During 2009 and 2010, a mumps outbreak occurred in several communities in the northeastern United States. There were 3502 reported cases, primarily involving well-vaccinated, adolescent, Orthodox Jewish males. The demographic characteristics of the patients, with a disproportionate involvement of males 13 to 17 years of age, suggest that yeshivas (religious schools separated by sex in which Orthodox Jews study religious texts) for boys were foci of the transmission of mumps virus during this outbreak, just as colleges were foci of transmission during the 2006 mumps outbreak.7-9

The features of this outbreak are best explained by intense exposures, particularly among boys in schools, that overwhelmed the protection afforded by the vaccine. In general, Orthodox girls receive conventional schooling, whereas boys in yeshivas receive intense religious education starting at 12 years of age, with school days that are up to 15 hours long. Yeshiva study is typically interactive, involving a “chavrusa” (a study partner). Partners face each other across narrow tables or lecterns to study religious texts; the format is face-to-face, often with animated discussion. Frequently, several pairs of students study at a single table. A typical day involves several study sessions, with students changing partners for each session.

This chavrusa style of study may have allowed for particularly efficient transmission of mumps virus. Although mumps is a respiratory infection, it is spread through droplets and requires closer exposure than do more contagious respiratory infections transmitted by the airborne route, such as measles.21 We postulate that chavrusa study, with its prolonged, face-to-face contact, resulted in high-inoculum exposures and that such exposures overcame vaccine-induced protection in individual students.22 The role that the transmitted dose of a respiratory virus plays in the determination of vaccine effectiveness is difficult to study in humans, but challenge studies in animals that have been vaccinated with an avian influenza vaccine,23 epidemiologic investigations involving patients with measles who had previously been vaccinated,24,25 and biologic plausibility, as suggested from a comparison of challenge methods among volunteers who had been administered an inactivated mumps-virus vaccine,26 all suggest that the risk of infection with mumps may be higher when the exposure dose of virus is large or intensely transmitted. This phenomenon can also explain why the efficacy of the mumps vaccine tends to be lower among household contacts than among school or community contacts.27 If, in fact, the intensity of exposure reduced the effective protection provided by the mumps vaccine, the frequent daily changing of partners helps to explain why the disease spread in the yeshiva setting.

The finding that transmission of mumps to non-Orthodox persons in the affected communities occurred rarely and was not sustained in that population supports the conclusion that intense exposure is necessary to overcome an individual person's vaccine-induced immunity. Although Orthodox Jewish persons generally cluster geographically and socially, they often interact with their non-Orthodox neighbors and others who work within their communities or visit their communities. However, exposures in these settings would typically not be as intense as those in yeshivas. Notably, a large mumps outbreak in Jerusalem, Israel, during 2009 was linked to an importation from the U.S. outbreak. Orthodox Jewish adolescent boys, typically yeshiva students, were also disproportionately affected in that outbreak, even though their vaccination rates were high and they mixed regularly with their non-Orthodox neighbors.28

Over time during the outbreak, transmission shifted from adolescent boys toward older and younger male and female contacts, as the infected boys introduced the virus into their homes. Although household exposures might not have been as intense as those in the yeshivas, transmission probably occurred in these settings too, particularly given the large families that are characteristic of Orthodox Jewish communities. Among Orthodox Jewish households in Brooklyn with at least one case of mumps, the median number of persons per household was 7 (range, 2 to 16),29 as compared with an estimated aggregate household density for all of Brooklyn of 2.7 persons per housing unit.30

Although intense exposures within households, and especially within yeshivas, may have facilitated this outbreak, other factors may also have played a role. Results from outbreak settings suggest that vaccine-induced protection against mumps may wane,8,9,31 and neutralizing antibody titers, which may correlate with protection against mumps,32,33 decline after vaccination,34 although they remain sufficiently high to effectively neutralize mumps virus.35 However, the burden of mumps in this outbreak was not increased among the oldest vaccine recipients, who would have experienced the most waning since their childhood vaccinations. Evidence suggesting that waning immunity contributed to this outbreak may have been difficult to discern because of differences in exposure risk according to age and the strong correlation between age and time since vaccination. Another possible factor is reduced vaccine effectiveness against the outbreak genotype. The virus in this outbreak was genotype G, the genotype identified in the 2009 U.K. outbreak and the 2006 U.S. outbreak.7,36 Mumps vaccine in the United States includes the genotype A Jeryl Lynn strain, and antibody induced by this vaccine effectively neutralizes genotype G viruses, albeit at a lower titer.33,35

Nonetheless, neither waning nor reduced heterotypic protection alone would explain why an outbreak would affect particular communities while sparing broader adjacent communities. Although correlates of protection for mumps are not well defined, there is some evidence that lower titers before exposure to mumps may increase the risk of clinical disease after exposure.32,33 However, the high rate of infection among females in dormitories during the mumps outbreaks in 20069,17 and the high proportion of cases among males attending yeshivas in this study suggest that a high-density setting, in which there are certain behaviors that facilitate transmission of the virus, may overwhelm existing antibody levels. When a recent study did not identify an antibody-titer cutoff point for protection, it was suggested that the level of immunity required to protect against clinical mumps may depend on the inoculum of virus to which one is exposed, so that protection at a particular titer is not absolute.33

This study had several limitations. Some true cases of mumps were probably not included because some ill persons did not seek medical care, some properly diagnosed or suspected cases were not reported to the health department, some cases were misdiagnosed, and some cases were subclinical. Attack rates could not be calculated because the size and age distribution of the specific affected communities were mostly unknown. Vaccination histories were often incomplete among adults, since documentation was rarely available for patients who were no longer in school. Clinical specimens were tested at a variety of laboratories with the use of a variety of assays, and therefore, the results that were reported reflect a range of sensitivities and specificities. Although only 50% of cases with an available specimen were laboratory-confirmed, those with a negative test result had a clinically compatible illness (almost always parotitis) and were epidemiologically linked to an affected community, thus reducing the likelihood of overreporting.

The fact that the outbreak did not spread to surrounding communities highlights the effectiveness of the two-dose MMR vaccine schedule in most settings. Previous studies have shown that two doses of mumps vaccine have an effectiveness of approximately 88% (range, 79 to 95) in preventing clinical mumps,8,31,37 and this schedule has been successful in controlling mumps in the general U.S. population6; a similar schedule has resulted in the elimination of mumps in Finland.38 Since this outbreak, rates of mumps in the United States have been at near-record low levels, with only 370 provisional cases reported by the end of 2011.39 Other outbreaks have occurred in populations that had high rates of vaccination (as did the population in the 2009–2010 outbreak), but they were limited to specific settings with opportunities for intense exposures7-12 and did not spread to other communities, despite numerous opportunities. Finally, vaccination appeared to limit the severity of cases; complication rates were lower than rates reported during the prevaccine era.40 Nonetheless, although the current vaccination schedule has been successful, there remains an ongoing threat of imported infections and of endemic transmission of mumps virus. The outbreak reported here highlights the importance of maintaining a high rate of two-dose MMR vaccine coverage in all communities.