Abstract
Effective protection against mumps can be achieved through 2 doses of the measles-mumps-rubella (MMR) vaccine. However, outbreaks of mumps have recently been described among populations with high vaccination coverage, including 2 doses of MMR. Here we describe an outbreak at a school in the East of England, UK. The school was attended by 540 pupils aged 10–19 years and had 170 staff. In total, 28 cases of mumps (24 pupils and 4 staff) were identified during 10 January to 16 March 2013. Vaccination status was known in 25 of the cases, and among these 21 (84.0%) had a documented history of 2 doses of MMR while the remaining had a history of one dose (2/25 cases, 8.0%) or no doses (2/25, 8.0%) of MMR. An outbreak control team recommended that MMR vaccine should be offered to all pupils whose parents consented to it, regardless of previous vaccination status. Additional MMR vaccines were administered to 103 pupils, including 76 (73.8%) third doses of MMR. Offering an additional dose of MMR appeared to be acceptable to parents, and we found it feasible to administer the intervention in a timely manner with resources from the local Public Health Centre (Primary Care Trust). An additional dose of MMR to all individuals at risk can be considered as an acceptable control measure for mumps outbreaks in schools even if the vaccination coverage is high. However, further evidence on the effectiveness, acceptability, and safety of this intervention is needed.
Keywords: Mumps, vaccine, MMR vaccine, recommendations, United Kingdom
Introduction
Mumps is an acute viral illness which commonly causes fever and parotitis, but can cause serious complications such as orchitis, meningitis, and acute pancreatitis. The measles-mumps-rubella (MMR) vaccine can provide effective protection against mumps, with 2 doses of vaccine being more effective than a single dose.1 In the United Kingdom (UK) vaccination is recommended at the age of 12 mo and again at 3 to 5 y. In England the coverage of 2 doses of MMR in children reaching their fifth birthday was 87.7% in 2012–13.2 Despite this vaccination coverage a provisional total of 3524 laboratory confirmed cases of mumps were reported in England in 2013.3 Outbreaks of mumps have been described in schools and universities in the UK and in other countries with MMR vaccination programmes, including in highly vaccinated populations.4-6
On 5 February, 2013, 8 cases of mumps were reported among pupils attending a school in the East of England. As a public health response an Outbreak Control Team (OCT) convened on 6 February. Because there were indications of illness in, and spread from cases who were fully vaccinated, the OCT recommended that MMR vaccine should be offered to all pupils whose parents consented to it, regardless of previous vaccination status. This report describes the outbreak and the provision of MMR vaccine as part of outbreak management.
Materials and Methods
The school was attended by 540 pupils aged 10–19 y and had 170 staff. About 100 of the pupils were boarders living on the school site. We defined the population at risk as pupils and staff who attended the school between 1 January and 13 April 2013. We collected information on demographic characteristics from electronic school information systems, and clinical data (including vaccination history) from cases, their parents or their general practitioner. Information on vaccination history was also available from written medical records at the school in 422 of 540 children (78%).
We considered cases in 3 categories: confirmed, symptomatic, and asymptomatic. These 3 categories were ad hoc definitions for this particular study. Confirmed cases were members of the population at risk who had clinical symptoms of mumps (defined as swelling of one or more parotid, sublingual, or submandibular gland, with onset of symptoms between 1 January and 13 April 2013) and had a positive laboratory test for mumps. Symptomatic cases were members of the population at risk who had clinical symptoms of mumps but had a negative laboratory test for mumps. Asymptomatic cases were members of the population at risk who had acute onset illness without gland swelling, but with a positive laboratory test for mumps. Asymptomatic cases were tested because they were members of the population at risk and had acute onset febrile illness. A positive laboratory test result was defined as individuals with either a positive IgM response in serum or oral fluid, detectable mumps virus RNA (by PCR) in a clinical specimen, or a high IgG response (test/cut-off optical density > 20), typical of individuals with a secondary immune response to infection All testing was performed at Public Health England’s Virus Reference Department (Colindale).
