Equity in vaccination policies to overcome social deprivation as a risk factor for invasive meningococcal disease

ABSTRACT

Introduction

Social deprivation is associated with poorer healthcare access. Vaccination is among the most effective public health interventions and achieving equity in vaccination access is vitally important. However, vaccines are often reimbursed by public funds only when recommended in national immunization programs (NIPs), which can increase inequity between high and low socioeconomic groups. Invasive meningococcal disease (IMD) is a serious vaccination-preventable disease. This review focuses on vaccination strategies against IMD designed to reduce inequity.

Areas covered

We reviewed meningococcal epidemiology and current vaccination recommendations worldwide. We also reviewed studies demonstrating an association between social deprivation and risk of meningococcal disease, as well as studies demonstrating an impact of social deprivation on uptake of meningococcal vaccines. We discuss factors influencing inclusion of meningococcal vaccines in NIPs.

Expert opinion

Incorporating meningococcal vaccines in NIPs is necessary to reduce inequity, but insufficient alone. Inclusion provides clear guidance to healthcare professionals and helps to ensure that vaccines are offered universally to all target groups. Beyond NIPs, cost of vaccination should be reimbursed especially for disadvantaged individuals. These approaches should help to achieve optimal protection against IMD, by increasing access and immunization rates, eventually reducing social inequities, and helping to protect those at greatest risk.

PLAIN LANGUAGE SUMMARY

According to the World Health Organization, health equity is achieved when every person has access to the highest attainable health standard regardless of socioeconomic status. Achieving health equity in access to vaccination is particularly important, as vaccination is one of the most effective public health measures. However, vaccines are often paid by public funds only when they are recommended in the country's National Immunization Program. This can increase inequity between the rich and poor, as people with fewer resources are less likely to have private insurance and be aware of vaccines that are not suggested by their doctor. Invasive meningococcal disease is uncommon and unpredictable but a serious infection that can result in long-term disability and can kill within 24 hours. Vaccination is the best measure to prevent it.

We reviewed scientific studies to assess the link between socioeconomic status, the risk of having the disease, and the likelihood of being vaccinated against it. We found that the poorest households have the highest risk of getting the disease and the lowest vaccination rates, even in countries with successful vaccination programs.

Achieving universal vaccination against invasive meningococcal disease is challenging for financial reasons and because the disease is uncommon. Key factors identified to improve vaccination uptake and reduce health inequity are the need for publicly funded vaccines, increased parents’ knowledge of available vaccines, and stronger engagement of vaccination recommendation by doctors/nurses (see also Supplementary Figure 1).

KEYWORDS:

• Equity
• meningococcal disease
• national immunization program (NIP)
• social deprivation
• vaccine

1. Introduction

The World Health Organization (WHO) defines health equity as the absence of unfair, avoidable or remediable differences among groups of people who may be defined socially, economically, demographically, geographically or by other factors such as sex, gender, ethnicity, disability or sexual orientation [1]. According to the WHO, health equity is achieved when everyone can attain their full potential for health and well-being [1].

Numerous studies have demonstrated inequity in access to healthcare, with poorer access linked to lower socioeconomic status and other social disadvantages [2,3]. Vaccination is one of the most effective public health measures [4], and achieving equity in access to vaccination is of vital importance [5]. Limited access to adequate healthcare translates to a disproportionate burden of disease and mortality associated with several vaccine-preventable diseases, not only in low- and middle-income countries, but also among racial and ethnic minority groups from high-income countries [6]. The concept of vaccine equity implies that vaccines should be accessible and allocated equally across all countries globally, independent of their economic status or development [7]. Every human should have the right to enjoy the highest achievable health standard regardless of any condition [7].

Vaccination against several infectious diseases has been shown to reduce the equity gap between high and low socioeconomic groups [8]. For example, in Australia, use of the pneumococcal conjugate vaccine was vital to ‘closing the gap’ during the 2000s in disease rates between indigenous peoples and others [9]. However, in most countries, vaccines are reimbursed by public funds only when they are recommended in the national immunization program (NIP). Vaccines not included in the NIP are not always reimbursed by private insurance, and health insurance coverage varies between countries. This can increase inequity between high and low socioeconomic groups, as the latter are less likely to have private insurance and are also less likely to be aware of vaccinations that are not suggested by their healthcare provider (HCP). Similarly, HCPs are less likely to suggest vaccines not included in the NIP.

Although NIPs help to deliver vaccine access for eligible groups and support improvements in health equity as a result, they do not deliver maximum health equity because not all eligible cohorts access vaccines even within NIPs. The majority of this group are in socially disadvantaged communities. This is the result of many factors including quality of healthcare access, quality of information provided, and historical experience of healthcare among the socially disadvantaged. Lower vaccine uptake in this group perpetuates health inequity. Data from the United Kingdom (UK), for instance, show that the most deprived groups see the largest gaps in vaccine coverage compared with the national average, notably due to deprivation, employment, income/occupation, and education [10]. Increasing uptake within NIPs is therefore a priority for improving health equity. Many people not reaching thresholds for inclusion in NIPs are still at risk of infection, and individuals who can afford and want to pay for vaccine protection are able to do so, assuming that the vaccines are locally available. This could further perpetuate health inequity in socially disadvantaged communities who cannot access vaccine due to cost. Therefore, equity is an important criterion to be considered when establishing NIPs [11].

Invasive meningococcal disease (IMD) is caused by Neisseria meningitidis, a Gram-negative diplococcus bacterium. Of the 12 serogroups identified, six (A, B, C, W, Y and X) are responsible for almost all IMD [12,13]. Although uncommon, the course of IMD is unpredictable, associated with severe long-term sequelae and case-fatality rates as high as 15 − 20% despite treatment [14–16]. Vaccination is currently the most effective strategy for prevention and control of IMD [12]. The first vaccines developed were based solely on capsular polysaccharides against serogroups A, C, W and Y, but these had a short duration of protection, poor immunogenicity in infants and no discernible reduction of carriage among vaccinees [13]. Subsequently, monovalent conjugate vaccines against meningococcal serogroup C (MenC) IMD were produced by conjugating the polysaccharide antigen to a carrier protein, the first of which was launched in 1999 [13]. The first quadrivalent conjugate vaccine (MenACWY) was launched in 2005 [13]. A meningococcal serogroup A (MenA) polysaccharide-tetanus toxoid conjugate vaccine (MenAfriVac, Serum Institute of India) was specifically developed and introduced in the African meningitis belt countries in late 2010 to control MenA IMD [13]. Since 2013, two recombinant vaccines against meningococcal serogroup B (MenB) IMD have become available (4CMenB and MenB-fHbp). 4CMenB contains three main Neisseria protein antigens (Neisseria adhesin A, Neisserial heparin binding antigen, and variant 1 of factor H binding protein [fHbp]) and outer membrane vesicle derived from a New Zealand MenB outbreak strain containing the PorA 1.4 protein [17], while MenBfHbp is composed of two lipidated fHbp antigens representative of the two subfamilies A and B of fHbp [18]. Both vaccines might also offer protection against non-MenB disease [19–21]. Preliminary studies indicate that 4CMenB may also provide protection against N. gonorrhoeae infections [22].

