ABSTRACT
Invasive meningococcal disease (IMD) is a serious disease that is fatal in 5–15% and disabling in 12–20% of cases. The dynamic and unpredictable epidemiology is a particular challenge of IMD prevention. Although vaccination against meningococcal serogroups A (MenA), MenC and, more recently, MenB, are proving successful, other serogroups are emerging as major IMD causes. Recently, surges in MenW incidence occurred in South America, Europe, Australia and parts of sub-Saharan Africa, with hypervirulent strains being associated with severe IMD and higher fatality rates. This review describes global trends in MenW-IMD epidemiology over the last 5–10 years, with emphasis on the response of national/regional health authorities to increased MenW prevalence in impacted areas. Several countries (Argentina, Australia, Chile, the Netherlands and UK) have implemented reactive vaccination campaigns to reduce MenW-IMD, using MenACWY conjugate vaccines. Future vaccination programs should consider the evolving epidemiology of MenW-IMD and the most impacted age groups.
Introduction
The bacterium Neisseria meningitidis only infects humans and causes invasive meningococcal disease (IMD). IMD is a serious disease with case fatality rates of around 10% even with treatment.Citation1 It is associated with severe sequelae in up to 20% of survivors, including limb amputation, neurological deficits, hearing loss, and other serious disabilities.Citation2 The highest incidence of IMD is typically reported in infants <1 year old, with secondary peaks in incidence occurring in adolescents/young adults and sometimes in older adults (≥65 years of age).Citation3
Worldwide, most regions have experienced a downward trend in the incidence of IMD in recent years,Citation4–Citation7 probably due in part to a combination of active immunization and secular change impacting risk factors for the diseaseCitation8,Citation9 (e.g., the overall improvement of socioeconomic status and changes in attitude towards behavioral risk factors like smoking habits). In the industrialized world, the majority of cases are sporadic (e.g., in the United States [US], less than 2% of cases are associated with outbreaksCitation10), but IMD is unpredictable with outbreaks and epidemics characterizing the pathogen since it was first identified.Citation11,Citation12
Almost all cases of both endemic and epidemic IMD are caused by one of 6 meningococcal serogroups: A (MenA), MenB, MenC, MenW, MenY, MenX. Their relative importance as causative agents vary considerably across geographical locations, time periods and age of the hosts.Citation3,Citation13,Citation14 Frequent unexplained changes in serogroup incidences and emergence of new, more or less virulent strain variants,Citation3 and higher CFRs have been observed for specific serogroupsCitation15 and clonal complexes globally. Meningococci often undergo horizontal gene transfer and spontaneous chromosomal mutations, which cause wide genetic and antigenic diversity between strains.Citation3,Citation16,Citation17 This is perhaps best illustrated by unexpected surges in the prevalence of meningococcal serogroups (e.g., for MenY in Scandinavian countries, between 2010 and 2012Citation18).
MenW was previously responsible for <5% of IMD cases,Citation19 until the first confirmed MenW-caused outbreak in Hajj pilgrims, during 2000.Citation20 Since then, this serogroup has become a dominant cause of IMD, albeit so far in a limited number of countries, particularly in Europe, South America, Australia and some parts of Sub-Saharan Africa.Citation9,Citation14
In this paper, an overview of the epidemiology of MenW during the last 5–10 years is provided, as well as of the preventive actions taken to date in countries that have experienced an increase of IMD incidence due to MenW.
summarizes the research, clinical relevance and impact on the patient population.
Global impact of the evolving epidemiology of MenW
MenW was first observed among military personnel in the US in the late 1960s by researchers at the Walter Reed Army Institute of Research,Citation21 where the W-135 designation originated. At the proposal of Harrison et al in 2013, the numeric component has since been dropped and the serogroup was renamed simply “W”.Citation22 Until the year 2000, MenW was responsible for relatively few cases of IMD and was not reported to cause large outbreaks.Citation3,Citation23
A pivotal event was the large outbreak among Hajj pilgrims in Mecca, Saudi Arabia, in the year 2000,Citation24 with more than 400 cases and 52 confirmed deaths among the pilgrims and their contacts.Citation23 The outbreak was caused by a clone in the sequence type-11 clonal complex (cc11),Citation24 and infections with MenW:c11 strains were subsequently reported throughout EuropeCitation24,Citation25 and the rest of the world,Citation26–Citation28 with epidemics in Africa from 2000. Several more outbreaks have since been reported in other countries, including France and the United Kingdom (UK).Citation23,Citation25 Over the last 2 decades, the most concerning MenW isolates are those from outbreaks occurring in England and WalesCitation29 and the Southern Cone in Latin AmericaCitation30; they were shown to belong to the same lineage (the South American/UK cc11 lineage) and were recently proved to be divergent from the Hajj outbreak strain.Citation31
As with other meningococci belonging to cc11,Citation31 MenW strains causing IMD in recent years are particularly virulent with higher morbidity and CFRs, atypical clinical features, and generally affecting more older adults compared to other common serogroups (A, B, C, X; except maybe Y).Citation23 To date, atypical clinical presentations have included septic arthritis and severe respiratory tract infections (including pneumonia, epiglottitis and supraglottitis).Citation32 Fatal cases have occurred among adolescents and young adults with MenW septicemia, who presented primarily with gastrointestinal symptoms and then had rapid progression of the disease.Citation33,Citation34 In the UK, the CFR observed after the clinical follow-up of all MenW cases (2010–2011 and 2012–2013) was 12%,Citation29 similar to that observed during MenC disease surveillance in 1999,Citation35 whereas in South America, isolates belonging to this lineage were reported to be even more deadly, with a CFR of 27% estimated during 2012.Citation36
The chronology of substantial change in the epidemiology of MenW IMD is presented in and an overview of selected relevant papers reporting on MenW IMD incidence is given in Supplementary Table S1.
Figure 2. Chronological overview of changes in MenW epidemiology in the last decade (up to July 2018). IMD, invasive meningococcal disease.
Note: MenW incidence rate is expressed per 100,000 population.
