{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,18]],"date-time":"2026-04-18T03:21:45Z","timestamp":1776482505535,"version":"3.51.2"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,1,5]],"date-time":"2019-01-05T00:00:00Z","timestamp":1546646400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Med Res Methodol"],"published-print":{"date-parts":[[2019,12]]},"DOI":"10.1186\/s12874-018-0650-3","type":"journal-article","created":{"date-parts":[[2019,1,5]],"date-time":"2019-01-05T11:59:13Z","timestamp":1546689553000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["Use of saliva to monitor meningococcal vaccine responses: proposing a threshold in saliva as surrogate of protection"],"prefix":"10.1186","volume":"19","author":[{"given":"Mari\u00ebtte B.","family":"van Ravenhorst","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fiona R. M.","family":"van der Klis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Debbie M.","family":"van Rooijen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elisabeth A. M.","family":"Sanders","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guy A. M.","family":"Berbers","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2019,1,5]]},"reference":[{"key":"650_CR1","doi-asserted-by":"crossref","unstructured":"Andrews N, Borrow R, Miller E. Validation of serological correlate of protection for meningococcal C conjugate vaccine by using efficacy estimates from postlicensure surveillance in England. Clin Diagn Lab Immunol. 2003;10(5):780-6.","DOI":"10.1128\/CDLI.10.5.780-786.2003"},{"issue":"8","key":"650_CR2","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.4161\/hv.20473","volume":"8","author":"KS Erlich","year":"2012","unstructured":"Erlich KS, Congeni BL. Importance of circulating antibodies in protection against meningococcal disease. Human vaccines & immunotherapeutics. 2012;8(8):1029\u201335.","journal-title":"Human vaccines & immunotherapeutics"},{"issue":"6","key":"650_CR3","doi-asserted-by":"publisher","first-page":"1569","DOI":"10.1086\/314753","volume":"179","author":"P Richmond","year":"1999","unstructured":"Richmond P, Borrow R, Miller E, Clark S, Sadler F, Fox A, Begg N, Morris R, Cartwright K. Meningococcal serogroup C conjugate vaccine is immunogenic in infancy and primes for memory. J Infect Dis. 1999;179(6):1569\u201372.","journal-title":"J Infect Dis"},{"issue":"Suppl 2","key":"650_CR4","doi-asserted-by":"publisher","first-page":"B117","DOI":"10.1016\/j.vaccine.2009.04.066","volume":"27","author":"DM Granoff","year":"2009","unstructured":"Granoff DM. Relative importance of complement-mediated bactericidal and opsonic activity for protection against meningococcal disease. Vaccine. 2009;27(Suppl 2):B117\u201325.","journal-title":"Vaccine"},{"key":"650_CR5","doi-asserted-by":"crossref","unstructured":"Miller E, Salisbury D, Ramsay M. Planning, registration, and implementation of an immunisation campaign against meningococcal serogroup C disease in the UK: a success story. Vaccine. 2001.","DOI":"10.1016\/S0264-410X(01)00299-7"},{"issue":"6","key":"650_CR6","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1084\/jem.129.6.1327","volume":"129","author":"I Goldschneider","year":"1969","unstructured":"Goldschneider I, Gotschlich EC, Artenstein MS. Human immunity to the meningococcus. II Development of natural immunity. The Journal of experimental medicine. 1969;129(6):1327\u201348.","journal-title":"The Journal of experimental medicine"},{"issue":"2","key":"650_CR7","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1128\/CDLI.4.2.156-167.1997","volume":"4","author":"SE Maslanka","year":"1997","unstructured":"Maslanka SE, Gheesling LL, Libutti DE, Donaldson KB, Harakeh HS, Dykes JK, Arhin FF, Devi SJ, Frasch CE, Huang JC, et al. Standardization and a multilaboratory comparison of Neisseria meningitidis serogroup a and C serum bactericidal assays. The Multilaboratory Study Group. Clinical and diagnostic laboratory immunology. 