People of all ages are affected by IMD, but the incidence is highest in infants and young children, with a peak in adolescents, and another in older adults in whom case fatality rates are high [15,23,24]. The peak in older adults is usually linked to isolates of serogroups W and Y (MenW and MenY), and older adults are at higher risk of an invasive pulmonary presentation [13,25,26]. Prevention of IMD by vaccination of children has led to a relative increase in the importance of the disease in older adults, but there are no specific recommendations for vaccination of this age group. In France, between 2006 − 2015, 11% of IMD cases were seen in individuals ≥60 years of age, with the highest case fatality rate (20.0%) seen in this age group [27]. By 2019, the proportion of IMD cases occurring in the ≥60 years age group doubled to 22%, again with the highest case fatality rate (23%) [28]. The increase was mainly driven by MenW and MenY, which together accounted for 30% of all IMD in the ≥60 years age group during 2006 − 2015 [27] and 50% during 2019 [28]. A similar burden of IMD in adults, also mainly due to MenY, has been reported in Australia since 2015 [29,30].

Because of the devastating impact of meningitis, the WHO has developed a road map with the aim of defeating the main causes of bacterial meningitis (meningococcus, pneumococcus, Haemophilus influenzae, and group B streptococcus) worldwide by 2030, with equity as a guiding principle [31]. The visionary goals of the road map are to eliminate bacterial meningitis epidemics, to reduce cases of vaccine-preventable bacterial meningitis by 50% and deaths by 70%, and to reduce disability and improve quality of life after meningitis due to any cause [31]. One of the aims of the road map is to achieve high coverage of existing and new vaccines with equal access in all countries, with vaccine coverage of the full immunization schedule maintained or achieved in all countries by 2030. Vaccination goals against meningococcal disease are outlined in Figure 1.

Figure 1. WHO road map goals for vaccination against meningococcal disease Created from the WHO road map of the goals for vaccination against meningococcal disease [31] Men A: meningitis A; MenACWY: meningitis A, C, W or Y; MenACWXY: meningitis A, C, W, X or Y; MenB: meningitis B; WHO: World Health Organization.

This review focuses on how vaccination against IMD associated with any serogroup could help to reduce inequity, via vaccination strategies based on clear recommendations for vaccination and equal access to protection for all, particularly those most at risk. We acknowledge that achieving equity in vaccination can also involve access to medical care facilities that can be particularly difficult to achieve in remote areas and among indigenous populations, the homeless, migrants, and refugees. However, our aim in this work was to focus on vaccines and vaccination strategies.

2. Meningococcal epidemiology and recommendations for vaccination

The incidence of IMD has been slowly declining in Europe since the early 2000s [32]. In 1999, there were 6917 cases reported across countries in the European Union/European Economic Area (EU/EEA), corresponding to a notification rate of 1.63 per 100,000 population [32]. The MenC conjugate vaccine was included in the infant NIP by numerous European countries, starting with the UK in 1999 [13]; countries introducing the vaccine experienced substantial reductions in MenC disease [33–36]. However, from 2013, the incidence of MenW IMD across Europe rose substantially [37,38]. Again, the UK was the first to introduce the MenACWY conjugate vaccine to the NIP in 2015, with a subsequent reduction in incidence of MenW cases [39]. MenB disease has been declining in incidence for the past two decades across Europe, with 4067 cases reported in the EU/EEA in 1999 compared with 1543 cases in 2018 [32], likely as a result of natural secular trends [40]. The UK and Italy introduced MenB vaccination into the NIP in 2015 and 2017, respectively, again resulting in a substantial reduction in MenB disease [20,41]. A systematic review from 2010 to 2017 reported that MenB was the most prevalent serogroup in most European countries (range 23 − 92%) [42].

In the United States of America (USA), IMD cases occur sporadically, although small outbreaks are common [43,44]. MenC was responsible for most outbreaks before the introduction of the MenACWY conjugate vaccine [44], but MenB has recently been the most prevalent serogroup [43]. The incidence of IMD in Latin America varies widely by geographical region, serogroup prevalence and time, with a decreasing trend in disease incidence observed in recent years [23]. Again, vaccine introduction has led to a reduction of cases [45,46].

In Australia, IMD cases peaked during 2002 at 3.5 cases per 100,000 population, falling to 0.6 cases per 100,000 population by 2013 following introduction of the MenC conjugate vaccine in 2003 [30]. Cases rose again to 1.5 per 100,000 in 2017; at this time, MenACWY vaccination was implemented [30]. In response to an outbreak of MenW disease, a change in the NIP in 2018 replaced the MenC vaccine with the MenACWY vaccine [47,48]. In 2020, only 87 confirmed cases were reported, corresponding to 0.3 cases per 100,000 population; MenB accounted for 64% of cases, MenW for 19%, MenY for 16% and MenC for 1% [30]. China experienced a peak incidence of 403 IMD cases per 100,000 population in 1967 [49]. Following introduction of MenA and MenA plus MenC polysaccharide vaccines to the routine immunization program, the reported incidence had declined to 0.05 cases per 100,000 population in 2009, with serogroups A, B and C accounting for 23%, 4% and 65%, respectively [50]. However, a systematic review and meta-analysis from 2005 to 2015 reported an IMD incidence of 1.84 per 100,000 population [51]. In the Asia-Pacific region in general, there is a lack of information on the incidence of IMD; however, in countries with available data, surveillance indicates a similar incidence of less than 0.2 cases per 100,000 population per year [52].

In the meningitis belt in sub-Saharan Africa, there is a high incidence of endemic IMD with periodic large epidemics [53], influenced by sociodemographic, environmental, sociocultural, and economic factors [54]. Historically, MenA was responsible for most cases of IMD [55]. In 2010, a MenA conjugate vaccine developed specifically for use in the African meningitis belt (MenAfriVac) was introduced in a mass vaccination campaign [56], resulting in a > 99% reduction in MenA disease by 2015 among fully vaccinated populations in nine countries [57]. Since the introduction of MenAfriVac, there has been a general decline in IMD incidence, periodic explosive epidemics are no longer seen, and the major causes of IMD in the meningitis belt have switched to MenW, serogroup X (MenX) and MenC [58–60]. Data from Africa outside the meningitis belt are scarce, but a recent review indicated that MenA predominated in North Africa up to the 1990s, but MenB is currently the most frequently identified serogroup [61]. In South Africa, the incidence of IMD peaked in 2006 at 1.4 cases per 100,000 population and declined to 0.23 cases per 100,000 in 2016, likely as a result of secular trends, as vaccination against meningococcal disease in South Africa is negligible [62]. MenW was the most common serogroup detected in South Africa (50%), followed by MenB (23%), MenY (12%), MenC (9%), MenA (5%) and MenX (0.3%) [62].

