The incidence of measles has decreased in many countries
around the world since the introduction of immunisation.
In 1994, a policy was initiated in the Americas to
eliminate the disease. This has resulted in the interruption of the
virus’ autochthonous transmission in North America, and a substantial
decrease of its incidence in the rest of the Americas (1,2). European
countries, including France, have set themselves the goal of eradicating
measles by 2007 (3). In Finland, no autochthonous cases of measles have
been recorded since 1996 (4).
Is France on the way to achieving this goal? To answer
this question, this article presents an overview of the epidemiology
of measles in France.
Evolution of the immunisation policy
The vaccine came on the market in 1966 in France and
was introduced into the vaccination schedule in 1983, for children between
the ages of 12-15 months. Three years later, mumps and rubella vaccination
was added to the measles vaccine.
In 1996, a second dose, justified by the elimination
prospect of the disease was introduced for children aged 11-13 years.
This second dose enables us to protect children who have missed vaccination,
and also those for whom it was not effective (there are failure rates
of between 5 and 10% after the first dose). This prevents the accumulation
of non-protected subjects, thereby hampering the emergence of clusters.
Modelling studies (5) have shown that the disease could be eliminated
faster if the second dose were given to children at a younger age, and
recommendations are now to give it to children between 3 and 6 years
of age (6).
Up to the age of 6, two doses are administered. After
6 and until 13, only one dose is offered to those who have never been
vaccinated. Vaccination is carried out mostly by doctors in private
practice. Campaigns are carried out each year to promote the triple
vaccine for measles, mumps and rubella (MMR). The focus of the 1999
campaign was that the vaccine was available free of charge. This action
gave the vaccine a priority status by making it more accessible.
Vaccination coverage surveillance
Since 1985, data on vaccination coverage have been
collected and managed by the Direction de la Recherche des Etudes de
l’Evaluation et des Statistiques (DREES) at the Ministry of Health.
National and departmental evaluations rely on the yearly
analyses of health certificates filled by the doctors at a child’s twenty
fourth month. Although these are mandatory, the certificates of only
60% of children aged 24 months are sent and analysed by the DREES. Coverage
for the first dose alone is evaluated. Moreover, twice-yearly transversal
surveys are carried out in schools using a representative sample of
the French population aged 6 years.
National coverage of 24 month old children was 32%
in 1985 and reached 80% in 1994. It has been stable since then (figure
1). It was 82.7% in 1999 and varied from 60.5% and 92.3% depending on
the departments. Northern France attained the highest coverage rates
(7) (figure 2). Provisional data for 2000 showed an 84.2% coverage rate.
During the last survey conducted in 2000-01, coverage
for six year olds was 90%. This shows that catch up vaccination was
incomplete for children over the age of 2 years (8).
Surveillance of morbidity
In 1945, measles was made a notifiable disease, but
this notifiable status was suspended in 1986 because of the low level
of notifications being made by doctors.
The Sentinel network, created by the INSERM U444 has
been monitoring measles since 1985 (9). It is composed of around 300
volunteer general practitioners, who report electronically the number
of measles cases observed during their consultations each week. The
case definition, comparable to the one used by the Centers for Disease
Control and Prevention (CDC) (10) includes generalised rash of more
than three days, and a fever above 38.5 °C, associated with coughing,
coryza or conjunctivitis.
Since its creation, the network doctors have reported
more than 8000 cases of measles. National incidence, extrapolated from
this data, has decreased considerably, from nearly 300 000 cases per
year in 1985 to around 10 000 cases in 2000 (figure 3).
At the same time, the Sentinel network observed an
increase in the age of the cases. The proportion of patients over 10
years old rose from 13% in 1985 to 48% in 1997. The proportion of vaccinated
cases also increased from 3% to 58% over the same period. This increase
primarily reveals the improvement of vaccination coverage. Until 1998,
these rates were calculated from more than 200 cases described by the
network doctors. In 1998, this number was reduced to around fifty cases,
which has made data interpretation very difficult.
Surveillance relies on clinical data alone, and presently
no laboratory confirmation of cases or procedure for the typing of strains
Alongside this surveillance system, data on morbidity
has been reported during the investigation of clusters or small outbreaks.
From 1995 to 2000, seven investigations were led by or reported to the
Institut de Veille Sanitaire. Vaccine efficacy, calculated in two primary
schools and a high school on clinical and biologically confirmed cases
has always been over 92% (11,12).
Surveillance of mortality
Data on mortality is collected by the epidemiological
centre for the medical causes of deaths (Centre d’Epidémiologie
sur les causes médicales de décès, CépiDc).
This data has been available since 1979.
Only information regarding the main causes of death
has been analysed. A detailed study including all the recorded causes
of deaths (principal, associated and immediate) showed that only two
deaths were not included in the 35 main causes registered from 1995
and 1998. This represents a 5% underestimation of the number of deaths
Mortality has decreased steadily, from around 30 deaths
per year in the 1980s to less than 10 per year at the present time.
The proportion of deaths in children under five years of age decreased
from over 50% in 1979 to less than 5% in recent years (figure 4).
In the same period, the main causes of death also changed.
From 1979 to 1987, causes other than encephalitic ones represented the
majority of deaths, bronchopneumonias being responsible for 34% of the
other causes. Since 1987, encephalitis is the first reported cause of
deaths, whether it is late encephalitis occurring a few years after
measles (subacute sclero-sing panencephalitis) or acute immediate or
delayed post-measles encephalitis occurring a few days or months after
A European seroepidemiological survey (13) (ESEN) was
carried out in seven countries. Immuno-globulins G of nearly 29 000
serum samples were analysed with standardised titration methods (14).