![Figure 2. Chronological overview of changes in MenW epidemiology in the last decade (up to July 2018). IMD, invasive meningococcal disease.Note: MenW incidence rate is expressed per 100,000 population.](/cms/asset/97c839e9-b017-4d64-b6ed-8ec41083647c/khvi_a_1532248_f0002_b.gif)
In South America, a localized increase in the prevalence of MenW was first observed in Southern Brazil in the years 2003–2005Citation37 and large increases have since been seen in Argentina and Chile.Citation38,Citation39 After the first reports in Brazil, Argentina experienced an increase in MenW cases from 2008,Citation40 with 78% of all MenW strains belonging to the hypervirulent c11 lineage.Citation39 Between 2012 and 2015, MenW was found to account for 47% of total IMD cases in all age groups, and for 46% of IMD in infants <9 months of age.Citation41 Infants continue to be the most impacted age group in Argentina, and contrary to findings in other countries, no increase in IMD incidence was observed in adolescents or older adults.Citation41
In Chile, the overall incidence of IMD was reported to decrease steadily between 2000 and 2012; however, this trend was not reflected by CFRs which showed a steep increase between 2009 and 2012.Citation38 This was due to the emergence of MenW strains belonging to the c11 lineage, which replaced MenB as the most common serogroup in Chile and affected mostly young children 0–5 years of age.Citation30,Citation38
Other adjacent countries, like Uruguay and Paraguay, also reported increases in the percentage of MenW-caused IMD in 2008 and 2009.Citation30,Citation40
In Europe, the UK and the Netherlands have seen up to 10-fold increases of MenW cases over just a few years.Citation42,Citation43 A recent study estimated a relative increase in MenW disease of 79% per year in England (from 30 MenW-IMD cases out of 730 total IMD cases in 2011–2012 to 176 out of 724 in 2014–2015) and of 418% in the Netherlands (from ~4 IMD cases in 2014–2015 to 26 MenW-IMD cases out of 114 total cases in 2015–2016).Citation44 The study further suggested the existence of a temporal association between the observed upsurges in these 2 countries.Citation44 Moreover, the age distribution of MenW cases in 2015–2016 in the Netherlands was similar to that observed in 2011–2013 in England, with most of the affected cases occurring initially in people aged ≥65 years and later on, in children and adolescents 10–19 years old.Citation32,Citation44 In 2014–2015, an age shift towards ≤5 year-olds was observed in the UK.Citation32 This trend is yet to be observed in the Netherlands. The increase in MenW disease in these 2 countries was due to cc11 strains, with the prevalence of non-cc11 isolates remaining relatively constant over the considered periods of time.Citation33,Citation45 While the MenW strains causing IMD in the UK starting from 2009 belonged to the so-called original UK strain of the South American/UK lineage, if one starts from 2013, a new variant was identified (the so-called UK 2013 strain).Citation29,Citation31 Isolates belonging to this strain are now responsible for most MenW cases and the steep increase in IMD incidence, including that observed in the Netherlands between 2014 and 2016,Citation44 and have displayed an ability to spread rapidly in the population in addition to their increased virulence.
A surge in the incidence of MenW IMD (from 0.02 to 0.2 per 100,000 population) observed between 2014 and 2016 in Sweden was also attributed mainly to isolates of the UK 2013 strain, with the ≥ 60 and 15–24 year age groups being the most impacted.Citation45
A steady increase in MenW incidence was also reported recently in Italy from 2012 to 2014, with no cases reported in infants.Citation46
In France, MenW was of less concern after the 2000–2003 global Hajj-associated outbreak, until 2016, when the frequency of MenW cases (albeit still the lowest of all serogroups) increased in comparison to previous years, leading to a reported incidence rate of 0.07 MenW cases/100,000 persons.Citation47 Similarly to findings in the other European countries, the majority of cases in 2015 and 2016 were attributed to isolates of the UK 2013 strain, and occurred in a large proportion (94%) in individuals ≥15 years of age.Citation47
More recently, during 2016 and the first trimester of 2017, an increase in MenW IMD was also evidenced in Spain, where isolates belonging to the South-American/UK lineage (both the original and the UK 2013 strain) were most commonly identified.Citation48
In Australia, IMD incidence was following a decreasing trend up to 2013, when it was reported as 0.6/100,000 population.Citation49 However, a recent series of increases was observed to 1.1/100,000 in 2016 and 1.6/100,000 individuals in 2017.Citation49,Citation50 This was mainly due to a surge in MenW cases, with notifications doubling from 2014 to 2015 (from 17 to 34 cases, respectively) and continuing to rise sharply in 2016 (108 cases) and 2017 (140 cases out of a total of 383 IMD reported cases).Citation49 Furthermore, an outbreak of MenW started in July 2017 in Central Australia with associated cases reported in other parts of the Northern Territory, Queensland, South Australia and Western Australia. The ongoing outbreak is impacting mostly young Aboriginal people in remote Central Australian communities.Citation51 A recent outbreak of 4 confirmed MenW cases, was reported in Tasmania.Citation52 The hypervirulent cc11 strain was identified for most cases of MenW reported between 2012 and 2017, with the majority of isolated being strain type P1.5,2:F1-1:ST11 or close variants, most of which clustered with isolates identified in the UK and South America during recent years.Citation53 MenW-caused IMD occurred more frequently in adults ≥45 years of age (in 2016, MenW caused 59% of IMD in ≥65-year-olds).Citation50 However, age-specific incidence of MenW IMD has increased in all age groups from 2015 to 2017, except the 15−19 years age-group where state-based vaccination programs have been introduced.Citation49,Citation50 While a large proportion of cases continue to occur in individuals aged ≥65 years, the steepest increase in the notification rates was observed in infants from 2015 to 2017.Citation49
National/regional vaccination recommendations for prevention of IMD
The essential desired effects of vaccination against IMD are firstly to protect vaccinees against IMD when exposed to N. meningitidis and also to reduce acquisition, carriage and onward transmission of the bacterium, particularly of hyperinvasive clones.Citation3 A characteristic which sets IMD apart from other infectious diseases is that for most circulating serogroups, the age group with the highest carriage (adolescents)Citation54 is not the one with the highest incidence (infants). Therefore, experiences with routine vaccination against N. meningitidis (particularly MenC campaigns) have historically followed one of possible 3 directions, illustrated with examples below: (i) offer direct protection only to high incidence groups, by targeting directly-impacted groups like infants; (ii) aim for indirect protection by vaccinating the carriers (adolescents), thus trying to prevent transmission to other age groups over time; or (iii) implement both of these strategies by vaccinating the high-incidence groups and offering catch-up campaigns.Citation3,Citation17 The latter approach may have the clear advantage of aiming to reduce both disease incidence and carriage.
Vaccination against IMD has been very effective in achieving control of the disease, as shown by several successful campaigns with conjugate meningococcal vaccines.Citation3,Citation14,Citation16 In 1999, in response to a steep increase in the number of MenC cases, the UK introduced conjugate MenC vaccine into the routine immunization program, first in infants, and subsequently in a single catch up program for everyone aged 12 months–17 years.Citation35,Citation55 The MenC vaccination program in the UK has been seen as a model for other countries across the world, with a similar “children plus catch-up” program (from 14 months of age up to 18 years old included) leading to comparable results in the Netherlands in preventing MenC-IMD.Citation56 A different approach was represented by the implementation of routine vaccination with MenC-conjugate vaccine in Brazil in 2010, for infants 3 and 5 months of age, with a booster at 12–15 months. This strategy achieved a rapid impact on the incidence of MenC, but only in the vaccinated age groups, with little to no effect observed in groups not targeted by the program.Citation57 As a result, Brazil decided to gradually implement MenC vaccination among adolescents 12–13 years of age starting in 2017, and targeting 9–10-year-olds by 2020.Citation58
Based on previous experience with conjugate vaccines used in the control of MenC (as illustrated) and subsequently, MenA-IMD in the African meningitis belt,Citation59 a mass vaccination campaign or routine immunization against MenW could also have the potential to decrease the incidence of MenW disease in affected areas, through direct protection and potentially also through indirect effects.Citation42,Citation60 To date, a growing number of countries worldwide are implementing vaccination programs to control outbreaks or increases over time of MenW-caused IMD, in view of the hypervirulence of currently circulating MenW strains. In addition, MenACWY vaccination – including booster vaccination after primary immunization against MenC – is recommended in several countries to maintain control over MenC-IMD and provide broader protection against other meningococcal serogroups (). Several other countries (Italy, the UK, the US, Greece, Austria, most of Canada, the Netherlands and regions in Australia) have included quadrivalent meningococcal vaccines for adolescents in their vaccination programs to provide a MenACWY booster in previously MenC primed individuals.Citation74
Table 1. Introduction of MenACWY vaccination in national immunization schedules.