1997;4(2):156\u201367.","journal-title":"Clinical and diagnostic laboratory immunology"},{"issue":"3","key":"650_CR8","doi-asserted-by":"publisher","first-page":"1568","DOI":"10.1128\/IAI.69.3.1568-1573.2001","volume":"69","author":"R Borrow","year":"2001","unstructured":"Borrow R, Andrews N, Goldblatt D, Miller E. Serological basis for use of meningococcal serogroup C conjugate vaccines in the United Kingdom: reevaluation of correlates of protection. Infect Immun. 2001;69(3):1568\u201373.","journal-title":"Infect Immun"},{"issue":"9","key":"650_CR9","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1016\/S1473-3099(14)70806-0","volume":"14","author":"MW Bijlsma","year":"2014","unstructured":"Bijlsma MW, Bekker V, Brouwer MC, Spanjaard L, van de Beek d, van der Ende A. Epidemiology of invasive meningococcal disease in the Netherlands, 1960-2012: an analysis of national surveillance data. Lancet Infect Dis. 2014;14(9):805\u20131012.","journal-title":"Lancet Infect Dis"},{"issue":"1","key":"650_CR10","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1097\/01.inf.0000195594.41449.c6","volume":"25","author":"SC Greeff de","year":"2006","unstructured":"de Greeff SC, de Melker HE, Spanjaard L, Schouls LM, van Derende A. Protection from routine vaccination at the age of 14 montis with meningococcal serogroup C conjugate vaccine in the Netherlands. Pediatr Infect Dis J. 2006;25(1):79\u201380.","journal-title":"Pediatr Infect Dis J"},{"key":"650_CR11","doi-asserted-by":"crossref","unstructured":"Knol MJ, Ruijs WL, Antonise-Kamp L, de Melker HE, van der Ende A. Implementation of MenACWY vaccination because of ongoing increase in serogroup W invasive meningococcal disease, the Netherlands, 2018. Euro Surveillance. 2018;23(16).","DOI":"10.2807\/1560-7917.ES.2018.23.16.18-00158"},{"issue":"32","key":"650_CR12","doi-asserted-by":"publisher","first-page":"3933","DOI":"10.1016\/j.vaccine.2015.06.055","volume":"33","author":"SP Stoof","year":"2015","unstructured":"Stoof SP, van der Klis FR, van Rooijen DM, Bogaert D, Trzcinski K, Sanders EA, Berbers GA. Salivary antibody levels in adolescents in response to a meningococcal serogroup C conjugate booster vaccination nine years after priming: systemically induced local immunity and saliva as potential surveillance tool. Vaccine. 2015;33(32):3933\u20139.","journal-title":"Vaccine"},{"issue":"5","key":"650_CR13","doi-asserted-by":"publisher","first-page":"2692","DOI":"10.1128\/IAI.68.5.2692-2697.2000","volume":"68","author":"Q Zhang","year":"2000","unstructured":"Zhang Q, Choo S, Everard J, Jennings R, Finn A. Mucosal immune responses to meningococcal group C conjugate and group a and C polysaccharide vaccines in adolescents. Infect Immun. 2000;68(5):2692\u20137.","journal-title":"Infect Immun"},{"issue":"2","key":"650_CR14","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1111\/sji.12451","volume":"84","author":"GK Barnes","year":"2016","unstructured":"Barnes GK, Workalemahu B, Kristiansen PA, Beyene D, Merdekios B, Fissiha P, Aseffa A, Caugant DA, Naess LM. Salivary and serum antibody response against Neisseria meningitidis after vaccination with conjugate polysaccharide vaccines in Ethiopian volunteers. Scand J Immunol. 2016;84(2):118\u201329.","journal-title":"Scand J Immunol"},{"issue":"36","key":"650_CR15","doi-asserted-by":"publisher","first-page":"4745","DOI":"10.1016\/j.vaccine.2017.06.053","volume":"35","author":"MB Ravenhorst van","year":"2017","unstructured":"van Ravenhorst MB, van der Klis FRM, van Rooijen DM, Knol MJ, Stoof SP, Sanders EAM, Berbers GAM. Meningococcal serogroup C immunogenicity, antibody persistence and memory B-cells induced by the monovalent meningococcal serogroup C versus quadrivalent meningococcal serogroup ACWY conjugate booster vaccine: a randomized controlled trial. Vaccine. 