ESEN: a comparison of vaccination programmes – Part three : measles mumps and rubella

Daniel Lévy-Bruhl (coordinator), RNSP/CIDEF, France
Richard Pebody, NPHI/EPIET, Finland
Irene Veldhuijzen, RIVM, Netherlands,
Marta Valenciano, RNSP/EPIET, France
Kate Osborne (ESEN project coordinator), CDSC, England and Wales

from data provided, on behalf of the ESEN project, by :

Martine Le Quellec Nathan, DGS / Nicole Guérin, CIDEF, France
Richard Pebody, NPHI, Finland
Anne-Marie Plesner, SSI, Denmark
Mary Ramsay, CDSC, England and Wales
Patrick Olin, Victoria Romanus, SIIDC, Sweden
Stefania Salmaso, Christina Rota, ISS, Italy
Marina Conyn-van Spaendonck, RIVM, Netherlands
Wolfgang Vettermann, Doris Altmann, RKI, Germany


This is the last of a series of three articles that compare vaccination programmes, immunisation schedules, vaccine coverage and the epidemiological impact of immunisation against diphtheria, pertussis, and measles, mumps and rubella in eight countries (Denmark, England and Wales, Finland, France, Germany, Italy, Sweden and the Netherlands). This analysis has been undertaken within the EU funded European Sero-Epidemiology Network (ESEN) (1). The methodology of the analysis, the characteristics of the immunisation programmes and the results for diphtheria and pertussis have been presented in the first two papers of the series (2,3). This article presents the results for measles, mumps, and rubella (MMR).


Immunisation schedule

All countries except Italy now have two dose strategies, with the first dose given between 1 and 2 years of age (table 1). The age at which the second dose is given ranges from 3.5 to 12 years. Several countries also undertook catch-up programmes either before or during introduction of the second dose.

Table 1: Measles vaccination characteristics according to level of control of the disease in eight European countries

Very high control level

High control level

Low control level




England and Wales





Incidence since 1990 (per 100 000)

< 1

< 1

0.4 – 3.5

20 – 35 (up to 1994)

0.4 – 3

Not notifiable

75 – 300 sentinel surveillance

10 – 120

Laboratory confirmation of suspected cases






Not applicable



% of cases over 10 years (year range)

8/9 cases (1994-96)

Not available

25 % (1994-96)

> 20 % (1992-94)

25 % (1993-95)

Not available

> 30 % (1993-95)

> 30 % (1990-94)

Date of onset of measles vaccination






GDR : 1970 GFR : 1975



MMR vaccination schedule

1982: 2 doses 18 months / 6 years

1982: 2 doses 18 months / 12 years

1987: 2 doses 15 months / 12 years

1988: 1 dose 12-18 months 1996: 2nd dose at 3,5 – 4 years

1987 : 2 doses 14 months / 9 years

1980: 1 dose 15 months 1991: 2nd dose at 6 years

1986: 1 dose 12 months* 1997: 2nd dose at 3-6 years + catch-up 11-13 ans

1982: 1 dose at 18 months

Coverage with first dose (1995-96)






Not available



Yearly coverage assessment









Coverage target







More or less


% vaccinations in public sector









% costs at recipient’s expense







Public: 0 % Private: 30 % to 35 %


* 1983 : 1 dose Measles Rubella at 12 months.Surveillance

Measles is a notifiable disease in all but two countries (France and Germany). France discontinued measles notification in 1985 and subsequently introduced a sentinel surveillance system. All the countries except France and Italy seek laboratory confirmation of suspected cases of measles. In Finland all suspected cases are laboratory tested, whereas only a fraction of all suspected cases are tested in Denmark, England and Wales, the Netherlands, and Sweden.

Vaccine coverage and epidemiology

The participating countries have been classified into three groups according to the incidence of reported measles cases in the past five years (very high level of control: < 1 case per 100 000, high level of control: 1-50/100 000, and low level of control: > 50/100 000) (table 1). Over 20% of cases in all countries are aged 10 years or over.

Finland and Sweden have virtually eliminated measles. They both introduced vaccination against measles in the 1970s and a two dose MMR strategy in 1982, which almost immediately achieved a very high coverage.

Denmark, England and Wales, and the Netherlands have achieved a high level of control of measles. Denmark introduced a two dose MMR vaccination schedule in 1987. Coverage has risen from 80 % in 1989 to 88 % in 1995, and the annual incidence declined dramatically to less than 3/100 000 between 1992 and 1996.

Single dose vaccination against measles was introduced in the Netherlands in 1976 with immediate coverage between 90% and 95 %. In 1987 measles vaccine was replaced by two doses of MMR (at 14 months and 9 years) with the same level of coverage, and a catch-up campaign for 4 year olds was carried out. Since 1990, the annual incidence of confirmed cases has not exceeded 3/100 000.