Country-specific responses to the changing epidemiology of MenW
Chile
In Chile, vaccination strategies targeted the age group with the highest incidence and risk of meningococcal disease. In 2012, an immunization campaign was initiated, using conjugate quadrivalent vaccines administered to children 9 months–< 5 years old, as 2-dose series for those < 2 years old and 1-dose for 2–4 year-olds.Citation75 From January 1, 2014, the single dose MenACWY vaccination was included in the national immunization schedule and became mandatory for all children at 1 year of age.Citation61
The proportion of IMD cases due to MenW in all age groups increased from 58% in 2012 to 65% and 75% in 2013 and 2014, and then remained in the 62–67% range from 2015 to 2017.Citation76 The overall yearly incidence of IMD remained ≤ 1/100,000 persons, with estimated annual incidences of 0.8/100,000 in 2012–2014, 0.7/100,000 in 2015, 0.6/100,000 in 2016 and 0.3/100,00 up to September 2017.Citation76,Citation77 Vaccine coverage of 95.7% was reported in 2016 in infants aged <1 year.Citation76 An early impact of vaccination on the incidence of MenW was only seen for the age groups targeted for the vaccination, as indicated by a reduction of MenW cases of 71% reduction from 2011 to 2016 in children aged 1–5 years.Citation60 As an illustration of the threat of the new MenW clone in adolescents, the number of IMD cases in this age group increased over the same period, with most due to MenW.Citation60 No reduction of cases in unvaccinated age groups (herd effect of vaccination) occurred following mass vaccination of infants.Citation3,Citation17,Citation60
Argentina
In Argentina, an incidence of 0.44–0.75 IMD cases per year was reported, with a high proportion of IMD cases (47%) caused by MenW between 2012 and 2015.Citation41 To reduce the incidence and burden of IMD in infants, starting with January 2017, MenACWY vaccination was included in the national immunization plan for infants >3 months of age, according to a 2 + 1 dose schedule (with vaccine doses administered at 3, 5 months of age and a booster dose at 15 months).Citation62 In addition, to reduce carriage by adolescents, a single dose of MenACWY vaccine is provided at 11 years of age.Citation62 Active surveillance is ongoing to closely monitor the impact of this national immunization program.
UK
In the UK, the almost 10-fold increase from 2008/09 to 2014/15 in the number of MenW cases (19 and 170 cases, respectively) was initially observed in the elderly (≥ 65 years old) but rapidly expanded across all age groups, particularly in children aged ≤ 4 years and 15–19-year old adolescents.Citation32 This increase led to a decision to offer the MenACWY conjugate vaccine to all adolescents aged from 14–18 years from August 2015.Citation34 The program set out to offer the vaccine to the entire cohort during 2015–17, with priority given to secondary school graduates in 2015 because of the recognized high risk of IMD for students about to live in dormitories or university residency halls.Citation78 Furthermore, the monovalent MenC vaccination at 14 years of age in the existing vaccination program was replaced by MenACWY and various catch-up programs were targeted at specific groups (adolescents and university entrants 18–25 years of age).Citation34
After 1 year, a vaccination coverage rate of ~37% had been attained and a reduction of 69% in the number of MenW cases in this cohort was observed, using trend analysis to compare with the predicted number of cases; the absolute impact was lower, with 218 meningococcal infections still reported in individuals of all ages in 2015–2016.Citation42 All confirmed MenW cases (6 among ~ 650,000 individuals) reported in the population eligible for vaccination occurred in unvaccinated individuals.Citation42 In a school-based vaccination program undertaken in adolescents, targeting 13–15-year-olds born between September 2000 and August 2002, coverage rates of routinely offered MenACWY vaccination amounting to 77–84% have been achievedCitation79; the program aimed to provide direct protection to the vaccinated cohort and indirect protection to other unvaccinated age group by reducing MenW-carriage.Citation80 In a recent cross-sectional evaluation of MenW carriage in 1st year university students in the UK, MenW carriage increased over a 6-month period in those studied,Citation81 while vaccination coverage in the student population increased from 31% to 70% over the same period.Citation82 The increase in MenW carriage was due to expansion of the hypervirulent P1.5,2:F1-1:ST-11 UK 2013 strain; these initial data suggested that the MenACWY vaccine did not prevent carriage of the MenW strain in adolescents.Citation81–Citation83 The potential for MenACWY to induce herd protection against MenW strains in the wider population in the UK and elsewhere is as yet uncertain and will require further study.
