High coverage of diverse invasive meningococcal serogroup B strains by the 4-component vaccine 4CMenB in Australia, 2007–2011: Concordant predictions between MATS and genetic MATS

ABSTRACT Meningococcal serogroup B (MenB) accounts for an important proportion of invasive meningococcal disease (IMD). The 4-component vaccine against MenB (4CMenB) is composed of factor H binding protein (fHbp), neisserial heparin-binding antigen (NHBA), Neisseria adhesin A (NadA), and outer membrane vesicles of the New Zealand strain with Porin 1.4. A meningococcal antigen typing system (MATS) and a fully genomic approach, genetic MATS (gMATS), were developed to predict coverage of MenB strains by 4CMenB. We characterized 520 MenB invasive disease isolates collected over a 5-year period (January 2007–December 2011) from all Australian states/territories by multilocus sequence typing and estimated strain coverage by 4CMenB. The clonal complexes most frequently identified were ST-41/44 CC/Lineage 3 (39.4%) and ST-32 CC/ET-5 CC (23.7%). The overall MATS predicted coverage was 74.6% (95% coverage interval: 61.1%–85.6%). The overall gMATS prediction was 81.0% (lower–upper limit: 75.0–86.9%), showing 91.5% accuracy compared with MATS. Overall, 23.7% and 13.1% (MATS) and 26.0% and 14.0% (gMATS) of isolates were covered by at least 2 and 3 vaccine antigens, respectively, with fHbp and NHBA contributing the most to coverage. When stratified by year of isolate collection, state/territory and age group, MATS and gMATS strain coverage predictions were consistent across all strata. The high coverage predicted by MATS and gMATS indicates that 4CMenB vaccination may have an impact on the burden of MenB-caused IMD in Australia. gMATS can be used in the future to monitor variations in 4CMenB strain coverage over time and geographical areas even for non-culture confirmed IMD cases.

[1]  F. Russo,et al.  Effectiveness and Impact of the 4CMenB Vaccine against Group B Meningococcal Disease in Two Italian Regions Using Different Vaccination Schedules: A Five-Year Retrospective Observational Study (2014–2018) , 2020, Vaccines.

[2]  K. Jolley,et al.  Meningococcal Deduced Vaccine Antigen Reactivity (MenDeVAR) Index: a Rapid and Accessible Tool That Exploits Genomic Data in Public Health and Clinical Microbiology Applications , 2020, Journal of Clinical Microbiology.

[3]  Monica Lahra,et al.  Australian Meningococcal Surveillance Programme annual report, 2018. , 2020, Communicable diseases intelligence.

[4]  N. Andrews,et al.  Vaccination of Infants with Meningococcal Group B Vaccine (4CMenB) in England. , 2020, The New England journal of medicine.

[5]  M. Pizza,et al.  Does vaccination with 4CMenB convey protection against meningococcal serogroup B strains not predicted to be covered by MATS? A study of the UK clonal complex cc269 , 2019, Human vaccines & immunotherapeutics.

[6]  R. Rappuoli,et al.  Genetic Meningococcal Antigen Typing System (gMATS): A genotyping tool that predicts 4CMenB strain coverage worldwide. , 2019, Vaccine.

[7]  P. De Wals,et al.  The Global Meningococcal Initiative meeting on prevention of meningococcal disease worldwide: Epidemiology, surveillance, hypervirulent strains, antibiotic resistance and high-risk populations , 2019, Expert review of vaccines.

[8]  M. Giuliani,et al.  Meningococcal Antigen Typing System (MATS): A Tool to Estimate Global Coverage for 4CMenB, a Multicomponent Meningococcal B Vaccine. , 2019, Methods in molecular biology.

[9]  J. Bray,et al.  Potential Coverage of the 4CMenB Vaccine against Invasive Serogroup B Neisseria meningitidis Isolated from 2009 to 2013 in the Republic of Ireland , 2018, mSphere.

[10]  D. Medini,et al.  Interplay Between Virulence and Variability Factors as a Potential Driver of Invasive Meningococcal Disease , 2018, Computational and structural biotechnology journal.

[11]  J. Breuer,et al.  Targeted DNA enrichment and whole genome sequencing of Neisseria meningitidis directly from clinical specimens. , 2017, International journal of medical microbiology : IJMM.

[12]  Monica Lahra,et al.  Australian Meningococcal Surveillance Programme annual report, 2016. , 2017, Communicable diseases intelligence quarterly report.

