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Six years later, an article in this issue of the Journal (pages 447–455) describes a 2005 measles outbreak in Indiana. Begun when a 17-year-old girl who was incubating measles returned to Indiana from Romania, the outbreak ultimately involved at least 34 persons, 1 of whom had life-threatening illness. With U.S. vaccination coverage at record levels, how could one imported case of measles lead to such an outbreak? This example illustrates the highly infectious nature of measles and the vulnerability of vaccinated communities in a world in which the virus continues to circulate.
Measles is an acute infectious disease that can affect persons of all ages but is most severe in young infants and adults. Person-to-person transmission occurs through direct contact or droplet spread, and there is some evidence that severity is related to infective dose, so that those who acquire the disease from close household contacts have the most severe disease.2 Infected persons can infect others during the prodromal period before the characteristic rash appears, creating ample opportunity for people who are incubating the disease to travel from a country where the virus is circulating, such as Romania or India (the latter being the probable origin of an outbreak in Boston in the spring and early summer of 2006), and bring the virus with them.
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At the time of the 2005 outbreak, the level of vaccination coverage in Indiana was 98 percent for the second dose delivered to school-age children. In such a setting, it can be expected that the number of vaccinated persons who do not acquire protective immunity will be small, so the primary group of persons who are susceptible to the disease will consist of those who are unvaccinated. An important subgroup will be children who are too young to be vaccinated. These infants become susceptible when maternal immunity wears off, and they remain susceptible until they are immunized.
There is evidence that maternal immunity is declining in some countries because, without the boosting effect of circulating wild virus, mothers must rely on immunity from their own vaccinations (which were usually delivered in the second year of life). As a result, infants become susceptible to measles earlier in the first year of life, thereby increasing the number of susceptible persons present in a community at any given time. The susceptibility of young infants is of particular concern, since they are more likely than older children to have severe disease if they become infected.
Furthermore, a generation of young adults with waning, vaccine-derived immunity may become susceptible to some extent to wild measles infection, although the role of such "secondary vaccine failures" in measles epidemiology is unclear. The longer a community goes without circulating measles virus, the more vigilant public health officials must be to maintain immunity levels in the community.
The Indiana outbreak was striking for a number of reasons. All but two of the cases occurred in unvaccinated hosts, indicating that it was the failure to vaccinate rather than vaccine failure that caused the problem. Five hundred people were reportedly present at the church gathering where the initial U.S. transmission occurred. Church officials estimated that 10 percent of them were unvaccinated, but it is unclear how they knew this or how accurate their estimate was. It seems unlikely that the person with the index case of measles could have directly infected 32 percent of all susceptible persons at the meeting, and I would suggest that the number of unvaccinated persons there may have been higher. But even 10 percent is a high proportion in a state with 98 percent coverage for the second dose of measles vaccine, despite the fluctuations in coverage that may have occurred during the lifetimes of those who became infected, most of whom were younger than 20 years old.
Community-based data such as levels of vaccine coverage represent averages for a district, state, or country; although homogeneity may seem to be implied, it never exists. Moreover, objection to immunization tends to occur in clusters, sometimes affecting whole communities. Thus, even with excellent coverage, there remain subgroups in which conditions suitable to an outbreak may persist. Large gatherings of these groups provide an ideal setting for transmission, and if a person who is incubating the disease attends such a gathering, an outbreak is inevitable.
Of the two vaccinated persons who acquired measles in Indiana, one was 34 years old and had been vaccinated only once in infancy. We cannot tell whether this case represents a primary vaccine failure (a failure of the vaccine to induce immunity) or a secondary vaccine failure (the result of waning immunity). The severity of the case suggests the former, since secondary vaccine failures tend to produce mild disease.4 In addition, a 16-year-old student acquired measles despite having received two doses of measles vaccine during early childhood.
In the United States, measles vaccine is delivered in combination with mumps and rubella vaccines. Although the two-dose strategy ensures that a high proportion of vaccinees will be immune to measles (seroconversion after two doses of vaccine is estimated to be 98 percent), the conversion rate is lower for mumps (approximately 88 percent). Thus, the proportion of persons in a U.S. community who are susceptible to mumps is greater than the proportion who are susceptible to measles, and outbreaks, when they occur, will be larger.
More than 50,000 cases of mumps have been identified in the United Kingdom during the past few years, and more than 2500 cases have already been identified in a U.S. outbreak this year.5 About half the persons affected in the U.S. outbreak had been vaccinated, and most were young adults. Although mumps is a less severe disease than measles, it does cause substantial illness, including parotitis, orchitis, and aseptic meningitis. These outbreaks demonstrate the potential for rapid dissemination of respiratory pathogens, facilitated by air travel and crowded conditions.
Despite the vision of the public health officials of the 1960s, global eradication of measles remains a long way off. In the meantime, countries must strive to immunize as high a proportion of children as possible, using a second dose to minimize the risk of primary vaccine failure and improve coverage. Better understanding of the epidemiology of measles in vaccinated communities will permit the optimization of vaccination strategies. The importation of virus can be minimized by ensuring that travelers to and from regions where the viruses are endemic provide evidence of immunization. Yet as long as measles continues to circulate in other parts of the world, cases will continue to be imported. And as long as some groups within a given community respond to spurious claims about the risks of the vaccine by refusing to vaccinate their infants, further outbreaks will occur even in industrialized countries.
Source Information
Dr. Mulholland is a professor in the Infectious Disease Epidemiology Unit of the London School of Hygiene and Tropical Medicine, London.
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