2017;35(36):4745\u201352.","journal-title":"Vaccine"},{"issue":"8","key":"650_CR16","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1128\/CVI.00478-07","volume":"15","author":"RM Voer de","year":"2008","unstructured":"de Voer RM, van der Klis FR, Engels CW, Rijkers GT, Sanders EA, Berbers GA. Development of a fluorescent-bead-based multiplex immunoassay to determine immunoglobulin G subclass responses to Neisseria meningitidis serogroup a and C polysaccharides. Clinical and vaccine immunology : CVI. 2008;15(8):1188\u201393.","journal-title":"Clinical and vaccine immunology : CVI"},{"issue":"2","key":"650_CR17","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1128\/CDLI.11.2.272-279.2004","volume":"11","author":"G Lal","year":"2004","unstructured":"Lal G, Balmer P, Joseph H, Dawson M, Borrow R. Development and evaluation of a tetraplex flow cytometric assay for quantitation of serum antibodies to Neisseria meningitidis serogroups a, C, Y, and W-135. Clin Diagn Lab Immunol. 2004;11(2):272\u20139.","journal-title":"Clin Diagn Lab Immunol"},{"key":"650_CR18","doi-asserted-by":"crossref","unstructured":"van Ravenhorst MB, van der Klis FRM, van Rooijen DM, Knol MJ, Stoof SP, Sanders EAM, Berbers GAM. Meningococcal serogroup C immunogenicity, antibody persistence and memory B-cells induced by the monovalent meningococcal serogroup C versus quadrivalent meningococcal serogroup ACWY conjugate booster vaccine: a randomized controlled trial. Vaccine. 2017.","DOI":"10.1016\/j.vaccine.2017.06.053"},{"key":"650_CR19","doi-asserted-by":"crossref","unstructured":"van Ravenhorst MB, van der Klis FRM, van Rooijen DM, Sanders EAM, Berbers GAM. Adolescent meningococcal serogroup a, W and Y immune responses following immunization with quadrivalent meningococcal a, C, W and Y conjugate vaccine: optimal age for vaccination. Vaccine. 2017.","DOI":"10.1016\/j.vaccine.2017.06.007"},{"issue":"1","key":"650_CR20","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1148\/radiology.143.1.7063747","volume":"143","author":"JA Hanley","year":"1982","unstructured":"Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143(1):29\u201336.","journal-title":"Radiology"},{"issue":"5","key":"650_CR21","first-page":"540","volume":"12","author":"K Fylkesnes","year":"1998","unstructured":"Fylkesnes K, Kasumba K. The first Zambian population-based HIV survey: saliva-based testing is accurate and acceptable. Aids. 1998;12(5):540\u20131.","journal-title":"Aids"},{"issue":"1","key":"650_CR22","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1128\/MMBR.62.1.71-109.1998","volume":"62","author":"H Marcotte","year":"1998","unstructured":"Marcotte H, Lavoie MC. Oral microbial ecology and the role of salivary immunoglobulin a. Microbiology and molecular biology reviews : MMBR. 1998;62(1):71\u2013109.","journal-title":"Microbiology and molecular biology reviews : MMBR"},{"issue":"10","key":"650_CR23","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1136\/jcp.2004.016253","volume":"57","author":"Q Zhang","year":"2004","unstructured":"Zhang Q, Finn A. Mucosal immunology of vaccines against pathogenic nasopharyngeal bacteria. J Clin Pathol. 2004;57(10):1015\u201321.","journal-title":"J Clin Pathol"},{"issue":"5","key":"650_CR24","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1017\/S0950268805004097","volume":"133","author":"RE Horton","year":"2005","unstructured":"Horton RE, Stuart J, Christensen H, Borrow R, Guthrie T, Davenport V, Finn A, Williams NA, Heyderman RS, Team AS. Influence of age and carriage status on salivary IgA to Neisseria meningitidis. Epidemiol Infect. 