Recommendations for vaccination differ between countries [63] (Supplementary Table 1 and references therein). Most European countries recommend MenC vaccination in infants and MenACWY in adolescents. Far fewer countries recommend MenB vaccination. Only Andorra, Czech Republic, Ireland, Italy, Malta, San Marino, and the UK target all the most prevalent serogroups in the age groups that are most affected, by offering MenB and MenC vaccination in infants (MenACWY in Czech Republic and Malta) and MenACWY in adolescents (Czech Republic will also offer MenB vaccination to adolescents from 2022 [64]). Other European countries offering MenB vaccination are Lithuania, Portugal, and France. Australia offers MenACWY vaccination to all toddlers and adolescents and MenB vaccination to Aboriginal and Torres Strait Islander infants; in addition to MenACWY, South Australia offers MenB vaccination to all infants and adolescents. In Latin America, Brazil offers MenC vaccination to infants and MenACWY vaccination to adolescents, Chile offers MenACWY vaccination to toddlers, Argentina offers MenACWY vaccination to infants and adolescents, and Cuba offers a locally produced combined MenB OMV with MenC polysaccharide vaccine in infants. In the USA, MenACWY vaccination is offered to all adolescents and MenB vaccination to those aged 16 − 23 years on a ‘shared clinical decision-making’ basis. In some countries in the African meningitis belt, MenA vaccination is offered to infants.

Table 1. Summary of studies evaluating the association of social deprivation with the risk of meningococcal disease

Reference	Location and year	Type of study	Measure of deprivation	Findings
Stuart et al [65]	UK, 1998	Enhanced surveillance in specific area	Townsend deprivation score Calculated as a composite score of four variables: 1. Proportion of all economically active residents aged older than 16 years who are unemployed 2. Proportion of households in the area with 1 person per room and over 3. Proportion of households with no car 4. Proportion of households not owning their own home Measures social and economic deprivation in a particular locality. Does not capture data for individuals	Risk of meningococcal disease in most versus least deprived areas: RR 1.76 (95% CI 1.14, 2.72) overall population RR 1.90 (95% CI 1.01, 3.58) <5 years of age
Fone et al [66]	UK, 1996 − 1999	Cases identified from statutory notification records in specific area		Risk of meningococcal disease in most versus least deprived areas: RR 2.4 (95% CI 1.7, 3.6) Overcrowding associated with highest risk
Heyderman et al [67]	UK, 1991 − 1999	Ecological study across England of hospital episode statistics among children <5 years of age		Incidence of hospitalization for IMD (linear increase with increasing deprivation): 33.5/100,000 in most affluent areas and 63.0/100,000 in least affluent areas (boys) 27.4/100,000 in most affluent areas and 51.0/100,000 in least affluent areas (girls) IMD mortality (non linear increase with increasing deprivation): 0.6/100,000 in most affluent areas and 2.2/100,000 in least affluent areas (boys) 0.7/100,000 in most affluent areas and 2.1/100,000 in least affluent areas (girls)
Williams et al [68]	UK, 1999 − 2000	Enhanced surveillance in specific area		Risk of meningococcal disease in most versus least deprived areas: RR 1.97 (95% CI 1.55, 2.51)
Olowokure et al [69]	UK, 1996 − 2001	Retrospective review of statutory notifications, laboratory records and death registrations in a specific area		Risk of meningococcal disease in most versus least deprived urban areas: RR 3.33 (95% CI 1.68, 6.60) No association between deprivation and risk of disease in rural areas
Stanton et al [70]	UK, 1977 − 2007	Hospitalization among children for meningococcal disease in a single hospital trust		Hospitalized children had higher Townsend scores (indicating greater deprivation) than the reference population for the area
Taha et al [71]	France, 2012 − 2017	Observational, case-control study using public health insurance database	1. Government-funded insurance that is available for individuals in employment whose income is below a specific threshold was used as a proxy measure of low income (reflects deprivation level of individuals) 2. Validated social deprivation index, a composite ecological marker classifying level of deprivation in a municipality of residence (reflects deprivation in a particular locality but does not capture data for individuals)	Low household income (threshold determining health insurance status) was strongly associated with risk of hospitalization for IMD in a multivariate analysis, with the strongest association in children <1 year of age and 1 − 4 years of age: OR 1.68 (95% CI 1.49, 1.89) overall population OR 4.81 (3.56, 6.49) <1 year of age OR 2.27 (95% CI 1.78, 2.89) 1 − 4 years of age Living in a socially deprived community was associated with IMD hospitalization in a univariate analysis (OR 1.07 [95% CI 1.00, 1.11], but not in a multivariate analysis. Low income is a marker of individual status, while living in a socially deprived community is a composite of several markers associated with the community. This study suggests that low income might reflect a specific individual risk factor for IMD that could be considered in targeted vaccination programs against IMD
Baker et al [72]	New Zealand, 1997 − 1998	Case-control study in children <8 years of age	Questionnaire developed for the study including measures of household crowding, use of public transport, bed-sharing, passive exposure to tobacco smoke, dampness in house, ventilation, heating, exposure to fumes, dust and animals, home and car ownership, parental education, parental employment, household income and receipt of community services benefits	Risk of meningococcal disease increased with increasing number of adults and adolescents per room (median 0.43 for controls, 0.60 for cases): OR 10.7 (95% CI 3.9, 29.5)
McCall et al [73]	Australia, 2000 − 2001	Case-control study	Questionnaire developed for the study including questions on socioeconomic indicators	Risk of IMD in children <6 years of age sharing a bedroom with ≥2 people versus fewer people: OR 7.4 (95% CI 1.5, 36.1)

CI: confidence interval; IMD: invasive meningococcal disease; OR: odds ratio; RR: relative risk; UK: United Kingdom.

3. What is the impact of social deprivation on the risk of meningococcal disease?

A summary of studies evaluating the association of social deprivation with the risk of meningococcal disease is shown in Table 1. All the studies identified were conducted in high-income countries, mainly the UK.

