Elsevier

Vaccine

Volume 30, Issue 41, 7 September 2012, Pages 5905-5913
Vaccine

Review
Measles outbreak in Europe: Susceptibility of infants too young to be immunized

https://doi.org/10.1016/j.vaccine.2012.07.035Get rights and content

Abstract

As women vaccinated against measles transfer low amounts of antibodies, an increasing number of infants lack early protection through maternal antibodies until being immunised themselves.

This paper reviews the literature on disease burden of measles in the population too young to be immunized according to the respective national recommendations during recent outbreaks in EU and EEA/EFTA countries. In addition, specific control strategies adopted to protect this young population are reviewed.

Pubmed, Unbound Medline, Web of Knowledge and the Eurosurveillance database were searched using MESH terms: measles and epidemiology, measles and infants, prevalence of measles, measles and outbreaks and measles and epidemic. Additionally, data from Euvac.net and ECDC were consulted. Databases were searched from January 2001 to September 2011.

Fifty-three papers were included in the analysis. The percentage of all measles cases during outbreaks affecting young infants ranged from 0.25% to 83.0%. Specific control strategies were adopted: e.g. administration of the first or second vaccine dose earlier than recommended.

Infants younger than 12 months are often involved in measles outbreaks, and advancing the first vaccine dose could reduce the burden of disease. However, immunization before 9 months of age is not systematically recommended because of dysmature humoral immune responses of infants. High coverage and timely administration of the recommended series of vaccines are the most important measures to decrease measles incidence and measles circulation and protect vulnerable infants from infection.

Highlights

► Literature is reviewed on measles among young infants during recent European outbreaks. ► Young infants are affected in 0.25–83.0% of reported cases during outbreaks. ► Specific control strategies are adopted for young infants. ► Advancing the first vaccine dose at younger age could reduce the burden of disease.

Introduction

In September 2010 the 53 member states of the European Region of the World Health Organization (WHO) adopted a renewed resolution on the elimination of measles and congenital rubella syndrome (CRS), with the goal of eliminating measles by 2015 [1]. Since 2005, the number of measles cases in western European countries has increased, with an incidence increasing from 3.5 cases per 1,000,000 inhabitants in 2005 to 11.4 cases per 1,000,000 in 2009 [2]. In 2010, 35,687 measles cases were reported in the WHO-European Region: the largest outbreak occurred in Bulgaria, accounting for 72% of all European cases [3]. For 2011, 37,075 cases have been reported in the WHO-European Region [4]. As predictable from sero-surveillance data in 2000 [5], a large outbreak began in France in 2008 and has persisted through 2011, with 6 fatalities in 2011. Major measles outbreaks in Europe are the consequence of susceptible age cohorts, the existence of pockets of susceptible people and circulation of the measles virus. Susceptibility can be explained by primary vaccine failure [6], insufficient vaccination coverage with the currently available vaccines [7] or waning immunity after one vaccine dose in combination with a lack of natural or vaccine boosting [6].

Infants under one year of age are too young to be immunized, according to most of the current immunization recommendations, and are no longer protected by passively transmitted maternal antibodies. These maternal antibodies remain present for an average of 3–6 months in infants of naturally immune women and even shorter in the offspring of vaccinated women [8], [9]. Determining the presence of maternal antibodies in infants is one way to measure susceptibility to measles infection; age specific case surveillance during outbreaks is another way. In Belgium, 12% of all measles cases in the 2011 outbreak occurred in the under one year age category [10]. Fig. 1 shows the number of measles cases by age (N = 68 among children younger than 12 months of a total number of 566 cases in 2011) in Belgium. In the same figure the decline in the proportion of infants protected by maternal antibodies is projected based on 2006–2008 data for Flanders, Belgium [8]. As expected, the population under one year of age becomes susceptible as soon as maternal antibodies disappear. Measles Mumps Rubella (MMR) vaccination is recommended in Belgium at the age of 12 months and 10–13 years. Vaccine coverage in Flanders, Belgium in 2005 was 94% with the first dose and 83.6% with the second dose [11].

The risk for measles-related complications is high in young children. In particular, otitis media, pneumonia, corneal ulcer and Subacute Sclerosing Panencephalitis (SSPE) are more frequent in young children than older children; SSPE occurs predominantly in children infected before 2 years of age [12]. The case fatality rate (CFR) of measles below 5 years of age ranges from 0.05% of all cases in industrialized countries to 5–6% of all cases in some African countries [13]. During a measles outbreak in a naïve population in Greenland (1951) the overwhelming majority of fatal cases occurred in infants younger than 1 year of age. The CFR was 37.7/1000, in children less than 1 year old compared with 5.7/1000 in 1- to 2-year-old children. The CFR further decreased with age [14]. In the WHO European Region, 52 measles-related deaths were reported between 2003 and 2009 [2]. Of these, 44% occurred in children aged 5 years or younger, and in 83% of all deaths, the individual had never received a vaccine. In 2011, 9 measles-associated deaths were reported, two deaths occurred among people aged <10 years [15].

This paper reviews the literature on the disease burden of measles in the population too young to be immunized according to the respective national recommendations during recent outbreaks in EU and EEA/EFTA countries. In addition, specific control measures adopted to protect this young population are reviewed and discussed.

Section snippets

Systematic literature review

The review of measles outbreaks was performed according to the MOOSE criteria (Meta-Analysis of Observational Studies in Epidemiology) [16]. Pubmed, Unbound Medline, Web of Knowledge and the database of Eurosurveillance were searched with the following MESH terms: Measles and epidemiology, Measles and infants, Prevalence of Measles, Measles and outbreaks and Measles and epidemic for the period from January 2001 to September 2011. This time frame was chosen because of the growing number of

Results of the search

The search results are shown in Fig. 2. The search produced a total of 303 papers for the past 10 years in Pubmed. On Unbound Medline, 252 papers were found, including two relevant papers not in the Pubmed search. The Web of Knowledge search produced 378 papers. The Eurosurveillance Archives database was additionally checked and produced 36 papers, of which 4 additional short communications that were missed in the other searches [18]. Ten more papers were found in the reference lists of other

Infants are often involved in measles outbreaks

Infants are susceptible to measles before receiving the first vaccine dose, independent whether the mother was vaccinated or contracted natural infection. Titres of maternal antibodies will further decrease because in the future increasing numbers of women will have been vaccinated. Together with other factors like increasing maternal age at delivery, less natural boosting due to high vaccine coverage and less natural virus circulation, an increase in susceptibility gap of infants will occur.

Conclusion

In Europe infants were prone to measles over the last 10 years and have often been involved in measles outbreaks (median 10.5% of cases during outbreaks). They are not well protected by their mother's passive antibodies. A susceptibility gap remains until the first dose of vaccine is administered, independent of whether the mother was vaccinated or naturally infected. For this reason, in at least 9 countries vaccination at the age of 6 or 9 months is recommended during outbreaks as well as

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