Introduction

Since the beginning of 2008, France has been facing an increase of measles incidence. To date, 579 cases were reported in 2008 through mandatory notification, whereas in 2006 and 2007 the numbers of reported cases were 40 and 44 respectively.
Mandatory notification of measles was reintroduced in July 2005, as part of the National Plan for Elimination of Measles and Congenital Rubella. Physicians and microbiologists have to report suspected measles cases without delay to the local Public Health Officer [1]. Laboratory confirmation is strongly recommended for sporadic cases, either through serum or salivary testing. Oral fluid samples (for IgM detection and PCR) are sent to the National Reference Laboratory which also performs genotyping of the circulating viruses (5-10 cases should be sampled when a localised outbreak is investigated). Notification forms are collected and analysed centrally at the InVS.
The current measles vaccination strategy consists of two doses of measles-mumps-rubella vaccine (MMR) to be administered before the age of two years, the first one at 12 months of age and the second one between 13 and 24 months of age. A catch-up with two doses is recommended for children born after 1991 and with one dose for subjects born between 1980 and 1991.

Outbreak description

The ongoing outbreak began in spring 2008 with several clusters. The more important were reported in Burgundy and northern regions of France. A total of 110 cases were identified among elementary and secondary students of two private religious schools and their siblings. The index case was a 10 year-old Swiss girl who had been in contact with a measles case in Austria in mid-April [2,3,4]. Since summer 2008, other clusters and outbreaks have been reported with an upsurge of measles cases in October and a peak in November (131 cases). The virus transmission is still ongoing with 80 cases reported in January 2009 (Figure 1).

Figure 1. Number of reported measles cases by month, France, January 2008 - January 2009, preliminary data (n=659)

Despite the fact that most of the outbreaks were initially linked to schools affiliated with the same religious group as in Burgundy, in several regions the virus is currently circulating in the community and outbreaks in both private and public schools have been reported (Figure 2).  The most affected regions are in north-west and south-east.

Figure 2. Number of reported measles cases and incidence per 100,000 inhabitants, by districts, France, 2008



More than half (55%) of the cases reported in 2008 have been confirmed, either by detecting measles IgM antibodies or viral RNA by RT-PCR (265 cases) or by an epidemiological link with a laboratory-confirmed cases (54 cases). However, the proportion of laboratory-confirmed cases decreased from an average of 71% between January and July to an average of 38% between August and December 2008. Preliminary results from the National Reference Laboratory showed that three main genotypes were co-circulating: D5, D8 and D4, the predominant one being D5.

The median age of the 579 cases reported in 2008 was 12 years (range: 0-56 years). One third of the cases were aged 15 years or above (Table). Amongst the 26 cases less than one year old, 13 were aged between three and nine months (eight were laboratory-confirmed).

Table. Reported cases of measles and incidence rates per 100,000 population, by age group, France, 2008

Vaccination status was known for 548 cases (95%). Among these, the proportion of unvaccinated cases was 88.5% (Figure 3). Of the 63 vaccinated cases, 51 were vaccinated with one dose (9%), 11 with two doses (2%) and for one case the number of doses was unknown.

Figure 3. Vaccination status of measles casees by age group, France, 2008 (n=548)

Complications

Hospitalisation was required for 110 patients (19%) according to the notification forms received in 2008. Among these cases, 18 were diagnosed with pneumonia but no encephalitis was reported. Unfortunately, one unvaccinated French 12-year-old girl died in January 2009 in Geneva University Hospital from acute measles encephalitis.

Control measures

Several control measures were implemented by local health authorities, according to national guidelines. They include general information to the public, targeted information to the health professionals covering the affected area, and specific recommendations to pupils’ parents, the schools and the involved religious community administration where clusters are identified. The main recommendations are to undergo vaccination according to the national immunisation schedule and to propose post-exposure vaccination or immunoglobulin, depending on age, time since exposure and existence of risk factors of severe measles [1].

Discussion

Although measles incidence rates in 2006 and 2007 were below 0.1 per 100,000 inhabitants, suggesting near elimination, the current measles resurgence is not unexpected in the context of the still insufficient measles vaccination coverage allowing for silent accumulation of susceptibles. Current coverage at 24 months of age with at least one dose is estimated between 87 % and 90 % [InVS, unpublished data]. A survey carried out in 2005 has shown a coverage at 11 years of age of 96% for at least one dose of MMR, through catch-up vaccination beyond two years and a coverage for the second dose of 74% [5].