In a rural region of South West England, enhanced surveillance identified 191 cases of meningococcal disease during 1998 [65]. Social deprivation in the population was measured using the Townsend score which comprises four variables (unemployment, lack of car ownership, lack of home ownership, and household crowding); higher scores are associated with a greater level of deprivation. The most deprived areas had higher rates of meningococcal disease than the least deprived (relative risk [RR] 1.76 [95% confidence interval [CI] 1.14, 2.72]). The finding was more pronounced in children <5 years of age where the risk of disease was almost twice as high in the most deprived than in the least deprived areas (RR 1.90 [95% CI 1.01, 3.58]) [65].

A study in the small, socially diverse area of Gwent in Wales (565,000 population) identified 295 cases of meningococcal disease during the period 1996 to 1999, equating to an annual incidence of 13.2 per 100,000 population [66]. The highest incidence was in children <1 year of age. Using the Townsend score to measure social deprivation, the incidence of meningococcal disease increased with increasing social deprivation, from 8.1 per 100,000 in the least deprived areas to 19.8 per 100,000 in the most deprived (RR 2.4 [95% CI 1.7, 3.6]). Of the four variables in the Townsend score, overcrowding was the most strongly associated with meningococcal disease [66].

An ecological study covering the whole of England identified 10,524 cases of meningococcal disease in children <5 years of age hospitalized between 1991 and 1999 [67]. Area deprivation was measured using the Townsend score. The study identified a linear increase in incidence by quintile of deprivation, with an incidence rate per 100,000 population between 1995 and 1999 of 33.5 in the most affluent areas and 63.0 in the least affluent areas for boys [67]. Corresponding values for girls were 27.4 and 51.0. The mortality rates over the same period were 0.6 and 2.2 per 100,000 for the most and least affluent, respectively, for boys, and 0.7 and 2.1 per 100,000, respectively, for girls. However, mortality rates did not show a linear pattern across quintiles of deprivation [67].

In a study of the Eastern region of England (population 5.3 million), the regional database of enhanced surveillance for meningococcal disease was used to identify cases and the Townsend score was used to measure deprivation levels [68]. A total of 773 cases were reported during 1999 and 2000, corresponding to 7.4 cases per 100,000 per year. The incidence per 100,000 per year was 3.0 in the least deprived areas compared with 5.9 in the most deprived areas (RR 1.97 [95% CI 1.55, 2.51]). The most striking difference was seen in children <5 years of age, with a 1.9 times higher incidence in the most versus the least deprived areas [68].

Another study identified meningococcal disease in a retrospective review of statutory notifications, laboratory records and death registrations in a single health area in the West Midlands of England from 1996 to 2001 [69]. Disease incidence was analyzed separately in rural and urban areas and deprivation was measured by the Townsend score. A total of 183 cases were identified (7.1 per 100,000 population), with the incidence being higher in urban than rural areas. In urban areas, the incidence of disease increased with increasing deprivation, with an incidence per 100,000 of 4.8 in the most affluent area compared with 16.2 in the most deprived area (RR 3.33 [95% CI 1.68, 6.60]); however, no such association was seen in rural areas [69].

A further study reported the incidence of meningococcal disease over a 31-year period (1977 to 2007) among children admitted to a single hospital trust in Merseyside in the North West of England [70]. A total of 1157 children were admitted, 80% of whom were <5 years of age. Children admitted to hospital had higher Townsend scores compared with the reference population of Merseyside, indicating that greater social deprivation was associated with meningococcal disease. However, deprivation was not a risk factor for death [70].

Studies in other countries have also shown an association between low socioeconomic status and risk of meningococcal disease. In France, an observational case-control study using the public health insurance database identified several risk factors for hospitalization for IMD [71]. Between 2012 and 2017, 3532 individuals were hospitalized for IMD. Medical risk factors or conditions identified included congenital immunodeficiency, acquired immunodeficiency, asplenia or hyposplenia, severe respiratory disorders, haemophilia, and autoimmune disorders. Low household income was also strongly associated with hospitalization for IMD in a multivariate analysis (odds ratio [OR] 1.68 [95% CI 1.49, 1.89]), with the strongest association being in children <1 year of age (OR 4.81 [95% CI 3.56, 6.49]), and 1 − 4 years of age (OR 2.27 [95% CI 1.78, 2.89]) [71]. Living in a socially deprived community was associated with IMD hospitalization in a univariate analysis (OR 1.07 [95% CI 1.00, 1.11], but not in a multivariate analysis. Low income is a marker of individual status, while living in a socially deprived community is a composite of several markers associated with the community. The results of the study suggest that low income might reflect a specific individual risk factor for IMD that could be considered in targeted vaccination programs against IMD [71].

A case-control study of meningococcal disease was performed in children <8 years of age living in Auckland, New Zealand from 1997 to 1999 during an epidemic of MenB disease [72]. A total of 202 cases were included in the study. The risk of disease was associated with household overcrowding (OR 10.7 [95% CI 3.9, 29.5]), corresponding to a doubling of risk with the addition of two adolescents or two adults to a 6-room house. Overcrowding was also identified as a risk factor for IMD in a case-control study conducted in South Queensland, Australia during 2000 and 2001 [73]. The study identified 84 cases of IMD notified to the region's public health authority. In a multivariate analysis, a higher risk of IMD was found only in children <6 years of age sharing a bedroom with ≥2 people (OR 7.4 [95% CI 1.5, 36.1]).

4. What is the impact of social deprivation on access to vaccination against meningococcal disease?

A summary of studies evaluating the association of social deprivation with access to vaccination against meningococcal disease is shown in Table 2.

Table 2. Summary of studies evaluating the association of social deprivation with access to vaccination against meningococcal disease