In metropolitan France, serum samples came from subjects
whose blood samples were drawn in medical laboratories. The choice of
serum samples was made according to predefined quotas by age group,
sex, and location to ensure a satisfactory representativeness without
random sampling (15).
In France, about 3500 serum sampled mainly in 1998
were analysed (13) (figure 5). Results for measles showed an important
rate of seronegative children (7% in those aged between 5 and 19 years).
Rates of seronegatives observed in all age groups under 20 are higher
than seronegativity thresholds proposed by the WHO European region to
reach the objective of measles elimination. Serological data have also
confirmed that the half southern metropolitan France, as defined in
figure 2 was less protected than the northern half.
Only the data from the Permanent Medical Prescription
Survey (16) currently allows us to appreciate the implementation of
catch up doses for children up to the ages of 11-13, and the introduction
of the second dose in 1998, through the analysis of prescriptions made
by private practitioners.
This survey is carried out by a list of GPs and specialists,
from which is selected a representative sample stratified according
to the doctors’ region and activity level. During a period of seven
days, the doctor reports a set of information on all his or her patients,
as well as copies of all prescriptions. The results are then extrapolated
to all French practitioners, yielding national incidence estimates.
In children under the age of two and a half years,
the rate of prescription of the triple vaccine has remained stable since
1996, data confirmed by the stagnation of vaccine coverage at 24 months.
The rate of prescription has increased in children aged between two
and a half and seven years of age since 1997, when the age for the second
dose was lowered, yielding a coverage for the second dose of about 50%.
Finally, in children over seven years of age, prescriptions have increased
widely, although it has been impossible to dissociate vaccines administered
as late second doses from those corresponding to first doses in non-vaccinated
children. The decrease of cases registered by the Sentinel network in
recent years favours the second hypothesis (figure 6).
Since 1983, promotion of measles vaccination has been
accompanied by a 97% reduction in morbidity and a 60% reduction in mortality.
These encouraging results are not equivalent to elimination. Stable
and suboptimal coverage around 84% causes a shift in the age of patient,
and the continuation of disease transmission within the country.
Because of the reduced circulation of the virus, measles
cases now occur in older patients. But complications are more frequent
and case fatality ratio is higher in adults, with acute encephalitis
being the major cause of death (17). This age shift in cases could therefore
partly explain the slower decrease of mortality compared to morbidity,
a stable number of deaths caused by post-measles encephalitis since
1988, and the increase in the age of the deceased patients. Deaths caused
by subacute sclerosing panencephalitis occur about ten years after infection
by the measles virus, and do not reflect the current incidence of the
disease, although they illustrate the severe potential of a disease
that is too often considered to be totally benign.
These paradoxical effects of vaccination linked to
the age shift can be fought only by eliminating the disease, and this
requires a vaccine coverage of more than 95% and the administration
of two doses of an efficient vaccine.
The vaccine used in France is of good quality considering
that the measures of vaccine efficacy carried out in investigations
of clustered cases have always been over 90%. However, the coverage
reached is not high enough to avoid the accumulation of susceptible
subjects, as confirmed by serological surveys and the occurrence of
epidemic clusters. France is still in the ‘honeymoon’ period, the name
given when the decrease of cases suggests that a disease is disappearing,
yet without any sign, groups of unprotected individuals are forming
the source of future outbreaks. Vaccination efforts have allowed an
important decrease of incidence without preventing the silent formation
of these groups. Important catch up activities in recent years have
probably reduced these groups of susceptible subjects without causing
them to disappear. Geographical differences are important, and alongside
national promotional campaigns, each department must strive to identify
the populations with the lowest vaccination coverage in order to find
solutions. This search is made possible by the measurement of local
vaccine coverage, the identification of clusters, and notification of
Improving vaccine coverage must be accompanied by a
change in the surveillance system. The decrease of incidence makes the
estimates from the Sentinel network very imprecise. In 2001, incidence
was extrapolated from 22 reported cases; the 95% confidence interval
was 2870-14050 (18). The decrease in the number of cases also ‰
‰ decreases the positive predictive value of the clinical
definition. In England and Wales, 2466 cases of measles were reported
from the clinical definition in 2000, 1751 (71%) had a saliva sample,
of which 74 (4 %) only were positive (19).
In the long term, surveillance tools should be those
used by the countries which are most advanced in the elimination process
(20), namely: exhaustive notification; wide clinical definition for
high sensitivity allowing detection of all suspect cases; biological
confirmation to improve specificity and to take into account real cases
only; typing of strains to trace their origin; measure of vaccine coverage
for each dose; and evaluation of the rate of susceptible population
by modelling or serological survey.
As clusters affect communities, school doctors should
be involved in the surveillance of the disease. Protocols for procedures
to be followed when one or several cases occur will be developed to
encourage case notification and investigation.
Research projects are led by the Sentinel network,
in collaboration with the Public Health Laboratory Service (PHLS) in
London and are related to the evaluation of the saliva diagnosis by
IgM detection and virological typing of strains. The results will contribute
to setting up the biological support to eliminate the disease.
In conclusion, France has improved its vaccine coverage,
but the rate reached still permits transmission of the disease, and
shifts the age of the cases to an age where complications and case fatality
ratio are higher. To eliminate the disease, vaccine coverage over 95%
with two doses will have to be reached.
All the tools can gradually be implemented to reach
this objective. The main obstacle, however, is to convince the policy
decision makers, the health professionals, and the public of the need
to eliminate the disease.