Australia
In response to the overall increase in MenW cases since 2014, 5 of 6 states have already implemented temporary, free MenACWY vaccination programs for 15–19 year old adolescents (only 17–18-year olds are targeted in New South Wales).Citation51 The programs are planned to last until December 2018 in Victoria and Western Australia, April 2018 in Tasmania, and May 2018 in Queensland. Furthermore, following the MenW-outbreak ongoing since July 2017 in Central Australia particularly affecting indigenous Australians, several states are currently implementing time-limited MenACWY vaccination programs for affected communities.Citation51 Thus, in certain regions, the initial program was expanded to include 1 dose of a quadrivalent meningococcal vaccine for all children 12–< 24 months of age in the Northern Territory,Citation84 children 1–< 5 years in Western Australia,Citation85 and for 1–19-year-olds in South Australia.Citation86 As an urgent response to the recent MenW cases reported in Tasmania, MenACWY vaccination will be offered to all individuals aged between 6 weeks and 20 years, as of August 2018.Citation52 Additionally, as of July 2018, the national immunization program will include a routine, funded, single dose of MenACWY vaccine at 1 year of age.Citation64
The Netherlands
In the Netherlands, the increase in MenW casesCitation43 has led to changes in the national immunization schedule; from May 1, 2018 onwards, MenACWY vaccination is replacing MenC vaccination that was recommended at 14 month of age and, will be offered to all children 13–14 years of age from October 2018.Citation65
Other countries
To date, no other country has launched reactive vaccination campaigns against MenW; however, strict surveillance has been widely instituted and possible vaccination strategies are being considered, based on surveillance trends. MenACWY vaccines are currently approved/licensed for use in different ages in several other regions and countries.Citation16,Citation17,Citation74 While many countries around the world recommend MenACWY vaccination for different at-risk populations, travelers to endemic countries or in case of outbreaks,Citation74 several countries also include them in their national immunization plan, to control IMD caused by four out of the six clinically-relevant meningococcal serogroups worldwide. In Austria, MenACWY vaccination is offered to children 10–13 years of age and as a booster dose to adolescents vaccinated with MenC during infancyCitation66,Citation67 since 2012. Since the year 2001 MenACWY has also been offered to adolescents in Greece (11–12 years of age, since 2011),Citation70,Citation71 and Italy (12–18 years of age, since 2017),Citation72 while in the Saudi Arabia, the vaccine has been introduced in the national vaccination schedule since 2013 (a 2-dose series at 9 and 12 months in infants, 2 doses administered 3 months apart for children ≥6 months to ≤2 years of age and a single dose in 2–5-year-olds).Citation73 In the US, MenACWY is included in the routine vaccination program for adolescents since 2013, as a single dose at 11–12 years, followed by a booster dose at age 16.Citation8 In Canada, as of 2017, MenC or MenACWY are recommended for the adolescent booster in all provinces and territories, except Manitoba and Quebec.Citation68
Discussion
Considerable increases in the incidence of MenW and/or in the proportion of all IMD cases caused by MenW have, so far, been seen in considerable number of countries in Europe, South America, Australia and some parts of sub-Saharan Africa, predominantly caused by closely similar strains belonging to the hypervirulent cc11 strain. All the affected countries have established surveillance and, until now, 5 of the countries (Chile, UK, Argentina, Australia, and the Netherlands) have implemented reactive vaccination campaigns directly addressing the increase in MenW-IMD incidence. Other countries have also introduced quadrivalent conjugate vaccines in their immunization program to protect against all-cause meningococcal disease. Surveillance is key to the control of MenW and IMD incidence, and active systems like those in place in Northern America,Citation87 the UKCitation88 or the NetherlandsCitation44 are more effective, allowing rapid mapping of emerging disease trends and fast disease control response measures.Citation13 Moreover, for all meningococcal infections, in addition to notification of clinical cases using clear and uniform case definitions, surveillance should include laboratory reportingCitation89; this is particularly relevant for MenW, in view of the distinct clinical manifestations of the circulating hypervirulent strains. The Global Meningococcal Initiative recently advocated for ongoing surveillance and expansion of vaccination programs, together with recommendations to enable DNA analysis methods (like multi-locus sequence typing and whole-genome sequencing) to further characterize isolates causing IMD.Citation3
Determining optimal vaccination strategies is complicated, in particular in countries with relatively low incidence of the disease. One important factor impacting the choice of a vaccination strategy is that carriage rates and disease incidence are both age-related but peaking at differing ages. In a meta-analysis of carriage data from countries where MenB and MenC are predominant, overall meningococcal carriage prevalence was shown to reach its highest at 23.7% in 19 year-olds versus 4.5% in infants and 7.8% in 50 year-oldsCitation54 whereas IMD incidence peaks in infancy and young children.Citation17 Although the impact of MenW carriage on MenW-caused incidence is yet to be elucidated, data from Chile for the year 2013 indicated that carriage of MenW hypervirulent strains among unvaccinated children and adolescents 9–19 years of age is low, and is not correlated with the increase in the incidence of IMD caused by the MenW strain.Citation90 In the UK, early data in vaccinated adolescents also suggested no impact of vaccination on MenW carriage.Citation83
In Chile, a strategy of aiming the vaccination campaign at the most susceptible age groups to be infected by MenW was effective in reducing the incidence and mortality in the targeted age groups. In Argentina, a strategy targeting both infants and adolescents was implemented, but an assessment of the effects of this combination strategy is not yet available as the vaccination campaign started in 2017. In the UK, the strategy selected was to target the vaccination campaign at the age groups with the highest carrier rates, considered to be the principal responsible for onward transmission. A rapid reduction in the number of MenW cases of 69% as compared to the number predicted by trend analysis was observed in the vaccinated age groupCitation42; however, increase in MenW carriage in university students has been measured despite high level of vaccine coverage. Further research is required to determine if there is potential for population-wide herd protection.Citation82
The possibility that a MenB protein vaccine may also afford some protection against MenW has been discussed.Citation91 The MenW:cc11 strain causing IMD in the UK possesses alleles of Neisseria adhesin A (NadA) 2/3 peptide variants and neisserial heparin binding antigen (NHBA) peptide 29. NadA and NHBA are 2 of the 4 components of the 4CMenB vaccine licensed for routine immunizations in the UK and therefore the vaccine could potentially induce cross-protection,Citation91 especially in case of NadA, for which the variant contained in 4CMenB vaccine was already predicted to be highly cross-reactive with the MenW NadA variant.Citation92
Offering one dose of MenACWY conjugate vaccine as a booster to individuals primed with MenC vaccine could have the advantage of maintaining herd protection against MenC, while also providing broader protection against other meningococcal serogroups.Citation17 This strategy has already been initiated by the UK, Italy, Greece, Austria,Citation93 the USCitation8 and CanadaCitation68 in reaction to the steep increase of IMD incidence.
Conclusion
The increased incidence and spread of MenW in different parts of the world over approximately the last decade warrants accurate surveillance and prompt action from national health authorities. Positive evidence supporting the effectiveness of MenACWY vaccination campaigns in the control of MenW-IMD in different age groups is emerging from a number of countries worldwide. Whether high levels of vaccination coverage among adolescents, typically carriers of N. meningitidis, will result in herd protection is still unconfirmed. However, due to the rapidly-evolving epidemiology of MenW globally, the diversity and virulence of MenW strain variants and the difference in impacted age groups, a responsive vaccination strategy that is tailored to local and regional epidemiology and available resources, will most likely be required.
Disclosure of potential conflicts of interest
RB’s institution received grants from all vaccine companies operating in Australia for the conduct of several clinical trials, for speaker’s honoraria, for participation in advisory boards and for support of the travel costs linked to conferences and meetings attendances. MN, JW, and VA are employees of the GSK group of companies. MN, JW and VA hold shares in the GSK group of companies as part of their employee remuneration. AG has nothing to disclose.
Authors’ contributions
All authors reviewed and commented critically drafts of the manuscript for important intellectual content and gave final approval to submit for publication. The corresponding author had final responsibility to submit for publication. Drafts were developed by a professional publication writer according to the recommendations, documentation, and outline provided by the lead author.
Trademark
Bexsero and Menveo are trademarks owned by the GSK group of companies.
Supplemental Material
Download MS Word (68.6 KB)Acknowledgments
The authors would like to thank Niels Neymark and Petronela M. Petrar (XPE Pharma & Science c/o GSK) for medical writing support and Maria Ana de la Grandiere (XPE Pharma & Science c/o GSK) for manuscript coordination and editorial support.
Supplementary material
Supplemental data can be accessed here
Additional information
Funding
References
- World Health Organization. Immunization, vaccines and biologicals. Meningococcal meningitis; Updated April 2015 [accessed 2018 Jan 15]. http://www.who.int/immunization/diseases/meningitis/en/.
- Edmond K, Clark A, Korczak VS, Sanderson C, Griffiths UK, Rudan I. Global and regional risk of disabling sequelae from bacterial meningitis: a systematic review and meta-analysis. Lancet Infect Dis. 2010;10(5):317–328. doi:10.1016/s1473-3099(10)70048-7.
