was also specific to this pathogen. The rApd ELISA could detect antibodies elicited by\n                      <jats:italic>H. parasuis<\/jats:italic>\n                      infection and vaccination, thereby exhibiting the potential to be applied for Gl\u00e4sser\u2019s disease diagnosis,\n                      <jats:italic>H. parasuis<\/jats:italic>\n                      vaccination evaluation, and large-scale serological surveillance.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12917-019-2128-x","type":"journal-article","created":{"date-parts":[[2019,12,3]],"date-time":"2019-12-03T10:03:27Z","timestamp":1575367407000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Development and application of an antibody detection ELISA for Haemophilus parasuis based on a monomeric autotransporter passenger domain"],"prefix":"10.1186","volume":"15","author":[{"given":"Yunbao","family":"Liu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yujiao","family":"Du","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuping","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Qi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinxue","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qigai","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangru","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huanchun","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuwang","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaojuan","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,12,3]]},"reference":[{"key":"2128_CR1","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1177\/104063879500700409","volume":"7","author":"L John","year":"1995","unstructured":"John L, Vahle JSH, Andrews JJ. Experimental reproduction of Haemophilus parasuis infection in swine: clinical bacteriologic and morphologic findings. J Vet Diag Invest. 1995;7:476\u201380.","journal-title":"J Vet Diag Invest"},{"issue":"1","key":"2128_CR2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.vetmic.2003.12.001","volume":"99","author":"S Oliveira","year":"2004","unstructured":"Oliveira S, Pijoan C. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet Microbiol. 2004;99(1):1\u201312.","journal-title":"Vet Microbiol"},{"issue":"3","key":"2128_CR3","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1016\/j.tvjl.2006.10.017","volume":"174","author":"A Olvera","year":"2007","unstructured":"Olvera A, Segales J, Aragon V. Update on the diagnosis of Haemophilus parasuis infection in pigs and novel genotyping methods. Vet J. 2007;174(3):522\u20139.","journal-title":"Vet J"},{"issue":"1","key":"2128_CR4","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1177\/1040638713510163","volume":"26","author":"L Galina Pantoja","year":"2014","unstructured":"Galina Pantoja L, Stammen B, Minton B, Amodie D. Serologic profiling of Haemophilus parasuis-vaccinated sows and their litters using a novel oligopeptide permease a enzyme-linked immunosorbent assay reveals unexpected patterns of serological response and maternal antibody transfer. J Vet Diag Invest. 2014;26(1):125\u201330.","journal-title":"J Vet Diag Invest."},{"key":"2128_CR5","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.rvsc.2016.05.006","volume":"107","author":"N Macedo","year":"2016","unstructured":"Macedo N, Oliveira S, Torremorell M, Rovira A. Immune response to oligopeptide permease a (OppA) protein in pigs naturally and experimentally infected with Haemophilus parasuis. Res Vet Sci. 2016;107:62\u20137.","journal-title":"Res Vet Sci"},{"key":"2128_CR6","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.vetmic.2017.03.035","volume":"204","author":"J Li","year":"2017","unstructured":"Li J, Wang S, Li C, Wang C, Liu Y, Wang G, et al. Secondary Haemophilus parasuis infection enhances highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) infection-mediated inflammatory responses. Vet Microbiol. 2017;204:35\u201342.","journal-title":"Vet Microbiol"},{"key":"2128_CR7","first-page":"33","volume":"55","author":"P Miniats","year":"1991","unstructured":"Miniats P, Smart NL, Ewert E. Vaccination of gnotobiotic primary specific pathogen-free pigs against Haemophilus parasuis. Can J Vet Res. 1991;55:33\u20136.","journal-title":"Can J Vet Res"},{"key":"2128_CR8","first-page":"37","volume":"55","author":"P Miniats","year":"1991","unstructured":"Miniats P, Smart NL, Rosendal S. Cross protection among Haemophilus parasuis strains in immunized gnotobiotic pigs. Can J Vet Res. 1991;55:37\u201341.","journal-title":"Can J Vet Res"},{"key":"2128_CR9","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1292\/jvms.63.487","volume":"63","author":"K Takahashi","year":"2001","unstructured":"Takahashi K, Nagai S, Yagihashi T, Ikehata T, Nakano Y, Senna K, Maruyama T, Murofushi J. A cross-protection experiment in pigs vaccinated with Haemophilus parasuis serovars 2 and 5 bacterins, and evaluation of a bivalent vaccine under laboratory and field conditions. J Vet Med Sci. 2001;63:487.","journal-title":"J Vet Med Sci"},{"key":"2128_CR10","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.actatropica.2015.04.009","volume":"148","author":"S Chen","year":"2015","unstructured":"Chen S, Chu Y, Zhao P, He Y, Jian Y, Liu Y, et al. Development of a recombinant OppA-based indirect hemagglutination test for the detection of antibodies against Haemophilus parasuis. Acta Trop. 2015;148:8\u201312.","journal-title":"Acta Trop"},{"issue":"8","key":"2128_CR11","doi-asserted-by":"publisher","first-page":"3861","DOI":"10.1128\/JB.169.8.3861-3865.1987","volume":"169","author":"EW Goodell","year":"1987","unstructured":"Goodell EW, Higgins CF. Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. J Bacteriol. 1987;169(8):3861\u20135.","journal-title":"J Bacteriol"},{"issue":"6","key":"2128_CR12","doi-asserted-by":"publisher","first-page":"3687","DOI":"10.1128\/IAI.01837-05","volume":"74","author":"M Tanabe","year":"2006","unstructured":"Tanabe M, Atkins HS, Harland DN, Elvin SJ, Stagg AJ, Mirza O, et al. The ABC transporter protein OppA provides protection against experimental Yersinia pestis infection. Infect Immun. 2006;74(6):3687\u201391.","journal-title":"Infect Immun"},{"issue":"2","key":"2128_CR13","doi-asserted-by":"publisher","first-page":"846","DOI":"10.1128\/IAI.00314-10","volume":"79","author":"M Yang","year":"2011","unstructured":"Yang M, Johnson A, Murphy TF. Characterization and evaluation of the Moraxella catarrhalis oligopeptide permease a as a mucosal vaccine antigen. Infect Immun. 2011;79(2):846\u201357.","journal-title":"Infect Immun"},{"issue":"1","key":"2128_CR14","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/S0378-1135(03)00208-6","volume":"96","author":"J Gr\u00f8ndahl-Hansen","year":"2003","unstructured":"Gr\u00f8ndahl-Hansen J, Barfod K, Klausen J, Andresen LO, Heegaard PMH, S\u00f8rensen V. Development and evaluation of a mixed long-chain lipopolysaccharide based ELISA for serological surveillance of infection with Actinobacillus pleuropneumoniae serotypes 2, 6 and 12 in pig herds. Vet Microbiol. 2003;96(1):41\u201351.","journal-title":"Vet Microbiol"},{"issue":"Pt 2","key":"2128_CR15","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1099\/mic.0.052399-0","volume":"158","author":"S Pina-Pedrero","year":"2012","unstructured":"Pina-Pedrero S, Olvera A, Perez-Simo M, Bensaid A. Genomic and antigenic characterization of monomeric autotransporters of Haemophilus parasuis: an ongoing process of reductive evolution. Microbiology. 2012;158(Pt 2):436\u201347.","journal-title":"Microbiology"},{"key":"2128_CR16","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1093\/clinchem\/39.4.561","volume":"39","author":"MH Zweig","year":"1993","unstructured":"Zweig MH, Campbell G. Receiver-operating characteristic (ROC) plots. A fundamental evaluation tool in clinical medicine. Clin Chem. 1993;39:561\u201377.","journal-title":"Clin Chem"},{"issue":"7","key":"2128_CR17","doi-asserted-by":"publisher","first-page":"2601","DOI":"10.1128\/JCM.40.7.2601-2605.2002","volume":"40","author":"G Gorkiewicz","year":"2002","unstructured":"Gorkiewicz G, Feierl G, Zechner R, Zechner EL. Transmission of Campylobacter hyointestinalis from a pig to a human. J Clin Microbiol. 2002;40(7):2601\u20135.","journal-title":"J Clin Microbiol"},{"issue":"1","key":"2128_CR18","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1292\/jvms.65.129","volume":"65","author":"Y Sasaki","year":"2002","unstructured":"Sasaki Y, Fujisawa T, Ogikubo K, Ohzono T, Ishihara K, Takahashi T. Characterization of Campylobacter lanienae from pig feces. J Vet Med Sci. 2002;65(1):129\u201331.","journal-title":"J Vet Med Sci"},{"issue":"10","key":"2128_CR19","doi-asserted-by":"publisher","first-page":"3046","DOI":"10.1128\/JCM.01004-17","volume":"55","author":"GL Bradshaw","year":"2017","unstructured":"Bradshaw GL, Thueson RK, Uriona TJ. Improved serodiagnostic performance for Lyme disease by use of two recombinant proteins in enzyme-linked immunosorbent assay compared to standardized two-tier testing. J Clin Microbiol. 2017;55(10):3046\u201356.","journal-title":"J Clin Microbiol"},{"issue":"3","key":"2128_CR20","doi-asserted-by":"publisher","first-page":"766","DOI":"10.1128\/JCM.02875-13","volume":"52","author":"K Caban-Hernandez","year":"2014","unstructured":"Caban-Hernandez K, Gaudier JF, Ruiz-Jimenez C, Espino AM. Development of two antibody detection enzyme-linked immunosorbent assays for serodiagnosis of human chronic fascioliasis. J Clin Microbiol. 2014;52(3):766\u201372.","journal-title":"J Clin Microbiol"}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-019-2128-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12917-019-2128-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-019-2128-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,1]],"date-time":"2020-12-01T19:34:45Z","timestamp":1606851285000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/s12917-019-2128-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12]]},"references-count":20,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["2128"],"URL":"https:\/\/doi.org\/10.1186\/s12917-019-2128-x","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12]]},"assertion":[{"value":"9 April 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 October 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 December 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Experimental protocols for pigs and mice were approved by the Scientific Ethic Committee of Huazhong Agricultural University (No. HZAUSW-2017-009 and No. HZAUMO-2018-028).","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"436"}}