The initial view from the school leadership was that they were unsure if parents would want their children to be given an additional dose of MMR. To estimate the number of parents who would wish for their child to have an additional dose of MMR we sent an online questionnaire via email to all parents on 8 February 2013, asking about vaccination status and willingness to receive a further MMR dose for each child as part of the outbreak response. We collected responses from parents up to 11 February. Vaccinations were administered on 12–14 February 2013. This intervention was organized and funded by Norfolk Primary Care Trust (PCT). Vaccinations were administered by a PCT-employed nurse and staff from a local general practice, with a licensed medical doctor on site in case of acute allergic reactions. Any subsequent adverse events were monitored by passive reporting.
We undertook a descriptive analysis of demographic data, vaccination history, and clinical outcomes. Vaccination status was classified as 0, 1, 2, or 3 doses of MMR or mumps specific vaccine. Cumulative incidences (attack rates) of mumps were estimated among subgroups of pupils by sex, school year, and boarder status. Differences in proportions between groups were assessed for significance (P < 0.05) using 2-sided Chi-square tests and Fisher’s exact test. We performed the analyses in Stata 12.0 (StataCorp LP).
Results
The population at risk consisted of 540 pupils and 170 staff. In total we identified 28 cases during the outbreak: 14 confirmed cases (50.0%), 11 symptomatic cases (39.3%), and 3 asymptomatic cases (10.7%).
The median age of cases was 14 y (range 12 to 45) and 19 cases (67.9%) were male. There were 24 pupils (22 d pupils and 2 boarders) and 4 members of staff. Vaccination status obtained from the general practitioner was available in 25 cases and among these 21 (84.0%) had a history of 2 doses of MMR while the remaining had a history of one dose (2/25 cases, 8.0%) or no doses (2/25, 8.0%) of MMR. Groin pain was reported by one male member of staff, but there were no known cases with a confirmed diagnosis of orchitis or oorphitis. An epidemic curve showing the distribution of cases by onset date of illness is shown in Figure 1.
Figure 1. Epidemic curve showing cases (n = 28) by onset of illness; Asymptomatic cases had acute illness with no gland swelling and a positive laboratory test for mumps; Symptomatic cases had acute illness with gland swelling and a negative laboratory test for mumps; and Confirmed cases had acute illness with gland swelling and a positive laboratory test for mumps. One symptomatic case with a negative laboratory test for mumps had onset of illness on 23 February had been vaccinated with MMR on 13 February.
Attack rates by sex, year group and boarding status are shown in Table 1. The overall attack rate in the population at risk was 5.0%. The highest attack rates were seen among pupils aged 13–14 y (attack rate 8.5%), 14–15 y (5.0%), and 15–16 y (13.7%). The attack rates in day pupils (4.8%) and boarders (2.7%) did not differ significantly (P = 0.56).
Table 1. Attack rates in pupils by subgroups.
| Subgroup | Cases (n) | Total (n) | Attack rate (%) | |
|---|---|---|---|---|
| Sex | Male | 18 | 345 | 5.2 |
| Female | 6 | 195 | 3.1 | |
| 11–12 | 0 | 14 | 0 | |
| Year group | 12–13 | 0 | 61 | 0 |
| 13–14 | 6 | 71 | 8.5 | |
| 14–15 | 5 | 100 | 5.0 | |
| 15–16 | 10 | 73 | 13.7 | |
| 16–17 | 1 | 86 | 1.2 | |
| 17–18 | 1 | 69 | 1. 5 | |
| 18–19 | 1 | 66 | 1.5 | |
| Boarder status | Boarder | 2 | 75 | 2. 7 |
| Day pupil | 22 | 463 | 4.8 | |
| Total | 24 | 540 | 5.0 | |
The online questionnaire about MMR vaccination was completed by parents of 156 of 540 children (28.9%) children, with parents of 110 (70.5%) children stating that they would like their child to have an additional MMR dose. The proportion of parents who gave this response was similar among parents whose child or children had previously received 2 doses of MMR (86 of 119 parents, 72.3%) or one dose of MMR (17 of 23 parents, 73.9%), but was lower among parents whose child or children had not previously received MMR vaccination (5 of 11 parents, 45.5%) (P = 0.045 for trend).
