{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T09:03:57Z","timestamp":1789549437135,"version":"build-2803163510"},"reference-count":39,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2021,1,4]],"date-time":"2021-01-04T00:00:00Z","timestamp":1609718400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vaccines"],"abstract":"<jats:p>Patients with chronic diseases are at increased risk of complications following infection. It remains, however, unknown to what extend they are protected against vaccine-preventable diseases. We assessed seroprevalence of antibodies against diphtheria, tetanus and pertussis to evaluate whether current vaccination programs in Belgium are adequate. Antibody titers were assessed with a bead-based multiplex assay in serum of 1052 adults with chronic diseases. We included patients with diabetes mellitus type 1 (DM1) (n = 172), DM2 (n = 77), chronic kidney disease (n = 130), chronic obstructive pulmonary disease (COPD) (n = 170), heart failure (n = 77), HIV (n = 196) and solid organ transplant (SOT) recipients (n = 230). Factors associated with seroprevalence were analysed with multiple logistic regression. We found seroprotective titers in 29% for diphtheria (\u22650.1 IU\/mL), in 83% for tetanus (\u22650.1 IU\/mL) and 22% had antibodies against pertussis (\u22655 IU\/mL). Seroprotection rates were higher (p &lt; 0.001) when vaccinated within the last ten years. Furthermore, diphtheria seroprotection decreased with age (p &lt; 0.001). Tetanus seroprotection was less reached in women (p &lt; 0.001) and older age groups (p &lt; 0.001). For pertussis, women had more often a titer suggestive of a recent infection or vaccination (\u2265100 IU\/mL, p &lt; 0.01). We conclude that except for tetanus, the vast majority of at-risk patients remains susceptible to vaccine-preventable diseases such as diphtheria and pertussis.<\/jats:p>","DOI":"10.3390\/vaccines9010018","type":"journal-article","created":{"date-parts":[[2021,1,4]],"date-time":"2021-01-04T08:35:19Z","timestamp":1609749319000},"page":"18","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Seroprevalence of Antibodies against Diphtheria, Tetanus and Pertussis in Adult At-Risk Patients"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9623-4482","authenticated-orcid":false,"given":"Lise","family":"Boey","sequence":"first","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eline","family":"Bosmans","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liane Braz","family":"Ferreira","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathalie","family":"Heyvaert","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa","family":"Nelen","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Smans","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanne","family":"Tuerlinckx","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3749-0475","authenticated-orcid":false,"given":"Mathieu","family":"Roelants","sequence":"additional","affiliation":[{"name":"Environment and Health, Department of Public Health and Primary Care, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8510-2345","authenticated-orcid":false,"given":"Kathleen","family":"Claes","sequence":"additional","affiliation":[{"name":"Department of Nephrology and Renal Transplantation, University Hospitals Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Inge","family":"Derdelinckx","sequence":"additional","affiliation":[{"name":"Department of General Internal Medicine, University Hospitals of Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1830-2982","authenticated-orcid":false,"given":"Wim","family":"Janssens","sequence":"additional","affiliation":[{"name":"Department of Respiratory Diseases, University Hospitals of Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chantal","family":"Mathieu","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, University Hospitals of Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johan","family":"Van Cleemput","sequence":"additional","affiliation":[{"name":"Department of Cardiology, University Hospitals of Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3468-9251","authenticated-orcid":false,"given":"Robin","family":"Vos","sequence":"additional","affiliation":[{"name":"Department of Respiratory Diseases\u2014Lung Transplantation Unit, University Hospitals of Leuven, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabelle","family":"Desombere","sequence":"additional","affiliation":[{"name":"NRC Bordetella Pertussis and NRC Toxigenic Corynebacteria, Sciensano (Public Health Belgium), Engelandstraat 642, 1180 Ukkel, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1954-7554","authenticated-orcid":false,"given":"Corinne","family":"Vandermeulen","sequence":"additional","affiliation":[{"name":"Department of Public Health and Primary Care, Leuven University Vaccinology Center, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"},{"name":"Environment and Health, Department of Public Health and Primary Care, KU Leuven, Kapucijnenvoer 35, P.O. Box 7001, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1093\/cid\/ciy889","article-title":"Severe pertussis infections in the United States, 2011\u20132015","volume":"69","author":"Mbaeyi","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1017\/S0950268817000887","article-title":"Economic burden of diagnosed pertussis among individuals with asthma or chronic obstructive pulmonary disease in the USA: An analysis of administrative claims","volume":"145","author":"Buck","year":"2017","journal-title":"Epidemiol. Infect."