Reference	Location and year	Type of study	Vaccine and population	Measure of deprivation	Findings
Vallejo-Aparicio et al [74]	Spain, 2018 − 2019	Ecological study	MenB (4CMenB) (self-funded)	Average income per capita in municipality	There was a statistically significant correlation between vaccine uptake per birth and income per capita
Taylor et al [75]	South Australia, 2013	Survey study of family physicians	MenB (self-funded)	Not defined in study	Percentage of physicians considering factors as ‘definitely a barrier’ to prescription: High cost of vaccine: 61% Low socioeconomic status of family: 59%
Lu et al [77]	USA, 2015	Based on National Immunization Survey – Teen data	MenACWY Adolescents	Insurance status	Vaccine coverage was 72.9% in uninsured adolescents versus 81.7% in insured adolescents
Huang et al [78]	USA, 2017	Physician survey	MenACWY and MenB Adolescents and young adults	Insurance status	Among physicians who prescribed both MenACWY and MenB vaccines, private or commercial insurance was held by 61% of patients in their practice, whilst 22% of their patients were covered by Medicaid. Among physicians who prescribed only MenACWY, 53% of patients were covered by private/commercial insurance and 29% were covered by Medicaid
Watkins & Feemster [79]	USA, 2015 − 2017	Retrospective cohort study	MenB 16 − 23 years of age	Insurance status	Percentage of individuals completing vaccination series: Private insurance: 48% Medicaid: 26%
Srivastava et al [80]	USA, 2016	Household survey	MenB Households with adolescent 16 − 19 years of age	Not applicable	Relative importance of variables predicting MenB vaccination (based on Classification and Regression Tree analysis): Annual household income: 35.9%; HCP knows family well: 24.2%; age: 23.9%; race/ethnicity: 15.7%
Blagden et al [84]	UK, 2015 − 2016	Ecological, general practice-based study	MenACWY (part of NIP) Catch-up cohort: 17 − 18 years and first-time university students	English Indices of Deprivation score [87] Calculated for a small geographical area as a weighted composite score of seven variables: 1. Income 2. Employment 3. Education 4. Crime 5. Health 6. Barriers to housing and services 7. Living environment	Vaccine uptake decreased with increasing deprivation: RR 0.991 (95% CI 0.986, 0.995)
Tiley et al [85]	UK, 2016 − 2017	Ecological, school-based study	MenACWY (part of NIP) 13 − 14 years	English Indices of Deprivation score [87] As above	Vaccine coverage according to quintile of area deprivation: 1 (most deprived): 76.0%; 2: 82.8%; 3: 82.0%; 4: 83.6%; 5 (least deprived): 88.2%
Fletcher et al [86]	UK, 2017 − 2018	Ecological, school-based study	MenACWY (part of NIP) 14 − 15 years	Effectiveness of education delivery in an individual school as judged by the national school inspection body (Ofsted) Proportion of children in an individual school eligible for free school meals	Vaccine coverage according to effectiveness of education delivery:Inadequate: 62.5%; requires improvement: 76.4%; good: 81.8%; outstanding: 87.0% (OR 3.54 [95% CI 3.00, 4.19]) Vaccine coverage according to percentage of children eligible for free school meals:Above average: 76.6%; below average: 83.4% (OR 1.56 [95% CI 1.41, 1.78])

4CMenB: 4-component meningitis B vaccine; CI: confidence interval; HCP: health care professional; MenACWY: meningitis A, C, W or Y; MenB: meningitis B; NIP: national immunization program; OR: odds ratio; RR: relative risk; USA; United States of America; UK: United Kingdom.

MenB vaccination is not currently part of the NIP in Spain but is funded by several regional immunization programs. An ecological correlation study using data reporting aggregate births, average income per capita and average MenB vaccine sales at the municipality level was conducted before implementation of any regional immunization program. The study showed that higher uptake of MenB vaccination was associated with higher family income [74]. A 2013 survey of 523 family physicians in South Australia evaluated physician perspectives on factors influencing their prescription of the MenB vaccine and other non-publicly funded vaccines (MenB vaccine was not funded in South Australia at the time of the survey) [75]. Respondents gave the MenB vaccine for children the highest priority out of eight non-funded vaccines, closely followed by pertussis vaccine for pregnant women. Physicians identified high cost of the MenB vaccine and perceived low socioeconomic status of families as barriers to vaccination, considered as ‘definitely a barrier’ by 61% and 59% of respondents, respectively [75]. Nearly one third of physicians stated that they never or rarely discussed non-funded vaccines at a routine immunization encounter. There was no significant association between identifying cost or socioeconomic status as a barrier to vaccination and likelihood of discussing non-funded vaccines. Physicians with previous experience of IMD were more likely to discuss non-funded vaccines [75].

MenACWY and MenB vaccination are covered in the USA by the Vaccines for Children Program, although the Advisory Committee on Immunization Practices (ACIP) recommends MenB vaccination only on a ‘shared clinical decision-making’ basis [76]. Despite reimbursement of both vaccines, several studies in the US have found an association between lower vaccine coverage and insurance or income status [77–82]. Coverage of the MenACWY vaccine was 72.9% in uninsured adolescents compared with 81.7% in those with insurance [77]. A survey of HCPs found that, among physicians who prescribed both MenACWY and MenB vaccines, private or commercial insurance was held by 61% of patients in their practice, whilst 22% of their patients were covered by Medicaid [78]. Among physicians who prescribed only MenACWY, 53% of patients were covered by private/commercial insurance and 29% were covered by Medicaid [78]. For adolescents and young adults in the USA, higher rates of MenB vaccination were reported among those with private versus Medicaid insurance [79], whilst a survey found that household income was the most important factor in the decision to receive MenB vaccination [80]. Medicaid provides coverage for low-income adults, children, pregnant women, the elderly and people with disabilities; care under Medicaid is generally free but some states operate cost-sharing arrangements with higher income target groups [83].

In the UK, both MenACWY and MenB vaccines have been offered as part of the NIP since 2015. Uptake of both vaccines is high in the UK, but several studies have shown lower uptake in more deprived areas [84–86]. An ecological study conducted in highly diverse areas across North West England (3.9 million population) evaluated the association between general practice characteristics and MenACWY vaccine uptake [84]. Data were collected for individuals eligible for vaccination in the 2015 − 2016 catch-up cohort, which included persons 17 − 18 years of age and first-time university students. Deprivation was measured by the English Indices of Deprivation score [87]. Vaccine uptake ranged from 20.8% to 46.8%. General practice characteristics associated with higher vaccine uptake were patient recommendation of the practice, higher quality score of the practice, the proportion of patients from an ethnic minority (primarily Asian and Asian British) and the proportion of patients 15 − 24 years of age [84]. Vaccine uptake decreased with increasing deprivation as (RR 0.991 [95% CI 0.986, 0.995]) [84].

An ecological study collected school-level data from 1432 schools on the uptake of MenACWY vaccine in the 2016 − 2017 academic year for children 13 − 14 years of age across England [85]. Vaccine coverage of >80% was reported in 68% of state-funded schools, 55% of non-state-funded (private) schools, 27% of schools for children with special educational needs, and 21% of schools for children excluded from mainstream education. There might be several reasons behind this variability, but school size is likely a factor (state-funded schools tend to be the largest of the school types evaluated). In a sub-analysis of state-funded mixed-sex schools, MenACWY vaccine coverage ranged from 76.0% in the most deprived areas to 88.2% in the least deprived areas (Figure 2) [85]. Another ecological study evaluated the influence of school characteristics on uptake of MenACWY vaccine in all 129 schools in the Manchester area of North West England among children 14 − 15 years of age in 2017 − 2018 [86]. Out of 19,898 eligible individuals, 16,065 (80.7%) were vaccinated. Schools judged by authorities to be least effective in delivery of education had lower vaccine uptake (62.5%) than the most effective schools (87.0%) (Figure 2), corresponding to an OR of 3.54 (95% CI 3.00, 4.19) in a multivariable analysis [86]. Schools with an above average proportion of children eligible for free school meals (a measure of deprivation) had vaccine uptake of 76.6% compared with 83.4% for schools with a below average proportion (OR 1.58 [95% CI 1.41, 1.78]) [86].