- Borrow R, Alarcón P, Carlos J, Caugant DA, Christensen H, Debbag R, De Wals P, Echániz-Aviles G, Findlow J, Head C, et al. The Global Meningococcal Initiative: global epidemiology, the impact of vaccines on meningococcal disease and the importance of herd protection. Expert Rev Vaccines. 2017;16(4):313–328. doi:10.1080/14760584.2017.1258308.
- European Centre for Disease Prevention and Control. Invasive meningococcal disease. In: ECDC. Annual epidemiological report for 2015. Stockholm: ECDC; 2017 [ accessed 2018 Jan 10]. https://ecdc.europa.eu/sites/portal/files/documents/AER_for_2015-meningococcal-disease.pdf.
- Centers for Disesease Control and Prevention. Enhanced meningococcal disease surveillance report; 2016 [ accessed 2018 Jan 14]. https://www.cdc.gov/meningococcal/downloads/NCIRD-EMS-Report.pdf.
- Borrow R, Lee JS, Vazquez JA, Enwere G, Taha MK, Kamiya H, Kim HM, Jo DS; Global Meningococcal Initiative. Meningococcal disease in the Asia-Pacific region: findings and recommendations from the Global Meningococcal Initiative. Vaccine. 2016;34(48):5855–5862. doi:10.1016/j.vaccine.2016.10.022.
- Safadi MA, O’Ryan M, Valenzuela Bravo MT, Brandileone MC, Gorla MC, de Lemos AP, Moreno G, Vazquez JA, Lopez EL, Taha MK, et al. The current situation of meningococcal disease in Latin America and updated Global Meningococcal Initiative (GMI) recommendations. Vaccine. 2015;33(48):6529–6536. doi:10.1016/j.vaccine.2015.10.055.
- Cohn AC, MacNeil JR, Clark TA, Ortega-Sanchez IR, Briere EZ, Meissner HC, Baker CJ, Messonnier NE; Centers for Disease Control and Prevention (CDC). Prevention and control of meningococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2013;62(RR–2):1–28.
- Harrison LH. Epidemiological profile of meningococcal disease in the United States. Clin Infect Dis. 2010;50(Suppl 2):S37–44. doi:10.1086/648963.
- Centers for Disease Control and Prevention. Epidemiology and prevention of vaccine-preventable diseases. In: Hamborsky J, Kroger A, Wolfe S, editors. Chapter 14: meningococcal disease. Washington D.C.: Public Health Foundation; 2015, p. 235.
- Vieusseux M. Memoire sur la maladie qui a regne a Geneve au printemps de 1805. J Med Chir Pharmacol. 1805;11:163–182.
- Weichselbaum A. Ueber die Aetiologie der akuten meningitis cerebrospinalis. Fortschr Med. 1887;5:573–583.
- Harrison LH, Trotter CL, Ramsay ME. Global epidemiology of meningococcal disease. Vaccine. 2009;27(Suppl 2):B51–63. doi:10.1016/j.vaccine.2009.04.063.
- Pelton SI. The global evolution of meningococcal epidemiology following the introduction of meningococcal vaccines. J Adolesc Health. 2016;59(2 Suppl):S3–S11. doi:10.1016/j.jadohealth.2016.04.012.
- Safadi MA, Gonzalez-Ayala S, Jakel A, Wieffer H, Moreno C, Vyse A. The epidemiology of meningococcal disease in Latin America 1945-2010: an unpredictable and changing landscape. Epidemiol Infect. 2013;141(3):447–458. doi:10.1017/s0950268812001689.
- Crum-Cianflone N, Sullivan E. Meningococcal vaccinations. Infect Dis Ther. 2016;5(2):89–112. doi:10.1007/s40121-016-0107-0.
- Vetter V, Baxter R, Denizer G, Safadi MA, Silfverdal SA, Vyse A, Borrow R. Routinely vaccinating adolescents against meningococcus: targeting transmission & disease. Expert Rev Vaccin. 2016;15(5):641–658. doi:10.1586/14760584.2016.1130628.
- Broker M, Bukovski S, Culic D, Jacobsson S, Koliou M, Kuusi M, Simoes MJ, Skoczynska A, Toropainen M, Taha MK, et al. Meningococcal serogroup Y emergence in Europe: high importance in some European regions in 2012. Hum Vaccin Immunother. 2014;10(6):1725–1728. doi:10.4161/hv.28206.
- Rosenstein NE, Perkins BA, Stephens DS, Lefkowitz L, Cartter ML, Danila R, Cieslak P, Shutt KA, Popovic T, Schuchat A, et al. The changing epidemiology of meningococcal disease in the United States, 1992–1996. J Infect Dis. 1999;180(6):1894–1901. doi:10.1086/315158.
- Lingappa JR, Al-Rabeah AM, Hajjeh R, Mustafa T, Fatani A, Al-Bassam T, Badukhan A, Turkistani A, Makki S, Al-Hamdan N, et al. Serogroup W-135 meningococcal disease during the Hajj, 2000. Emerg Infect Dis. 2003;9(6):665–671. doi:10.3201/eid0906.020565.
- Evans JR, Artenstein MS, Hunter DH. Prevalence of meningococcal serogroups and description of three new groups. Am J Epidemiol. 1968;87(3):643–646.
- Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB, Jolley KA, Corton C, Care R, Poolman JT, Zollinger WD, et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis. 2013;19(4):566–573. doi:10.3201/eid1904.111799.
- Mustapha MM, Marsh JW, Harrison LH. Global epidemiology of capsular group W meningococcal disease (1970-2015): multifocal emergence and persistence of hypervirulent sequence type (ST)-11 clonal complex. Vaccine. 2016;34(13):1515–1523. doi:10.1016/j.vaccine.2016.02.014.
- Taha MK, Achtman M, Alonso JM, Greenwood B, Ramsay M, Fox A, Gray S, Kaczmarski E. Serogroup W135 meningococcal disease in Hajj pilgrims. Lancet. 2000;356(9248):2159. doi:10.1016/s0140-6736(00)03502-9.
- Aguilera JF, Perrocheau A, Meffre C, Hahne S; W135 Working Group. Outbreak of serogroup W135 meningococcal disease after the Hajj pilgrimage, Europe, 2000. Emerg Infect Dis. 2002;8(8):761–767. doi:10.3201/eid0805.010422.
- Issack MI, Ragavoodoo C. Hajj-related Neisseria meningitidis serogroup W135 in Mauritius. Emerg Infect Dis. 2002;8(3):332–334. doi:10.3201/eid0803.010372.
- Kilic A, Urwin R, Li H, Saracli MA, Stratton CW, Tang YW. Clonal spread of serogroup W135 meningococcal disease in Turkey. J Clin Microbiol. 2006;44(1):222–224. doi:10.1128/jcm.44.1.222-224.2006.
- Nicolas P, Ait M’barek N, Al-Awaidy S, Al Busaidy S, Sulaiman N, Issa M, Mahjour J, Molling P, Caugant DA, Olcen P, et al. Pharyngeal carriage of serogroup W135 Neisseria meningitidis in Hajjees and their family contacts in Morocco, Oman and Sudan. APMIS. 2005;113(3):182–186. doi:10.1111/j.1600-0463.2005.apm1130305.x.
