The potential for measles transmission in England

Measles vaccination was introduced in the UK in 1968 for children in the second year of life [1]. Coverage gradually improved from approximately 50% during the 1970s to 86% when MMR vaccine replaced single antigen vaccine in 1988, and reached 92% in 1995. As a result, measles epidemics, which had occurred biennially in the pre-vaccination period with hundreds of thousands of notified cases, became smaller and less frequent. Control of measles reached a new level following a national vaccination campaign in November 1994, when measles-rubella vaccine was offered to all school children aged 5–16 years to prevent a predicted epidemic of measles; coverage of 92% was achieved and endemic transmission of measles was interrupted [2]. In 1996, a second dose of MMR was added to the routine vaccination schedule at around 4 years of age. Despite the occurrence of occasional outbreaks, caused by limited secondary spread from imported cases, measles has been eliminated in England and Wales for more than 10 years [3].

To maintain measles elimination, the effective reproduction number, R, (the average number of secondary cases infected by a typical infectious case) needs to remain below 1 [4]. This can be achieved through maintaining low levels of susceptibility by vaccinating a high proportion of the population. The European region of the World Health Organisation (WHO) defined target levels of susceptibility to sustain measles elimination: the level of susceptibility in 1–4 year olds should be less than 15%, in 5–9 year olds less than 10% and in all older cohorts less than 5% [5]. As around 90% of individuals are protected from measles after a first dose of vaccine, and 99% after a second dose, to achieve these target levels requires high vaccination coverage to be sustained [6].

Coverage for MMR vaccine in two year old children in England fell from the peak of 92% in 1995 to reach the low of 80% in 2003. Coverage in London is lower than in the rest of England. We have used routine data on vaccine coverage in two and five year old children to estimate the level of susceptibility, and hence the reproduction number for measles in England. These results can be used to predict future control of measles and to estimate the possible impact of measles becoming re-established [7].

Our analysis has identified several DHAs and SHAs in England with the potential for sustaining measles transmission. Among 99 former DHAs, fourteen have R values above 1, meaning that they run the risk of re-establishment of measles transmission in the community. Such transmission could lead to an outbreak involving many thousands of measles cases. A measles epidemic in Italy in 2002 led to around 40,000 cases, with direct costs estimated at between €9.9 and €12.4 million, and total costs around €14.8 million [17]. With such information, the outbreak sizes estimated in this paper can be a valuable tool to estimate the epidemic costs and the cost effectiveness of possible interventions in England, such as a catch-up campaign.

Our analysis ignores immunity through natural infection in children aged under 17 years, as the incidence of measles has been too low to have a significant effect in the cohorts considered. The last national epidemic was in 1988 and the incidence declined further following the national vaccination campaign in November 1994 [2]. The quality of the COVER data is a weakness of this study, as it is likely to underestimate the true vaccine coverage, as some vaccinations are not be recorded on the child health computer system and the total number of children (the denominator) may be inaccurate [9, 18]. There has been no published validation of data held for children aged five years, but it is expected that the quality of coverage data would decline with the age of the child as movements out of the denominator are often not recorded. Data is less accurate in populations of high mobility, and therefore the accuracy of COVER data for London is likely to be worse than for the rest of country. Outside of London, some of the DHAs with R above the epidemic threshold are known to have problems with data accuracy. Our estimates of susceptibility to measles by age in England are consistent with data from serological surveillance [12]. Unfortunately few samples in these serosurveys are collected in London, so these data do not reduce the uncertainty regarding vaccination status and susceptibility in London. Even after allowing for considerable under-estimation of coverage, however, many London areas still remain at high risk. In addition, unless routine coverage can be further improved and sustained, the total number of susceptibles will be expected to increase each year. Although there has been an increase in MMR1 coverage at two years since 2003, this is offset by a small decline at five years, suggesting that further accumulation of susceptibles will lead to a higher risk of measles outbreaks in the future [19].

In response to earlier analyses of measles risk for London DHAs, primary care trusts across the city conducted a catch-up campaign among primary school aged children to reduce the number of susceptibles in London [6]. To eliminate the risk of a major outbreak, the campaign would have had to vaccinate 40% of unvaccinated primary school children. More than 40,000 children in this age group were identified and vaccinated by the campaign, including over 17,000 previously unvaccinated children. Initial evaluation indicates, however, that the campaign has achieved only a modest reduction to the epidemic risk in London and that endemic measles transmission risk remains high in several health districts [20].

Each health area should review the vaccination status of school children born since 1990 in order to validate the coverage data, and if necessary, to focus on reducing the proportion of children who are completely unvaccinated against measles. The threat of re-establishing measles transmission could be removed if the proportion of each cohort susceptible to measles was reduced to less than 10% in primary school and to less than 5% in secondary school. Opportunities to improve routine coverage need to be reinforced and supplementary vaccination initiatives for children already attending school will also have to be taken in some areas. Catching-up children born between 1997 and 2003, the cohorts most affected by the decline in MMR coverage should be a priority. A catch-up programme of this type has recently been announced by the Chief Medical Officer [21]. Later cohorts can then be assessed at school entry on a routine basis. A further opportunity at secondary school entry, when a higher level of immunity is required to prevent transmission, should be formalised in each health area. To reduce the number of young adults leaving school susceptible to measles, mumps or rubella, MMR vaccine should also be offered to all unvaccinated or partially vaccinated adolescents at the time of the school leaving booster. If this final opportunity is not taken, adults will be difficult to access in the event of an increase in incidence. This problem has been graphically illustrated by epidemics of rubella in 1996/7 and mumps in 2004/5 [3, 4].

We identified several areas with the potential for sustaining measles transmission. A number of former London health districts remained at high risk of a measles epidemic even allowing for considerable under-reporting of vaccination coverage. Most of those susceptible to measles are unvaccinated children under 17 years old. Vaccinating a significant proportion of these children in the highest risk areas is necessary to remove the risk of an epidemic. Primary care trusts should ensure that accurate systems are in place to identify unimmunised children and to offer catch-up immunisation for those not up to date for MMR.