[13]  D. Medini,et al.  Meningococcal Antigen Typing System (MATS)-Based Neisseria meningitidis Serogroup B Coverage Prediction for the MenB-4C Vaccine in the United States , 2017, mSphere.

[14]  J. McVernon,et al.  Epidemiology of invasive meningococcal B disease in Australia, 1999–2015: priority populations for vaccination , 2017, The Medical journal of Australia.

[15]  O. Bjørnstad,et al.  Differences in the population structure of Neisseria meningitidis in two Australian states: Victoria and Western Australia , 2017, PloS one.

[16]  M. Pizza,et al.  Meningococcal serogroup B strain coverage of the multicomponent 4CMenB vaccine with corresponding regional distribution and clinical characteristics in England, Wales, and Northern Ireland, 2007-08 and 2014-15: a qualitative and quantitative assessment. , 2017, The Lancet. Infectious diseases.

[17]  M. Pizza,et al.  Predicted strain coverage of a meningococcal multicomponent vaccine (4CMenB) in Portugal , 2017, PloS one.

[18]  INVASIVE MENINGOCOCCAL DISEASE NATIONAL SURVEILLANCE REPORT , 2017 .

[19]  David R. Riley,et al.  In-silico prediction and deep-DNA sequencing validation indicate phase variation in 115 Neisseria meningitidis genes , 2016, BMC Genomics.

[20]  D. Medini,et al.  Pooled-sera hSBA titres predict individual seroprotection in infants and toddlers vaccinated with 4CMenB. , 2016, Vaccine.

[21]  Monica Lahra,et al.  Meningococcal disease epidemiology in Australia 10 years after implementation of a national conjugate meningococcal C immunization programme , 2016, Epidemiology and Infection.

[22]  M. Comanducci,et al.  Predicted Strain Coverage of a New Meningococcal Multicomponent Vaccine (4CMenB) in Spain: Analysis of the Differences with Other European Countries , 2016, PloS one.

[23]  M. Stella,et al.  High predicted strain coverage by the multicomponent meningococcal serogroup B vaccine (4CMenB) in Poland. , 2016, Vaccine.

[24]  D. Medini,et al.  MATS: Global coverage estimates for 4CMenB, a novel multicomponent meningococcal B vaccine. , 2015, Vaccine.

[25]  M. Valenzuela,et al.  [Laboratory surveillance for invasive meningococcal disease in Chile, 2006-2012]. , 2014, Revista chilena de infectologia : organo oficial de la Sociedad Chilena de Infectologia.

[26]  M. Comanducci,et al.  Diversity of greek meningococcal serogroup B isolates and estimated coverage of the 4CMenB meningococcal vaccine , 2014, BMC Microbiology.

[27]  D. Medini,et al.  Diversity of Canadian meningococcal serogroup B isolates and estimated coverage by an investigational meningococcal serogroup B vaccine (4CMenB). , 2013, Vaccine.

[28]  D. Medini,et al.  Bactericidal antibody against a representative epidemiological meningococcal serogroup B panel confirms that MATS underestimates 4CMenB vaccine strain coverage. , 2013, Vaccine.

[29]  R. Rappuoli,et al.  Predicted strain coverage of a meningococcal multicomponent vaccine (4CMenB) in Europe: a qualitative and quantitative assessment. , 2013, The Lancet. Infectious diseases.

[30]  R. Rappuoli,et al.  Interlaboratory Standardization of the Sandwich Enzyme-Linked Immunosorbent Assay Designed for MATS, a Rapid, Reproducible Method for Estimating the Strain Coverage of Investigational Vaccines , 2012, Clinical and Vaccine Immunology.

[31]  Julie C Dunning Hotopp,et al.  Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination , 2011, Proceedings of the National Academy of Sciences.

[32]  R. Rappuoli,et al.  Qualitative and quantitative assessment of meningococcal antigens to evaluate the potential strain coverage of protein-based vaccines , 2010, Proceedings of the National Academy of Sciences.

[33]  M. Pizza,et al.  Characterization of fHbp, nhba (gna2132), nadA, porA, and Sequence Type in Group B Meningococcal Case Isolates Collected in England and Wales during January 2008 and Potential Coverage of an Investigational Group B Meningococcal Vaccine , 2010, Clinical and Vaccine Immunology.

[34]  R. Rappuoli,et al.  A universal vaccine for serogroup B meningococcus. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Achtman,et al.  Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. , 1998, Proceedings of the National Academy of Sciences of the United States of America.