Figure 2. Coverage of the MenACWY vaccine according to two measures of socioeconomic status in England Tiley et al [85]: Graph shows vaccine coverage according to quintile of social deprivation measured by the English Indices of Deprivation score, which is calculated for a small geographical area as a weighted composite score of seven variables: 1. Income; 2. Employment; 3. Education; 4. Crime; 5. Health; 6. Barriers to housing and services; 7. Living environment. Fletcher et al [86]: Graph shows vaccine coverage according to individual school effectiveness score: 1. Inadequate; 2. Requires improvement; 3. Good; 4. Outstanding. MenACWY: meningitis A, C, W or Y.

5. Guiding principles in fostering equitable access to meningococcal vaccination

Based on the success of the MenAfriVac project (described earlier) [56], the WHO and partner organizations aim to replicate the success of the MenAfriVac model to create other affordable vaccines, including a MenACWXY conjugate vaccine. A goal of the WHO road map is to have at least one such vaccine licensed by 2022 (Figure 1). In high-income countries, despite the rarity of IMD, several factors could warrant vaccination, including the high case-fatality rates, devastating impact and high treatment costs of potentially lifelong sequelae, loss of productivity, as well as the threat of outbreaks, fear of the disease, and fear of misdiagnosis. However, even in high-income countries, achieving universal coverage of meningococcal vaccines continues to be challenging. MenC vaccine coverage is now high in most European countries, thanks to the inclusion of the vaccine in NIPs across Europe. However, wide implementation of the quadrivalent MenACWY conjugate vaccine is still to be achieved despite an increase in incidence of the MenW and MenY serogroups [37,88].

Adoption of the MenB vaccine into NIPs has proved more challenging than adoption of the MenC and MenACWY vaccines because of the higher cost of the MenB vaccine. In the UK, which has been a leader in the introduction of publicly funded meningococcal vaccination, the Joint Committee on Vaccination and Immunization (JCVI) initially concluded that a MenB (4CMenB) vaccination program was unlikely to be cost-effective based on economic analysis [89]. This decision was reconsidered following challenges from multiple groups [90,91]. A second cost-effectiveness analysis was conducted, in which several parameters were revised, including a quality of life adjustment factor to account for the severity of the disease and the innovative nature of the vaccine; quality of life losses to family members, recognizing that IMD has a considerable impact on families beyond the individual patient; a higher incidence of disease considering a longer term average to account for the unpredictability of the disease; a higher proportion of major and minor sequelae, taking into account recent evidence of the major impact of sequelae on patients; and inclusion of litigation costs to the health service [92,93]. The analysis concluded that various scenarios could result in the vaccine being cost-effective if competitively priced [93]. Following consideration of the new analysis and extensive campaigning by representative charities and affected families, the JCVI recommended inclusion of the MenB vaccine in the infant immunization program [92]. Since that time, several other analyses have argued for a more comprehensive approach to evaluation of cost-effectiveness, accounting for the broad disease burden [94–100].

Very recently, the French National Authority for Health (Haute Autorité de Santé [HAS]) also initially decided not to recommend inclusion of the MenB vaccine (4CMenB) into the infant NIP, but the decision led to intense opposition from numerous stakeholders. Pediatric scientific societies highlighted not only the severity of MenB disease, the impact on the family of long-term sequelae and the effectiveness of the vaccine, but also emphasized the social inequity inherent in the availability of a vaccine that offers effective prevention of a severe disease, but is affordable only by higher income families [101]. The recognition of low income as a risk factor for hospitalization due to IMD also supported the argument that vaccination against MenB should reduce health inequity [71]. It was also recognized that there is a risk of increased susceptibility in the population resulting from reduced meningococci circulation during coronavirus disease 2019 (COVID-19) restrictions, leading to a potential meningitis epidemic cycle following lifting of restrictions [101].

Following further consultation, the HAS revised its recommendation and 4CMenB is now included for infants in the French NIP [102]. Notably, the HAS recognized the difficulties created by the availability of a vaccine not accessible to the most vulnerable social categories and the impact of social inequities on infection management, including delayed recognition and treatment [102]. This decision acknowledged for the first time in a country recommendation that the introduction of the MenB vaccine for infants into the NIP is an important measure to reduce inequity and protect those who are most at risk of IMD. This clear position on the need to introduce MenB vaccination into the NIP to assure equity should be followed by other countries who are still questioning their recommendation.

Although vaccination against MenB is not part of the NIP in Spain as a whole, it is funded by several autonomous regions, including the Canary Islands, Castilla y León and, most recently, Catalonia and Andalusia [103]. Inclusion of the vaccine into the regional programs recognized the importance of long-term sequelae and was supported by the Spanish Association against Meningitis, along with four medical associations and other organizations and individuals [103].

Introduction of a vaccine into the NIP and clear recommendations from health authorities are likely to increase vaccine uptake and promote equity. Potential challenges with non-universal vaccine recommendations can be illustrated by ACIP's ‘shared clinical decision-making’ recommendation for MenB vaccination [104]. There is evidence that many HCPs do not understand the recommendation or do not have sufficient time to engage in shared decision-making discussions with patients [78,82,104,105]. Moreover, many HCPs do not realize that the MenB vaccine is reimbursed under the Vaccines for Children Program and therefore might not initiate discussions because of a perception that a patient cannot afford it [105]. Indeed, a survey of HCPs found that 34% of pediatricians strongly recommended MenB vaccination to healthy 16 − 18 year olds, 24% recommended it, although not strongly, 37% made no recommendation, and 5% recommended against it [105]. Lack of HCP recommendation is likely to have contributed to the overall low coverage of MenB vaccination achieved in the USA [82]. In 2019, among adolescents in the USA aged 17 years at interview, only 22% had received at least one dose of MenB vaccine, compared with 54% who had received at least two doses of MenACWY vaccine (the second dose is recommended at ≥16 years of age) [106].

In the UK and Italy, where the MenB vaccine has been included in the NIP for infants, uptake of the vaccine is high, with coverage of 93% reported in the UK for 2019 − 2020 [107] and coverage of 69% overall in 2019 in Italy (regional range 47 − 91%) [108]. Although inclusion of a vaccine into the NIP is the first step towards simplifying HCP recommendations and optimizing vaccine coverage, the UK experience illustrates that it is not enough on its own to ensure equity. Although both MenC/MenACWY and MenB vaccines are universally recommended and freely available in the UK, inequity still exists in the form of lower vaccine uptake in disadvantaged groups, as described earlier [84–86]. Other initiatives, such as improving parent, adolescent and HCP knowledge of vaccines, strengthening provider recommendations, and ensuring vaccine supply are also needed to ensure equitable access to and uptake of vaccines [11,82,109].