- Ladhani SN, Beebeejaun K, Lucidarme J, Campbell H, Gray S, Kaczmarski E, Ramsay ME, Borrow R. Increase in endemic Neisseria meningitidis capsular group W sequence type 11 complex associated with severe invasive disease in England and Wales. Clin Infect Dis. 2015;60(4):578–585. doi:10.1093/cid/ciu881.
- Abad R, López EL, Debbag R, Vázquez JA. Serogroup W meningococcal disease: global spread and current affect on the Southern Cone in Latin America. Epidemiol Infect. 2014;142(12):2461–2470. doi:10.1017/s0950268814001149.
- Lucidarme J, Hill DM, Bratcher HB, Gray SJ, Du Plessis M, Tsang RS, Vazquez JA, Taha MK, Ceyhan M, Efron AM, et al. Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage. J Infect. 2015;71(5):544–552. doi:10.1016/j.jinf.2015.07.007.
- Campbell H, Saliba V, Borrow R, Ramsay M, Ladhani SN. Targeted vaccination of teenagers following continued rapid endemic expansion of a single meningococcal group W clone (sequence type 11 clonal complex), United Kingdom 2015. Euro Surveill. 2015;20:28. doi:10.2807/1560-7917.ES2015.20.28.21188.
- Campbell H, Parikh SR, Borrow R, Kaczmarski E, Ramsay ME, Ladhani SN. Presentation with gastrointestinal symptoms and high case fatality associated with group W meningococcal disease (MenW) in teenagers, England, July 2015 to January 2016. Euro Surveill. 2016;21:12. doi:10.2807/1560-7917.es.2016.21.12.30175.
- Ladhani SN, Ramsay M, Borrow R, Riordan A, Watson JM, Pollard AJ. Enter B and W: two new meningococcal vaccine programmes launched. Arch Dis Child. 2016;101(1):91–95. doi:10.1136/archdischild-2015-308928.
- 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;20(Suppl 1):S58–67. doi:10.1016/S0264-410X(01)00299-7.
- Valenzuela MT, Moreno G, Vaquero A, Seoane M, Hormazabal JC, Bertoglia MP, Gallegos D, Sotomayor V, Diaz J. [Emergence of W135 meningococcal serogroup in Chile during 2012]. Rev Med Chil. 2013;141(8):959–967. doi:10.4067/s0034-98872013000800001.
- Weidlich L, Baethgen LF, Mayer LW, Moraes C, Klein CC, Nunes LS, Rios Sda S, Kmetzsch CI, Rossetti ML, Zaha A. High prevalence of Neisseria meningitidis hypervirulent lineages and emergence of W135: P1.5,2:ST-11clone in Southern Brazil. J Infect. 2008;57(4):324–331. doi:10.1016/j.jinf.2008.07.014.
- Araya P, Fernandez J, Del Canto F, Seoane M, Ibarz-Pavon AB, Barra G, Pidal P, Diaz J, Hormazabal JC, Valenzuela MT. Neisseria meningitidis ST-11 clonal complex, Chile 2012. Emerg Infect Dis. 2015;21(2):339–341. doi:10.3201/eid2102.140746.
- Sorhouet-Pereira C, Efron A, Gagetti P, Faccone D, Regueira M, Corso A, Gabastou JM, Ibarz-Pavon AB; Argentinean SIREVA II Working Group. Phenotypic and genotypic characteristics of Neisseria meningitidis disease-causing strains in Argentina, 2010. PLoS One. 2013;8(3):e58065. doi:10.1371/journal.pone.0058065.
- Ibarz-Pavon AB, Lemos AP, Gorla MC, Regueira M, Gabastou JM; SIREVA Working Group II. Laboratory-based surveillance of Neisseria meningitidis isolates from disease cases in Latin American and Caribbean countries, SIREVA II 2006–2010. PLoS One. 2012;7(8):e44102. doi:10.1371/journal.pone.0044102.
- Dirección de Control de Enfermedades Inmunoprevenibles. Fundamentos de la introducción de la vacuna tetravalente (ACYW) conjugada contra meningococco al Calendario Nacional de Inmunizaciones. Argentina. 2016 [ accessed 2016 Jan 15]. http://www.msal.gob.ar/images/stories/bes/graficos/0000000927cnt-2016-12_lineamientos-meningo.pdf.
- Campbell H, Edelstein M, Andrews N, Borrow R, Ramsay M, Ladhani S. Emergency meningococcal ACWY vaccination program for teenagers to control group W meningococcal disease, England, 2015-2016. Emerg Infect Dis. 2017;23(7):1184–1187. doi:10.3201/eid2307.170236.
- Knol MJ, Ruijs H, De Melker H, Sanders L, Van der Ende A. Increase in invasive serogroup W meningococcal disease since 2015 in the Netherlands. 14th Congress of the EMGM, European Meningococcal and Haemophilus Disease Society; 2017 Sept 18–21; Prague, Czech Republic.
- Knol MJ, Hahne SJM, Lucidarme J, Campbell H, de Melker HE, Gray SJ, Borrow R, Ladhani SN, Ramsay ME, van der Ende A. Temporal associations between national outbreaks of meningococcal serogroup W and C disease in the Netherlands and England: an observational cohort study. Lancet Public Health. 2017;2(10):e473–e82. doi:10.1016/s2468-2667(17)30157-3.
- Eriksson L, Thulin Hedberg S, Jacobsson S, Fredlund H, Molling P, Stenmark B. Whole genome sequencing of the emerging invasive Neisseria meningitidis serogroup W in Sweden. J Clin Microbiol. 2018. doi:10.1128/jcm.01409-17.
- Stefanelli P, Fazio C, Neri A, Boros S, Renna G, Pompa MG; National Surveillance System Collaborative Centers. Changing epidemiology of infant meningococcal disease after the introduction of meningococcal serogroup C vaccine in Italy, 2006-2014. Vaccine. 2015;33(31):3678–3681. doi:10.1016/j.vaccine.2015.06.032.
- Hong E, Barret AS, Terrade A, Denizon M, Antona D, Aouiti-Trabelsi M, Deghmane AE, Parent Du Chatelet I, Levy-Bruhl D, Mk T. Clonal replacement and expansion among invasive meningococcal isolates of serogroup W in France. J Infect. 2017;76(2):149–158. doi:10.1016/j.jinf.2017.10.015.
- Abad R, Navarro C, Vazquez JA. Increase of serogroup W meningococcal invasive strains in Spain: genomic analysis. 14th Congress of the EMGM, European Meningococcal and Haemophilus Disease Society; 2017 Sept 18–21; Prague, Czech Republic.
- Australian Department of Health. Invasive meningococcal disease national surveillance report. With a focus on MenW. 2017 Dec. 31 [accessed 2018 Mar 4]. http://www.health.gov.au/internet/main/publishing.nsf/Content/5FEABC4B495BDEC1CA25807D001327FA/$File/31-Dec17-IMD-Surveillance-report.pdf.