2005;133(5):883\u20139.","journal-title":"Epidemiol Infect"},{"issue":"2","key":"650_CR25","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1017\/S0950268899002915","volume":"123","author":"R Borrow","year":"1999","unstructured":"Borrow R, Fox AJ, Cartwright K, Begg NT, Jones DM. Salivary antibodies following parenteral immunization of infants with a meningococcal serogroup a and C conjugated vaccine. Epidemiol Infect. 1999;123(2):201\u20138.","journal-title":"Epidemiol Infect"},{"issue":"4","key":"650_CR26","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0191261","volume":"13","author":"MB Ravenhorst van","year":"2018","unstructured":"van Ravenhorst MB, den Hartog G, van der Klis FRM, van Rooijen DM, Sanders EAM, Berbers GAM. Induction of salivary antibody levels in Dutch adolescents after immunization with monovalent meningococcal serogroup C or quadrivalent meningococcal serogroup a, C, W and Y conjugate vaccine. PLoS One. 2018;13(4):e0191261.","journal-title":"PLoS One"},{"issue":"1","key":"650_CR27","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1093\/infdis\/135.1.94","volume":"135","author":"MP Glode","year":"1977","unstructured":"Glode MP, Robbins JB, Liu TY, Gotschlich EC, Orskov I, Orskov F. Cross-antigenicity and immunogenicity between capsular polysaccharides of group C Neisseria meningitidis and of Escherichia coli K92. J Infect Dis. 1977;135(1):94\u2013104.","journal-title":"J Infect Dis"},{"issue":"6","key":"650_CR28","doi-asserted-by":"crossref","first-page":"1654","DOI":"10.1128\/IAI.13.6.1654-1662.1976","volume":"13","author":"WF Vann","year":"1976","unstructured":"Vann WF, Liu TY, Robbins JB. Bacillus pumilus polysaccharide cross-reactive with meningococcal group a polysaccharide. Infect Immun. 1976;13(6):1654\u201362.","journal-title":"Infect Immun"}],"container-title":["BMC Medical Research Methodology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12874-018-0650-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12874-018-0650-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12874-018-0650-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,11,21]],"date-time":"2020-11-21T19:52:47Z","timestamp":1605988367000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmedresmethodol.biomedcentral.com\/articles\/10.1186\/s12874-018-0650-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,5]]},"references-count":28,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["650"],"URL":"https:\/\/doi.org\/10.1186\/s12874-018-0650-3","relation":{},"ISSN":["1471-2288"],"issn-type":[{"value":"1471-2288","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,1,5]]},"assertion":[{"value":"14 November 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 December 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 January 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Ethical approval was obtained from the local Medical research Ethics Committees United (MEC-U). The trial was undertaken in accordance with the Good Clinical Practice guidelines established by the International Conference on Harmonization and with the Declaration of Helsinki. Written informed consent was obtained from both parents or guardians and subjects aged \u226512\u2009years before enrollment. This study was registered at the EU Clinical Trials database (EudraCT number: 2013\u2013001823-38) and at the Dutch Trial Register (; NTR4430).","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":"MBvR, FRMvdK, DMvR, and GAMB report no conflict of interest. EAMS declares to have received research grants from GlaxoSmithKline and from Pfizer.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Publisher\u2019s Note"}}],"article-number":"1"}}