The single dose measles vaccination schedule introduced in 1968 in England and Wales was replaced by single dose MMR in 1988. Coverage remained below 80% until 1988 with disease incidence exceeding 100/100 000. Coverage has risen to above 90% during the 1990s and the incidence has fallen to less than 20/100 000. A second dose of MMR for 4 year olds was introduced in 1996.

Two countries are classified as having low levels of control: Italy and France. In Italy, single dose measles vaccine has been available since 1979. Estimated coverage from cluster sample surveys remained below 50% until 1994 and was 56% in 1997. The incidence varies between 40 and 140/100 000, with regular epidemics. In France, single dose measles vaccine has been available since 1966 and MMR since 1986. Vaccination coverage has levelled off since 1991 at around 80% and the average annual incidence remains around 100/100 000. In 1996 a second dose of MMR was introduced for 11 to 13 year olds. The age at which the second dose is offered was reduced to 3 to 6 years in 1997, in response to mathematical modelling of measles in France facilitated by the ESEN project (4). A catch-up for unvaccinated boys and girls aged 11-13 was maintained.

In Germany, where measles vaccination (MMR) includes one dose at 15 months and a second at 6 years, no data on disease incidence or coverage are available.


Although the performance of the surveillance systems varies between countries, our classification based on the reported incidence of measles should be robust. In Finland, no case of measles has been confirmed since 1996, although about 2000 suspected cases are tested each year (5); in Sweden, only a few imported cases and cases among groups who oppose vaccination still occur; the very low incidence of notified measles in countries in the high control group, even if underreporting exists, makes it very unlikely that the real incidence of measles in these countries could exceed 50/100 000.

A two dose strategy with coverages higher than 95% appears necessary to reach elimination. In the Netherlands, transmission of measles seems not to have been interrupted despite coverage of 90% to 95% with two doses for 20 years. Countries like France, England and Wales, where vaccine coverage remained under 80% for many years with no catch up programme, have built up large cohorts of susceptible people in older age groups, with the result that the average age of cases has increased. This pool of susceptibility represents a potential for large outbreaks with more severe disease, as older cases are more likely to suffer severe illness. Serological surveillance in England and Wales confirmed the accumulation of susceptible people and led to a catch-up campaign being targeted at children aged 5 to 16 years in 1994. Serological and epidemiological data collected since the campaign suggest that England and Wales is approaching the elimination of endemic measles transmission with an incidence below 1/100 000 (6).

In France, efforts are currently underway to increase vaccination coverage at various ages. Denmark may actually be in a ‘honeymoon period’, with a very low incidence currently, but a history of moderate coverage and thus an increasing pool of people without immunity to measles.

The three groups defined according to their level of measles control differ by parameters other than coverage and incidence (table 1). The countries with poor control of the disease are those where the private sector plays a substantial or even major role in delivering immunisation (France, Germany, and Italy). In such countries immediate and extensive implementation of immunisation strategies and targets may be more difficult. The cost of vaccination for recipients in France and Italy may also be an obstacle for vaccination. These three countries illustrate other characteristics that may also reflect a lower level of priority given to measles control. Germany and Italy do not measure coverage routinely and no immunisation targets are set. Measles is not notifiable in France and Germany.


Immunisation schedule

Most of the participating countries introduced rubella vaccine as selective vaccination for prepubertal girls in the 1970s in order to prevent rubella infections in pregnant women. Some countries included a programme to vaccinate older susceptible people. Only Denmark and Germany introduced rubella vaccination later as part of routine MMR immunisation for all children, in 1980 and 1987, respectively. In the late 1980s, epidemiological data and results of mathematical modelling showed that the selective strategy alone could not eliminate congenital rubella syndrome (CRS) (7), and all the countries with selective vaccination strategies introduced MMR vaccination for young children of both sexes. Selective vaccination ceased when the universal strategy was implemented (the Netherlands and Sweden) or after a few years of mixed strategy (England and Wales and Finland). Rubella vaccination therefore now shares the same schedule and levels of coverage as measles vaccination. In Denmark, France, Germany, and Italy however, catch-up doses are still indicated for unvaccinated or susceptible girls or women.

Surveillance and epidemiology

Methods of rubella surveillance vary widely, limiting comparisons between countries. In England and Wales, Finland, and Sweden only laboratory confirmed cases are notifiable whereas in Italy and the Netherlands notifications are only made on clinical grounds. In France, and in Denmark since 1994, only infections during pregnancy and CRS are under surveillance. Germany monitors CRS only. England and Wales monitor both all rubella cases and infections during pregnancy.

Finland and Sweden have virtually eliminated rubella. In Denmark, England and Wales, and the Netherlands lack of immunity in older children and young adults, especially males, has led to persistence of infections during pregnancy despite a dramatic reduction in the overall incidence of rubella due to high coverage in children. In France and Italy the rubella virus is still circulating significantly. In Italy the shift of infections towards higher age groups due to poor coverage in both childhood and teenage girls is of great concern and may lead to an increasing number of infections during pregnancy . No data are available from Germany, where the virus is likely to circulate widely.