- National Centre for Immunisation. Research&Surveillance. NCIRS fact sheet. Meningocooccal vaccines for Australians: information for immunisation providers; 2018 Feb [accessed 2018 Mar 4]. http://www.ncirs.edu.au/assets/provider_resources/fact-sheets/Meningococcal-vaccines-FactSheet-Feb-2018.pdf.
- Australian Department of Health. Communicable diseases information. Meningococcal W disease: information for health professionals; 2017 [ accessed 2018 Jan 10]. http://www.health.gov.au/internet/main/publishing.nsf/Content/ohp-meningococcal-W-info-hp.htm
- Tasmanian Government. Department of Health. Free meningococcal ACWY vaccine for all young people in Tasmania; 2018 [ accessed 2018 Aug 30]. https://www.dhhs.tas.gov.au/__data/assets/pdf_file/0009/347508/FAQs_2018_0830_Final.pdf.
- Martin NV, Ong KS, Howden BP, Lahra MM, Lambert SB, Beard FH, Dowse GK, Saul N; Communicable Diseases Network Australia MenW Working Group. Rise in invasive serogroup W meningococcal disease in Australia 2013-2015. Commun Dis Intell Q Rep. 2016;40(4):E454–E9.
- Christensen H, May M, Bowen L, Hickman M, Trotter CL. Meningococcal carriage by age: a systematic review and meta-analysis. Lancet Infect Dis. 2010;10(12):853–861. doi:10.1016/s1473-3099(10)70251-6.
- Borrow R, Abad R, Trotter C, van der Klis FR, Vazquez JA. Effectiveness of meningococcal serogroup C vaccine programmes. Vaccine. 2013;31(41):4477–4486. doi:10.1016/j.vaccine.2013.07.083.
- Kaaijk P, van der Ende A, Berbers G, van Den Dobbelsteen GP, Rots NY. Is a single dose of meningococcal serogroup C conjugate vaccine sufficient for protection? experience from the Netherlands. BMC Infect Dis. 2012;12:35. doi:10.1186/1471-2334-12-35.
- Andrade AL, Minamisava R, Tomich LM, Lemos AP, Gorla MC, de Cunto Brandileone MC, Domingues CMS, de Moraes C, Policena G, Bierrenbach AL, et al. Impact of meningococcal C conjugate vaccination four years after introduction of routine childhood immunization in Brazil. Vaccine. 2017;35(16):2025–2033. doi:10.1016/j.vaccine.2017.03.010.
- Brazil. [Information on changes to the national vaccination calendar for the year 2017] [ accessed 2018 Mar 4]. http://portalsaude.saude.gov.br/images/pdf/2016/outubro/20/Nota-Informativa-311-Calendario-Nacional-de-Vacinacao-2017.pdf.
- Epidemic meningitis control in countries of the African meningitis belt, 2016. weekly epidemiological record of the World Health Organization. 2017;92(13):145–154.
- Villena R, Santolaya ME. Chilean experience with serogroup W outbreak and meningococcal ACWY conjugate vaccines. Abstract for the 14th Congress of the EMGM; 2017 Sept 18–21; Prague, Czech Republic.
- Ministry of Health, Chile. Calendarios de Vacunación [ accessed 2018 Sept 10]. http://www.enfermeriaaps.com/portal/wp-content/uploads/2018/03/Calendario-vacunas-chile-2018.jpg.
- Ministry of Health, Argentina. Glosario de Salud. Vacuna contra el meningococo [ accessed 2018 Jan 14]. https://www.argentina.gob.ar/salud/glosario/vacunameningococo.
- Public Health England. Guidance on the prevention and management of meningococcal meningitis and septicaemia in higher education institutions; 2016 [ accessed 2018 Sept 10]. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/582511/MenACWY_HEI_Guidelines.pdf.
- National Centre for Immunisation Research & Surveillance. Meningococcal vaccines FactSheet; 2018 Aug [accessed 2018 Aug 31]. http://www.ncirs.edu.au/assets/provider_resources/fact-sheets/meningococcal-vaccines-fact-sheet.pdf.
- Tweede Kamer der Staten-Generaal, vergaderjaar 2017–2018, 32 793, nr. 279 [ accessed 2018 Mar 5]. https://www.tweedekamer.nl/kamerstukken/brieven_regering/detail?id=2017Z12606&did=2017D26519.
- Impfplan Österreich 2018 [ accessed 2018 Mar 3]. https://www.bmgf.gv.at/cms/home/attachments/3/3/1/CH1100/CMS1515753153756/impfplan_2018.pdf.
- Impfplan Österreich 2012 [ accessed 2018 Sept 14]. http://www.doc-for-kids.at/uploads/lexikon_pdf/impfplan_2012.pdf
- Robinson JL. Update on invasive meningococcal vaccination for Canadian children and youth. Paediatr Child Health. 2018;23(1):e1–e4. doi:10.1093/pch/pxx162.
- Public Health Agency of Canada. Canada’s provincial and territorial routine (and catch-up) vaccination routine schedule programs for infants and children; 2018 [ accessed 2018 Sept 10]. https://www.canada.ca/content/dam/phac-aspc/documents/services/provincial-territorial-immunization-information/childhood_%20schedule.pdf.
- Safadi MA, McIntosh ED. Epidemiology and prevention of meningococcal disease: a critical appraisal of vaccine policies. Expert Rev Vaccines. 2011;10(12):1717–1730. doi:10.1586/erv.11.159.
- Greek Paediatric Society, 2014 [accessed 2018 Jan 10]. http://vaccines.e-child.gr/sistasis/sistasis-ellinikis-pediatrikis-eterias/.
- Piano nazionale prevenzione vaccinale 2017–2019 [accessed 2018 Jan 10. http://www.salute.gov.it/imgs/C_17_pubblicazioni_2571_allegato.pdf.
- Ministry of Health, Kingdom of Saudi Arabia, 2014. Mengingococcal Meningitis [accessed 2018 Jan 10]. https://www.moh.gov.sa/en/HealthAwareness/EducationalContent/Diseases/Infectious/Pages/MeningococcalMeningitis.aspx.
- World Health Organization. WHO vaccine-preventable diseases: monitoring system. 2018 global summary [accessed 2018 Aug 10]. http://apps.who.int/immunization_monitoring/globalsummary/schedules
- Safadi MA, Berezin EN, Arlant LH. Meningococcal disease: epidemiology and early effects of immunization programs. J Pediatric Infect Dis Soc. 2014;3(2):91–93. doi:10.1093/jpids/piu027.
- Enfermedad meningocócica (CIE 10: A39). Semana epidemiológica 1-39 (1 de enero al 30 de septiembre). Chile, 2017. Boletín Epidemiológico Trimestral. 2018;113(3) [accessed 2018 Mar 8]. http://epi.minsal.cl/wp-content/uploads/2017/10/BET_MENINGITIS_OCTUBRE_2017.pdf.
- Vigilancia de laboratorio enfermedad invasora Neisseria meningitidis 2011–2015. Vol. 5 (10). Chile: Boletín del, Public Health Institute of Chile (Instituto de Salud Pública de Chile); 2015 [accessed 2018 Aug 31]. http://www.ispch.cl/sites/default/files/Boletin_NeisseriaMeningitidis.pdf.