The data available through the routine notification system underestimate the actual measles incidence. During outbreak investigations, up to 10 times more cases have been identified than those notified to the local health authorities. This is the consequence of both the absence of medical consultation for a large proportion of the cases (especially when several cases occur within the same family) and the insufficient knowledge or motivation of some doctors regarding the notification procedure.

The current measles virus circulation in the community has been triggered by the clustered measles susceptibility in children belonging to traditionalist religious groups where measles vaccination coverage is low. The fact that these children often share the same schools and leisure activities such as summer camps have lead to several outbreaks in this group and to the secondary spread of the virus outside of this community. Efforts have been undertaken by the Ministry of Health to dialogue with representatives of the religious community regarding this specific measles vaccination issue.

The contribution of groups with low vaccination coverage due either to geographical or financial difficulties in accessing vaccination services or reluctance to measles vaccination for religious or philosophical reasons has been identified as one of the major impediments to achieve measles elimination in Europe [6,7,8].

In France, there are virtually no geographical or financial impediments in receiving the vaccine. The network of both private practitioners and public health clinics ensures optimal geographical access to measles vaccination. Furthermore, measles-containing vaccines are the only vaccines offered totally free of charge for children up to 13 years of age. If elimination in France is to be reached, the priority therefore lies in maintaining the efforts to persuade as many parents and health professionals reluctant to measles vaccination as possible. In the context of the current measles situation, communication to the general public and the health professionals has therefore been strengthened, amplified by the media attention drawn by the recent measles-related death case.

References

1. Republique Francaise. Ministère de la Santé et de la Solidarité. Plan for the elimination of Measles and Congenital Rubella in France 2005-2010. Paris: Ministère de la Santé et de la Solidarité ; 2005. Available from: http://www.euvac.net/graphics/euvac/pdf/plan_france_eng.pdf
2. Thierry S, Alsibai S, Parent du Châtelet I, on behalf of the investigation team. An outbreak of measles in Reims, eastern France, January-March 2008 - a preliminary report. Euro Surveill. 2008;13(13):pii=8078. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=8078
3. Noury U, Stoll J, Haeghebaert S, Antona D, Parent du Châtelet I, The investigation team. Outbreak of measles in two private religious schools in Bourgogne and Nord-Pas-de-Calais regions of France, May-July 2008 (preliminary results). Euro Surveill. 2008;13(35):pii=18961. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=18961
4. Cellule Interrégionale d'épidémiologie des Pays de Loire. [Investigation of measles cases among partcipants of a summer camp and their families – July 2008. Final report.] [in French]. Paris: Institut de veille Sanitaire; 2008. Available from: http://www.invs.sante.fr/publications/2008/rougeole_290908/rapport_rougeole_camp_49.pdf
5. Fonteneau L, Urcun J-M, Kerneur C, Guthmann J-P, Guignon N, Lévy-Bruhl D, et al. Couverture vaccinale des enfants ages de 11 ans, scolarisés en CM2, France, 2004-2005 / Vaccination coverage of 11 years old junior school-children (5th grade), France, 2004-2005. Bull Epidemiol Hebd 2008;51-52:493-97. Available  from: http://www.invs.sante.fr/beh/default.htm
6. Lernout T, Kissling E, Hutse V, De Schrijver K, Top G. An outbreak of measles in orthodox Jewish communities in Antwerp, Belgium, 2007-2008: different reasons for accumulation of susceptibles. Euro Surveill. 2009;14(2):pii=19087. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19087
7. Schmid D, Holzmann H, Abele S, Kasper S, König S, Meusburger S, et al. An ongoing multi-state outbreak of measles linked to non-immune anthroposophic communities in Austria, Germany, and Norway, March-April 2008. Euro Surveill. 2008;13(16):pii=18838. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=18838
8. Muscat M, Bang H, Wohlfahrt J, Glismann S, Molbak K, EUVAC.NET group. Measles in Europe: an epidemiological assessment. Lancet. 2009;373(9661):383-9.