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1080\/21645515.2019.1652517","article-title":"The unmet need for pertussis prevention in patients with chronic obstructive pulmonary disease in the Italian context","volume":"16","author":"Blasi","year":"2019","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_4","unstructured":"Gisle, L., Hesse, E., Drieskens, S., Demarest, S., Van der Heyden, J., and Tafforeau, J. (2020, January 14). Health Survey Belgium, 2008, (In Dutch)."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5222","DOI":"10.1016\/j.vaccine.2012.06.012","article-title":"Variation in adult vaccination policies across Europe: An overview from VENICE network on vaccine recommendations, funding and coverage","volume":"30","author":"Kanitz","year":"2012","journal-title":"Vaccine"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"6681","DOI":"10.1016\/j.vaccine.2016.11.015","article-title":"Vaccination of special populations: Protecting the vulnerable","volume":"34","author":"Doherty","year":"2016","journal-title":"Vaccine"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1542\/peds.2008-3645","article-title":"Booster vaccinations: Can immunologic memory outpace disease pathogenesis?","volume":"124","author":"Pichichero","year":"2009","journal-title":"Pediatrics"},{"key":"ref_8","unstructured":"Offit, P.A., Plotkin, S.A., and Orenstein, W. (2018). Vaccine immunology: How do vaccines mediate protection?. Plotkin\u2019s Vaccines, Elsevier. [7th ed.]."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/0272-6386(95)90491-3","article-title":"Tetanus immunization and its association to hepatitis B vaccination in patients with chronic renal failure","volume":"26","author":"Girndt","year":"1995","journal-title":"Am. J. Kidney Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.autrev.2011.05.015","article-title":"Immunization in the adult immunocompromised host","volume":"11","author":"Loebermann","year":"2012","journal-title":"Autoimmun. Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1017\/S0950268810001536","article-title":"Are we hitting immunity targets? The 2006 age-specific seroprevalence of measles, mumps, rubella, diphtheria and tetanus in Belgium","volume":"139","author":"Theeten","year":"2010","journal-title":"Epidemiol. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2412","DOI":"10.1016\/S0264-410X(03)00062-8","article-title":"Seroprevalence of Bordetella pertussis antibodies in Flanders (Belgium)","volume":"21","author":"Siegrist","year":"2003","journal-title":"Vaccine"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1542\/peds.2004-2648","article-title":"The epidemiology of pertussis: A comparison of the epidemiology of the disease pertussis with the epidemiology of Bordetella pertussis infection","volume":"115","author":"Cherry","year":"2005","journal-title":"Pediatrics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/cei.12822","article-title":"Adult vaccination against tetanus and diphtheria: The European perspective","volume":"187","author":"Weinberger","year":"2016","journal-title":"Clin. Exp. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1017\/S0950268812000210","article-title":"Comparative seroepidemiology of diphtheria in six European countries and Israel","volume":"141","author":"Kafatos","year":"2013","journal-title":"Epidemiol. Infect."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1099\/jmm.0.001039","article-title":"Diphtheria in Belgium: 2010\u20132017","volume":"68","author":"Martini","year":"2019","journal-title":"J. Med. Microbiol."},{"key":"ref_17","unstructured":"Van Damme, P., Theeten, H., Braeckman, T., Lernout, T., Hens, N., Roelants, M., and Hoppenbrouwers, K. (2020, March 03). Study of the Vaccination Coverage in Young Children and Adolescents in Flanders in 2012, (In Dutch)."},{"key":"ref_18","unstructured":"(2020, March 03). UZ Leuven. (In Dutch)."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2136","DOI":"10.1080\/21645515.2020.1763739","article-title":"Vaccination coverage of recommended vaccines and determinants of vaccination in at-risk groups","volume":"16","author":"Boey","year":"2020","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1900164","DOI":"10.1183\/13993003.00164-2019","article-title":"Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease: The GOLD science committee report 2019","volume":"53","author":"Singh","year":"2019","journal-title":"Eur. Respir. J."},{"key":"ref_21","unstructured":"(2019, November 21). American Heart Association: Classes of Heart Failure. Available online: https:\/\/www.heart.org\/en\/health-topics\/heart-failure\/what-is-heart-failure\/classes-of-heart-failure."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2089","DOI":"10.1111\/j.1523-1755.2005.00365.x","article-title":"Definition and classification of chronic kidney disease: A position statement from kidney disease: Improving global outcomes (KDIGO)","volume":"67","author":"Levey","year":"2005","journal-title":"Kidney Int."