- Bruce MG, Rosenstein NE, Capparella JM, Shutt KA, Perkins BA, Collins M. Risk factors for meningococcal disease in college students. JAMA. 2001;286(6):688–693.
- Public Health England. Preliminary vaccine coverage for the school based meningococcal ACWY (MenACWY) adolescent vaccination programme in England, September 1, 2015 to August 31, 2016. Heal Prot Rep 2016;10 [accessed 2017 Jan 14]. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/578772/hpr4416_menacwy-vc.pdf.
- Public Health England. Meningococcal ACWY (MenACWY) vaccination programme; 2016 [accessed 2018 Aug 30]. https://www.gov.uk/government/collections/meningococcal-acwy-menacwy-vaccination-programme.
- Oldfield NJ, Cayrou C, Mak A, Aaa A-R, Green LR, Dada S, Steels OD, Stirrup C, Wanford J, Atwah BAY, et al. Rise in group W meningococcal carriage in university students, United Kingdom. Emerg Infect Dis. 2017;23(6):1009–1011. doi:10.3201/eid2306.161768.
- Turner DP, Oldfield NJ, Bayliss CD. University vaccine campaign increases meningococcal ACWY vaccine coverage. Public Health. 2017;145:1–3. doi:10.1016/j.puhe.2016.12.010.
- Oldfield NJ, Green LR, Parkhill J, Bayliss CD, Turner DPJ. Limited impact of adolescent meningococcal ACWY vaccination on Neisseria meningitidis serogroup W carriage in university students. J Infect Dis. 2018;217(4):608–616. doi:10.1093/infdis/jix596.
- Northern Territory Health. Menningococcal ACWY vaccination schedule; 2017 Oct [accessed 2018 Mar 3]. http://hdl.handle.net/10137/1395.
- Government of Western Australia. Department of Health. Mengococcal ACWY vaccine [accessed 2018 Mar 3]. http://healthywa.wa.gov.au/Articles/J_M/Meningococcal-vaccine.
- Government of South Australia. SA Health. Meningococcal W outbreak in APY lands; Media releases, 2017 Oct 5 [accessed 2018 Mar 3]. http://www.sahealth.sa.gov.au/wps/wcm/connect/Public+Content/SA+Health+Internet/About+us/News+and+media/Media+releases/Meningococcal+W+outbreak+in+APY+lands.
- Baccarini C, Ternouth A, Wieffer H, Vyse A. The changing epidemiology of meningococcal disease in North America 1945-2010. Hum Vaccin Immunother. 2013;9(1):162–171. doi:10.4161/hv.22302.
- Gray SJ, Trotter CL, Ramsay ME, Guiver M, Fox AJ, Borrow R, Mallard RH, Kaczmarski EB; Meningococcal Reference Unit. Epidemiology of meningococcal disease in England and Wales 1993/94 to 2003/04: contribution and experiences of the Meningococcal Reference Unit. J Med Microbiol. 2006;55(Pt 7):887–896. doi:10.1099/jmm.0.46288-0.
- Commission implementing Decision of 8 August 2012 amending Decision 2002/253/EC laying down case definitions for reporting communicable diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council (notified under document C(2012) 5538) (1). European Commission. 2012;L 262/1:55. doi:10.3000/19770677.L_2012.262.eng.
- Rubilar PS, Barra GN, Gabastou J-M, Alarcón P, Araya P, Hormazábal JC, Fernandez J. Increase of Neisseria meningitidis W: cc11 invasive disease in Chile has no correlation with carriage in adolescents. PLoS one. 2018;13(3):e0193572. doi:10.1371/journal.pone.0193572.
- Ladhani SN, Giuliani MM, Biolchi A, Pizza M, Beebeejaun K, Lucidarme J, Findlow J, Ramsay ME, Borrow R. Effectiveness of meningococcal B vaccine against endemic hypervirulent Neisseria meningitidis W strain, England. Emerg Infect Dis. 2016;22(2):309–311. doi:10.3201/eid2202.150369.
- Comanducci M, Bambini S, Brunelli B, Adu-Bobie J, Aricò B, Capecchi B, Giuliani MM, Masignani V, Santini L, Savino S, et al. NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med. 2002;195(11):1445–1454.
- European Centre for Disease Prevention and Control. Meningococcal disease: recommended vaccinations [accessed 2018 Mar 5]. https://vaccine-schedule.ecdc.europa.eu/Scheduler/ByDisease?SelectedDiseaseId=48&SelectedCountryIdByDisease=−1.
- Koutangni T, Boubacar Mainassara H, Mueller JE. Incidence, carriage and case-carrier ratios for meningococcal meningitis in the African meningitis belt: a systematic review and meta-analysis. PLoS One. 2015;10(2):e0116725. doi:10.1371/journal.pone.0116725.
- MacNeil JR, Medah I, Koussoube D, Novak RT, Cohn AC, Diomande FV, Yelbeogo D, Kambou JL, Tarbangdo TF, Ouedraogo-Traore R, et al. Neisseria meningitidis serogroup W, Burkina Faso, 2012. Emerg Infect Dis. 2014;20(3):394–399. doi:10.3201/eid2003.131407.
- Lingani C, Bergeron-Caron C, Stuart JM, Fernandez K, Djingarey MH, Ronveaux O, Schnitzler JC, Perea WA. Meningococcal meningitis surveillance in the African Meningitis Belt, 2004–2013. Clin Infect Dis. 2015;61(Suppl 5):S410–5. doi:10.1093/cid/civ597.
- Carville KS, Stevens K, Sohail A, Franklin LJ, Bond KA, Brahmi A, Romanes F, Ong KS. Increase in meningococcal serogroup W disease, Victoria, Australia, 2013–2015. Emerg Infect Dis. 2016;22(10):1785–1787. doi:10.3201/eid2210.151935.
- Araya P, Diaz J, Seoane M, Fernandez J, Terrazas S, Canals A, Vaquero A, Barra G, Hormazabal JC, Pidal P, et al. [Laboratory surveillance for invasive meningococcal disease in Chile, 2006-2012]. Rev Chilena Infectol. 2014;31(4):377–384. doi:10.4067/s0716-10182014000400001.
- Efron AM, Sorhouet C, Salcedo C, Abad R, Regueira M, Vazquez JA. W135 invasive meningococcal strains spreading in South America: significant increase in incidence rate in Argentina. J Clin Microbiol. 2009;47(6):1979–1980. doi:10.1128/jcm.02390-08.
- Stefanelli P, Fazio C, Neri A, Rezza G, Severoni S, Vacca P, Fasciana T, Bisbano A, Di Bernardo F, Giammanco A. Imported and indigenous cases of invasive meningocococcal sisease W:P1.5,2: F1-1:ST-11 in migrants’ reception centers. Italy, June–November 2014. Adv Exp Med Biol. 2016;897:81–83. doi:10.1007/5584_2015_5006.
- Abad R, Vazquez JA. Early evidence of expanding W ST-11 CC meningococcal incidence in Spain. J Infect. 2016;73(3):296–297. doi:10.1016/j.jinf.2016.06.010.