The COVID-19 pandemic has increased the visibility of inequity in access to vaccination and disparities between countries. The COVAX collaboration between the WHO and Gavi, the Vaccine Alliance, aimed to achieve an equitable supply of vaccines to low- and middle-income countries, but as of summer 2021, has been responsible for supplying less than 4% of doses delivered worldwide [110]. The Vaccine Equity Declaration of the WHO calls on world leaders to increase contributions to COVAX and share doses in parallel with national vaccination programs; vaccine manufacturers to share know-how with the COVID-19 Technology Access Pool and prioritize supply to COVAX; regulatory bodies to safely accelerate approvals; and governments to invest in vaccine delivery and data systems, to ensure that vaccines are free of charge and to prioritize affected communities [111]. Some high-income countries are also specifically addressing the issue of equity. For example, the USA Health Resources and Services Administration (HRSA), which funds health centers for medically underserved communities, and the Centers for Disease Control and Prevention are directly allocating COVID-19 vaccine to HRSA clinics, in addition to federal allocations of vaccine [112]. The recent decision by the UK government to recommend and fund universal COVID-19 vaccinations in teenagers recognizes that, in areas of relative deprivation, the negative impact of COVID-19 has been especially great, with even more apparent and enduring effects of missed or disrupted education [113].

It is noteworthy that the social constraints resulting from the COVID-19 pandemic have generated the undesired consequence of reducing the uptake of non-COVID vaccines, particularly those implemented within NIPs, including meningococcal vaccines [114–116]. In France, although IMD cases decreased during 2020 compared with the previous 2 years, those associated with unusual isolates in the elderly were increased [117]. Rebound of IMD might therefore be a concern upon return to normal social conditions.

6. Conclusion

Social deprivation is a recognized individual risk factor for IMD. Numerous studies have shown that households with low socioeconomic status have the highest risk of IMD, but also have the lowest coverage rates of MenACWY and MenB vaccines. Moreover, certain social at-risk groups such as migrants and the homeless might not even be considered in these studies as they might not be included in national health databases. It should be acknowledged that social deprivation is context dependent; even socially deprived individuals in high-income countries have greater access to healthcare resources than most individuals in middle- and low-income countries. In this regard, it is noteworthy that all the studies of association between social deprivation and risk of IMD or vaccine uptake were conducted in high-income countries.

Including both MenB and MenACWY vaccines in a simple schedule in the NIP could help to provide clear guidance for HCPs from health authorities to ensure that vaccines are offered universally to all target groups. Initiatives to improve knowledge about vaccines among parents, adolescents and HCPs could also improve uptake of vaccine and might be particularly important among disadvantaged communities with less access to reliable vaccine information. Delivery of a reliable and respectful health care service to socially deprived communities also has a role in building trust and ensuring that people are open to receiving health care information. Although no NIP to date includes meningitis vaccination for the elderly, equity between age groups should also be considered, especially given the burden of meningitis in adults. Beyond NIPs, the cost of vaccination should be reimbursed for disadvantaged individuals, such as those on a low income. These approaches should help to achieve optimal protection against IMD, reduce social inequity and protect those at greatest risk of IMD.

7. Expert opinion

Upon vaccine licensure, the process of decision-making in tailoring vaccine recommendations usually considers epidemiological characteristics of the disease as well as characteristics of the vaccine and cost-effectiveness studies. These considerations remain global and might fail to account for other aspects of real-world clinical practice. In particular, access to healthcare might differ depending on the social and economic characteristics of the population, both between countries and within the same country. Equity is a constitutional right and equity in access to healthcare can improve preventive medical practices. Notably, vaccination is a key preventive tool, and universal recommendation and reimbursement of vaccines can improve equity. Approaches such as the Italian Vaccination Calendar for Life, in which an alliance of professional societies propose the ‘ideal’ vaccination schedule from birth to old age based on scientific evidence, are also helpful [118]. It must be recognized, however, that not all countries will support universal vaccination programs; in this situation, it is important that health insurance policies cover the cost of vaccination. Universal Health Coverage for everyone is a goal of the WHO and vaccinations are an essential element of this. The modalities for delivering vaccinations will differ from country to country. Publicly funded NIPs guarantee the principle of universal access, whether sourced via country financing or international (Gavi) sources. Where public funding is not provided, or is only partially available, private insurance can provide a complimentary financing tool. However, where public funding is not provided and private insurance is beyond the means of citizens, gaps will remain and inequity will persist.

As social deprivation seems to be a specific risk factor for IMD, more efforts should be made to ensure the access of the whole population to vaccines. However, evaluation of deprivation can be difficult because markers of deprivation and approaches differ between countries. In addition, some studies have evaluated deprivation at a community level and others at an individual level. In the study by Taha et al described earlier, low household income (a marker of individual status) was associated with hospitalization for IMD in a multivariate analysis, but living in a socially deprived community was not [71]. One future area of work might be to tailor standardized tools to evaluate social deprivation that consider personal and environmental factors. Such a standardized social deprivation index could be an additional working tool in vaccine recommendation and implementation.

Data on the burden of meningitis globally come from many different sources and are hard to interpret, which impedes tracking of progress towards tackling the disease. The Meningitis Progress Tracker is a tool developed to track progress against the WHO roadmap and is a source of up-to-date meningitis data including cases and deaths, prevention, surveillance, treatment, and impact on quality of life [119]. Its purpose is to enable governments and global health agencies to tackle problems and focus effort, provide a training tool for public health doctors and epidemiologists, and empower civil society to campaign for improvement. Citizen movements for rights and equity are set to gain importance. Although many rights are already enshrined in law, they are not universally implemented, and a ‘rights approach’ might not be embedded in health care cultures. Patient associations can be increasingly influential in public health policy decision-making. Knowledge of the social and economic risk factors of vaccine-preventable diseases should help the voice of the patient to be more audible by public authorities.

Financial considerations are a major factor in universal vaccine recommendations. With regard to meningococcal vaccines, a more comprehensive approach to evaluation of cost-effectiveness is needed that accounts for the broad disease burden, including mid- and long-term sequelae, as well as the unpredictable nature of the disease [94–100]. It should be recognized that social deprivations that result in reduced access to vaccination will also result in poorer access to general healthcare; thus, long-term sequelae in socially deprived survivors are likely to have more impact than in non-socially deprived survivors. Other approaches to managing the high costs include discounts for large tenders, financial support or lower prices for low- and middle-income countries, and support for manufacturing facilities in low- and middle-income countries. Decisions should be made based on the assumption that IMD is a severe and unpredictable vaccine-preventable disease anywhere in the world.