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Cabor\u00e9, R.N., Pi\u00e9rard, D., and Huygen, K. (2016). A Belgian serosurveillance\/seroprevalence study of diphtheria, tetanus and pertussis using a Luminex xMAP technology-based pentaplex. Vaccines, 4.","DOI":"10.3390\/vaccines4020016"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1128\/CVI.00131-10","article-title":"Correlates of protection induced by vaccination","volume":"17","author":"Plotkin","year":"2010","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s10096-010-1104-y","article-title":"What to do and what not to do in serological diagnosis of pertussis: Recommendations from EU reference laboratories","volume":"30","author":"Guiso","year":"2010","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1264","DOI":"10.1053\/ajkd.2001.29223","article-title":"A 5-year follow-up on antibody response after diphtheria and tetanus vaccination in hemodialysis patients","volume":"38","author":"Kirchner","year":"2001","journal-title":"Am. J. Kidney Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1034\/j.1399-3046.1999.00013.x","article-title":"Duration of immunity to diphtheria and tetanus in young kidney transplant patients","volume":"3","author":"Pedrazzi","year":"1999","journal-title":"Pediatr. Transplant."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1016\/j.vaccine.2013.03.035","article-title":"Impaired cellular immune response to tetanus toxoid but not to cytomegalovirus in effectively HAART-treated HIV-infected children","volume":"31","author":"Alsina","year":"2013","journal-title":"Vaccine"},{"key":"ref_29","unstructured":"Litzroth, A., Desombere, I., Martini, H., Pi\u00e9rard, D., Carrillo, P., Mahieu, R., Schirvel, C., and Top, G. (2018). Epidemiologische Surveillance van Kinkhoest Bordetella pertussis-2018, Sciensano. Available online: https:\/\/www.sciensano.be\/nl\/biblio\/epidemiologische-surveillance-van-kinkhoest-bordetella-pertussis-2018."},{"key":"ref_30","unstructured":"(2020, February 23). European Centre for Disease Prevention and Control (ECDC): Pertussis\u2014Annual Epidemiological Report for 2017. Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/pertussis-annual-epidemiological-report-2017."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/S1081-1206(10)61114-3","article-title":"Declining cell-mediated immunity and increased chronic disease burden","volume":"94","author":"Rafi","year":"2005","journal-title":"Ann. Allergy Asthma Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.trre.2008.07.001","article-title":"Vaccination of the solid organ transplant recipient","volume":"22","author":"Sester","year":"2008","journal-title":"Transplant. Rev."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Schaefer, F., Rutt, S., Fine, R.N., and Warady, B.A. (2012). Immune function and immunizations in dialyzed children. Pediatric Dialysis, Springer US.","DOI":"10.1007\/978-1-4614-0721-8_28"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.2215\/CJN.00950208","article-title":"Aspects of immune dysfunction in end-stage renal disease","volume":"3","author":"Kato","year":"2008","journal-title":"Clin. J. Am. Soc. Nephrol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1177\/1753465816646050","article-title":"Influenza vaccination for patients with chronic obstructive pulmonary disease: Understanding immunogenicity, efficacy and effectiveness","volume":"10","author":"Sanei","year":"2016","journal-title":"Ther. Adv. Respir. Dis."},{"key":"ref_36","first-page":"172","article-title":"High seroprevalence of Bordetella pertussis in patients with chronic obstructive pulmonary disease: A case-control study","volume":"14","author":"Hashemi","year":"2015","journal-title":"Tanaffos"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1001\/jamapediatrics.2018.4954","article-title":"Incidence of hospitalization for vaccine-preventable infections in children following solid organ transplant and associated morbidity, mortality, and costs","volume":"173","author":"Feldman","year":"2019","journal-title":"JAMA Pediatr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1093\/cid\/cix421","article-title":"Reduced severity of pertussis in persons with age-appropriate pertussis vaccination\u2014United States, 2010\u20132012","volume":"65","author":"McNamara","year":"2017","journal-title":"Clin. Infect. Dis."},{"key":"ref_39","unstructured":"Dhondt, D.E., Leroux-Roels, G., and Leroux-Roels, I. (2013). Evaluatie van de Implementatiegraad van de Cocoonvaccinatiestrategie Tegen Kinkhoest. In Welke Mate Zijn Ouders Anno 2012 Ge\u00efnformeerd en Gevaccineerd? [Evaluation of Implemation of the Cocoon Vaccination Strategy against Pertussis. How Well Are Parents Informed and Vaccinated in 2012?]. [Master\u2019s Thesis, University of Ghent]. (In Dutch)."}],"container-title":["Vaccines"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/1\/18\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:06:47Z","timestamp":1760159207000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/1\/18"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,4]]},"references-count":39,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["vaccines9010018"],"URL":"https:\/\/doi.org\/10.3390\/vaccines9010018","relation":{},"ISSN":["2076-393X"],"issn-type":[{"value":"2076-393X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,4]]}}}