As part of the outbreak response additional MMR vaccines were administered to 103 pupils, at which point the vaccine supply was exhausted. The remaining 7 pupils were encouraged to contact their GP for vaccination and a letter was sent to their GP outlining the situation. Out of the 103 MMR vaccines administered, 76 vaccines (73.8%) were third doses of MMR. No adverse events were reported by clinical staff or the school in relation to vaccine administration.
Discussion
This is to our knowledge the first time an unconditional offer of MMR vaccination, regardless of prior vaccination status, has been used as a control measure for an outbreak of mumps in the UK. In previous outbreaks, MMR vaccination has only been offered to those who have previously received fewer than 2 doses of MMR. A third dose of MMR is not part of the immunisation schedule in England, but has been given as a public health response on several occasions in the US.7,8 The immunogenicity of a third MMR dose has not been extensively studied, but one evaluation following its use in an outbreak setting suggested that it was effective in eliciting an anamnestic immune response.9 In the present outbreak it was not possible to reliably assess the effectiveness of the additional MMR vaccine intervention given the small numbers of cases after the intervention. However, we found that the intervention appeared acceptable to parents and was feasible to organize and administer in a timely manner using available resources.
Most cases identified in the outbreak had previously received 2 doses of MMR vaccine; only 2 cases were documented as previously unvaccinated. Possible explanations for the high proportion of cases who were vaccinated could include waning vaccine-induced immunity,10 primary vaccine failure, antigenic variation among mumps viruses, and insufficient immunity when exposed to high levels of mumps virus in a school setting. The highest attack rate was observed in pupils in years 8, 9, and 10, which corresponds to children aged 13–16. These children would have been born between 1997 and 2000 and due to be vaccinated between 1998 and 2002. During this period, vaccine coverage fell as a result of adverse media coverage of the MMR vaccine.11 Given this, and because pupils might come from countries with varying vaccination coverage, there is continuing concern that boarding schools could be particularly susceptible to outbreaks of mumps and measles.12 Then again, in our report most of the cases identified had a history of receiving one or more doses of MMR vaccine.
The incubation period of mumps is 15 to 24 d (median 19 d).13 Few new cases of mumps were noted, once a typical incubation period had passed after vaccine administration. However, it is difficult to judge if there were few cases was because the vaccination intervention had been effective or because the outbreak had run its course.
A limitation of this study was the lack of an accurate vaccination history in all pupils. These data were not always accurately recorded in the school medical records, and it was not always possible to obtain the information from other sources. Given these limitations we could not calculate vaccination coverage rates for all pupils at the school. Our experience highlights the benefits of having accurate, electronic records available, to facilitate a rapid risk assessment in similar outbreak situations.
In summary, we provide further evidence that mumps outbreaks can occur in highly vaccinated populations and highlight the option of offering an additional dose of MMR as a public health measure in educational settings. Offering an additional dose of MMR to all pupils regardless of their vaccination status appeared to be acceptable to a large proportion of those parents who responded, and we found it feasible to administer the intervention in a responsive and timely manner. We recommend public health practitioners to consider offering an additional dose of MMR to all individuals at risk as an acceptable control measure for mumps outbreaks in school settings, even if the vaccination coverage is assumed to be high, although we emphasize that further evidence is needed to evaluate this intervention.
Glossary
Abbreviations:
- MMR
measles-mumps-rubella
- OCT
outbreak control team
- PCR
polymerase chain reaction
Disclosure of Potential Conflicts of Interest
The authors have no potential conflicts of interest to declare in relation to the study.
Financial Support
Erlend T Aasheim is funded by an Academic Clinical Fellowship from the National Institute for Health Research (NIHR).
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