Data from Finland and Sweden show that rubella can be eliminated with very high levels of coverage with a two dose MMR strategy. The second dose essentially acts as a catch-up of older susceptibles, the primary failure rate for rubella vaccination being very low. However, because of the early age of administration of the second dose, Finland needed to undertake supplementary immunisation activities to fill the immunity gaps in older children or young adults.

Data from Denmark and the Netherlands show that coverage below 95%, even with two doses in childhood, is insufficient to eliminate CRS, because of immunity gaps in older populations. It may be sufficient if catch-up activities are carried out in these older age groups. Recent experience in England and Wales shows that circulation of rubella virus is now mainly sustained through a gap in immunity in males too old to have been covered by the 1994 campaign (8).


Immunisation schedule and surveillance

Routine vaccination for mumps was introduced in all countries during the 1980s and the vaccine is now given as part of MMR. The immunisation schedule, vaccination coverage, and surveillance of mumps and measles are the same.


Finland and Sweden have virtually eliminated mumps.

In Denmark, where mumps vaccination was introduced as MMR, a high level of mumps control has been achieved. The annual incidence based on notification has remained under 1/100 000 since 1994. A third of the cases are over 20 years of age.

In the Netherlands, the introduction of a two dose schedule of MMR was followed immediately by a fall in incidence to less than 1/100 000. The average proportion of notified cases over 20 years of age has been over 27 % for the 1989-1996 period.

In England and Wales, in 1988, after MMR vaccine was introduced, the incidence decreased from between 220/100 000 and 600/100 000 in the 1981-88 period to less than 50/100 000 in the 1991-95 period.

The countries with the highest incidence rates are Italy and France. In Italy the annual incidence is still between 50 and 100/100 000 with less than 20 % of cases over 15 years of age. In France incidence exceeds 80/100 000 and the age distribution is stable (8% to 10 % of cases were over 20 years of age from 1986 to 1988 and 11% to 13 % from 1993 to 1995).

No data are available for Germany.

The generalised use of MMR has made the situation for mumps control like that of measles.


Vaccine effectiveness, level of immunity needed to interrupt the circulation of the virus and probably duration of immunity, differ between the three antigens of the MMR vaccine, But the levels of control of the three diseases achieved in individual countries are very similar and depend mainly on the number of doses and levels of coverage. Very high levels of coverage with two doses of MMR have resulted in Finland and Sweden reaching the WHO/EURO targets of an incidence of less than 1/100 000 for measles and mumps. Data from Denmark, England and Wales, and the Netherlands show that those countries should reach these targets soon.

The success of the measles and rubella campaign carried out in England and Wales in 1994 and its impact on transmission of the diseases shows that countries with insufficient past control over the disease can make up for it, provided that measures are taken to prevent the accumulation of new cohorts of susceptibles. This requires a high level of commitment from the health authorities, which has to be translated into the setting of targets, implemention of managerial tools, and mobilisation of resources. The measles elimination objective currently being adopted at the European level will represent a major challenge for countries in the low level control group, especially as their immunisation delivery services have less favourable characteristics for the rapid achievement of high levels of coverage. If achieved, the benefit will be further enhanced by simultaneous interruption of indigenous transmission of mumps and elimination of CRS.

Comparisons between countries are constrained by the lack of comparability of coverage and surveillance data. Availability of standardised serological data through the ESEN project will allow more detailed comparisons.

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3. Lévy-Bruhl D, Pebody R, Veldhuijzen I, Valenciano M, Osborne K. ESEN: a comparison of vaccination programmes – Part two: pertussis. Eurosurveillance 1998; 3: 107-10.

4. Lévy-Bruhl D, Maccario J, Richardson S, Guérin N. Modélisation de la rougeole en France et conséquences pour l’âge d’administration de la seconde vaccination rougeole-oreillons-rubéole.Bulletin Epidémiologique Hebdomadaire 1997; 29:133-5

5. Peltola H, Davidkin I, Valle M, Paunio M, Hovi T, Heinonen OP, et al. No measles in Finland. Lancet 1997; 350: 1364-5.

6. Gay N, Ramsay M, Cohen B, Hesketh L, Morgan-Capner P, Brown D, et al. The epidemiology of measles in England and Wales since the 1994 vaccination campaign. Commun Dis Rep CDR Rev1997; 7: R21-6.

7. Anderson RM, May RM. Vaccination against rubella and measles: quantitative investigations of different politics. Journal of Hygiene (Cambridge) 1983; 90: 259-325.

8. Miller E, Waight P, Gay N, Ramsay M, Vurdien J, Morgan-Capner P, et al. The epidemiology of rubella in England and Wales before and after the 1994 measles and rubella vaccination campaign: fourth joint report from the PHLS and the National Congenital Rubella Surveillance Programme. Commun Dis Rep CDR Rev 1997; 7: R26-32

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