Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage

Jay Lucidarme; Dorothea M C Hill; Holly B Bratcher; Steve J Gray; Mignon du Plessis; Raymond S W Tsang; Julio A Vazquez; Muhamed-Kheir Taha; Mehmet Ceyhan; Adriana M Efron; Maria C Gorla; Jamie Findlow; Keith A Jolley; Martin C J Maiden; Ray Borrow

doi:10.1016/j.jinf.2015.07.007

Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage

J Infect. 2015 Nov;71(5):544-52. doi: 10.1016/j.jinf.2015.07.007. Epub 2015 Jul 28.

Authors

Affiliations

¹ Vaccine Evaluation Unit, Public Health England, Manchester Medical Microbiology Partnership, Second Floor, Clinical Sciences Building II, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WZ, UK. Electronic address: jay.lucidarme@phe.gov.uk.
² Department of Zoology, University of Oxford, Oxford, UK. Electronic address: dorothea.hill@zoo.ox.ac.uk.
³ Department of Zoology, University of Oxford, Oxford, UK. Electronic address: holly.bratcher@zoo.ox.ac.uk.
⁴ Meningococcal Reference Unit, Public Health England, Manchester Medical Microbiology Partnership, Second Floor, Clinical Sciences Building II, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WZ, UK. Electronic address: Steve.Gray@phe.gov.uk.
⁵ Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, National Health Laboratory Service, 1 Modderfontein Road, Sandringham, Johannesburg, 2131, South Africa. Electronic address: mignond@nicd.ac.za.
⁶ National Microbiology Laboratory, Public Health Agency of Canada, 1015 Arlington Street, Winnipeg, MB R3E 3R2, Canada. Electronic address: Raymond.Tsang@phac-aspc.gc.ca.
⁷ Reference Laboratory for Meningococci, Institute of Health Carlos III, Majadahonda, Spain. Electronic address: julioavazquez@gmail.com.
⁸ Institut Pasteur, Unité des Infections Bactériennes invasives, Département Infection et Epidémiologie, Paris, France. Electronic address: muhamed-kheir.taha@pasteur.fr.
⁹ Faculty of Medicine, Hacettepe University, Ankara, Turkey. Electronic address: mceyhan@hacettepe.edu.tr.
¹⁰ Servicio Bacteriología Clínica, Departamento de Bacteriología, Instituto Nacional de Enfermedades Infecciosas-ANLIS «Dr. Carlos G. Malbrán», Ciudad Autónoma de Buenos Aires, Argentina. Electronic address: amefron@anlis.gov.ar.
¹¹ Division of Medical Biology, Bacteriology Department, Adolfo Lutz Institute, São Paulo 01246-902, Brazil. Electronic address: mcgorla@ial.sp.gov.br.
¹² Vaccine Evaluation Unit, Public Health England, Manchester Medical Microbiology Partnership, Second Floor, Clinical Sciences Building II, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WZ, UK. Electronic address: Jamie.Findlow@phe.gov.uk.
¹³ Department of Zoology, University of Oxford, Oxford, UK. Electronic address: keith.jolley@zoo.ox.ac.uk.
¹⁴ Department of Zoology, University of Oxford, Oxford, UK. Electronic address: martin.maiden@zoo.ox.ac.uk.
¹⁵ Vaccine Evaluation Unit, Public Health England, Manchester Medical Microbiology Partnership, Second Floor, Clinical Sciences Building II, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WZ, UK; Meningococcal Reference Unit, Public Health England, Manchester Medical Microbiology Partnership, Second Floor, Clinical Sciences Building II, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WZ, UK. Electronic address: Ray.Borrow@phe.gov.uk.

Abstract

Objectives: Neisseria meningitidis is a leading cause of meningitis and septicaemia. The hyperinvasive ST-11 clonal complex (cc11) caused serogroup C (MenC) outbreaks in the US military in the 1960s and UK universities in the 1990s, a global Hajj-associated serogroup W (MenW) outbreak in 2000-2001, and subsequent MenW epidemics in sub-Saharan Africa. More recently, endemic MenW disease has expanded in South Africa, South America and the UK, and MenC cases have been reported among European and North American men who have sex with men (MSM). Routine typing schemes poorly resolve cc11 so we established the population structure at genomic resolution.

Methods: Representatives of these episodes and other geo-temporally diverse cc11 meningococci (n = 750) were compared across 1546 core genes and visualised on phylogenetic networks.

Results: MenW isolates were confined to a distal portion of one of two main lineages with MenB and MenC isolates interspersed elsewhere. An expanding South American/UK MenW strain was distinct from the 'Hajj outbreak' strain and a closely related endemic South African strain. Recent MenC isolates from MSM in France and the UK were closely related but distinct.

Conclusions: High resolution 'genomic' multilocus sequence typing is necessary to resolve and monitor the spread of diverse cc11 lineages globally.

Keywords: Genome; Meningococcal; ST-11 clonal complex; Serogroup C; Serogroup W.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Disease Outbreaks
Endemic Diseases
France / epidemiology
Homosexuality, Male
Humans
Male
Meningococcal Infections / epidemiology*
Meningococcal Infections / microbiology*
Multilocus Sequence Typing*
Neisseria meningitidis / classification
Neisseria meningitidis / genetics*
Neisseria meningitidis / isolation & purification
Neisseria meningitidis, Serogroup B / classification
Neisseria meningitidis, Serogroup B / genetics*
Neisseria meningitidis, Serogroup B / isolation & purification
Neisseria meningitidis, Serogroup C / classification
Neisseria meningitidis, Serogroup C / genetics*
Neisseria meningitidis, Serogroup C / isolation & purification
North America / epidemiology
Phylogeny
Serogroup
Serotyping
South Africa / epidemiology
South America / epidemiology
United Kingdom / epidemiology

Grants and funding

087622/WT_/Wellcome Trust/United Kingdom