Finally, the COVID-19 pandemic has changed profoundly the epidemiology of several diseases, including IMD, with an important reduction of the circulation of isolates in the general population that might lead to lower natural immunity. Moreover, there has been an associated reduction in vaccine uptake that is expected to further diminish population immunity, leaving a higher proportion of the population susceptible to IMD and other vaccine preventable diseases. Vaccine uptake might be even further reduced among the socially deprived because patients might have limited access to information or because HCPs might, rightly or wrongly, anticipate that patients could not afford to pay for a non-reimbursed vaccine and therefore do not initiate discussion with the patient. Furthermore, restrictive measures for pandemic control worsen the economic situation of the most deprived members of the population, leaving them at higher risk of rebound IMD when social restrictions are lifted. Plans to promote vaccines and vaccination are needed and should consider equity in access to vaccines at sub-national, national and supra-national levels.

8. Funding

GlaxoSmithKline Biologicals SA funded this study and was involved in all stages of study conduct, including data analysis. GlaxoSmithKline Biologicals SA also took charge of all costs associated with developing and publishing this manuscript.

9. Declaration of interests

M-K Taha reports grants/contracts from the GSK group of companies, Pfizer, and Sanofi Pasteur for activities outside the presented work. M-K Taha also reports a patent 630,133 issued for activities outside the presented work. F Martinon-Torres reports his institution received trial fees from the GSK group of companies, Ablynx, Abbott, Janssen, Medimmune, MSD Merck, Novartis, Novavax, Pfizer, Regeneron, Roche, Sanofi Pasteur, and Seqirus for activities outside the presented work. F Martinon-Torres also reports his institution received grants from AstraZeneca, Janssen, MSD Merck, and Pfizer for activities outside the presented work. F Martinon-Torres also reports having received personal fees from Biofabri, Novavax, and Sanofi Pasteur; and personal fees and non-financial support from the GSK group of companies, MSD Merck, Pfizer, and Seqirus for activities outside the presented work. F Martinon-Torres also reports having received support from the Instituto de Salud Carlos III for research activities outside of the presented work. R Köllges reports having received honoraria and travel support for advisory boards, speakers bureaus, presentations, and studies for activities outside the presented work and studies by the GSK group of companies, Pfizer, MSD Merck, Sanofi Pasteur, Novartis, and AstraZeneca. P Bonanni reports having received payment or honoraria for numerous engagements as speaker at meetings and webinars, and participant to advisory boards on vaccination-related matters from the GSK group of companies, AstraZeneca, Janssen, MSD Merck, Pfizer, Sanofi Pasteur, and Seqirus for activities outside the presented work. P Bonanni also reports having received travel support for attending these meetings from the GSK group of companies, MSD Merck, Pfizer, Sanofi Pasteur, and Seqirus. P Bonanni also reports being part of DSMC for Shigella Investigational Vaccine, for the GSK Vaccines Institute for Global Health. MA Palazzi Safadi reports his institution received research grants from Pfizer for activities outside the presented work. MA Palazzi Safadi also reports having received fees for advisory board consultation and lectures from the GSK group of companies, Abbott, Sanofi-Pasteur, Seqirus, AstraZeneca, MSD, Janssen and Pfizer; for activities outside the presented work.

R Booy consulted to the GSK group of companies for this work, and regularly consults to all vaccine companies in Australia, including Abbott, AstraZeneca, Gene Expert, the GSK group of companies, Janssen, Medimmune, MSD Merck, Novartis, Novavax, Pfizer, Roche, Sanofi Pasteur, and Seqirus for activities outside the presented work. R Booy provides input to advisory boards and lectures and educational material. He also received a grant from Sanofi Pasteur for research outside of the submitted work; and equipment from Roche and Gene Expert outside of the submitted work. V Smith is the CEO of the Meningitis Research Foundation and Confederation of Meningitis Organizations who received grants and sponsorship from the GSK group of companies, Pfizer, Sanofi, and Serum Institute of India. S Garcia, R Bekkat-Berkani and V Abitbol are employed by the GSK group of companies and hold shares in the GSK group of companies. S Garcia was also previously a consultant for Business & Decision Life Sciences on behalf of the GSK group of companies. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript.

Table of abbreviations

4CMenB	=	4 component meningococcal serogroup B vaccine
ACIP	=	Advisory Committee on Immunization Practices
CI	=	Confidence interval
EU/EEA	=	European Union/European Economic Area
fHbp	=	factor H binding protein
HAS	=	Haute Autorité de Santé
HCP	=	Healthcare provider
HRSA	=	Health Resources and Services Administration
IMD	=	Invasive meningococcal disease
JCVI	=	Joint Committee on Vaccination and Immunization
MenA	=	Meningococcal serogroup A
MenACWY	=	Meningococcal serogroup A, C, W, or Y
MenB	=	Meningococcal serogroup B
MenC	=	Meningococcal serogroup C
MenW	=	Meningococcal serogroup W
MenX	=	Meningococcal serogroup X
MenY	=	Meningococcal serogroup Y
NIP	=	National immunization program
OMV	=	Outer membrane vesicle
OR	=	Odds ratio
RR	=	Relative risk
UK	=	United Kingdom
USA	=	United States of America
WHO	=	World Health Organization

Article highlights

• Communities with low socioeconomic status have the highest risk of invasive meningococcal disease and the lowest uptake of meningococcal vaccines.

• Including meningococcal vaccines in national immunization programs is a critical step that helps to ensure that vaccines are offered universally to all target groups.

• However, there have been significant challenges in introducing meningococcal vaccines, particularly serogroup B vaccines, to national immunization programs.

• Initiatives to improve meningococcal vaccine knowledge might be particularly important to improve uptake among disadvantaged communities with less access to reliable vaccine information.

• Plans to promote vaccination should consider equity in access to vaccines at national and regional levels.

Author contributions

All authors participated in the conception and design of the review article and interpretation of the relevant literature and were involved in writing the review article or revising it for intellectual content. All authors have approved the final version of the manuscript.

Reviewer disclosures

Peer reviewers on this manuscript have no relevant financial or other relationships to disclose.

Acknowledgments

The authors thank Business & Decision Life Sciences platform for editorial assistance and manuscript coordination, on behalf of GSK. Aurélie Roth (Business & Decision Life Sciences, on behalf of GSK) coordinated manuscript development and editorial support and Mary L Greenacre (An Sgriobhadair, UK, on behalf of GSK) provided medical writing support.

Supplementary material

Supplemental data for this article can be accessed here.