Elsevier

Vaccine

Volume 27, Issue 44, 19 October 2009, Pages 6186-6195
Vaccine

Mumps resurgences in the United States: A historical perspective on unexpected elements

https://doi.org/10.1016/j.vaccine.2009.06.109Get rights and content

Abstract

In 2006 the United States experienced the largest nationwide mumps epidemic in 20 years, primarily affecting college dormitory residents. Unexpected elements of the outbreak included very abrupt time course (75% of cases occurred within 90 days), geographic focality (85% of cases occurred in eight rural Midwestern states), rapid upward and downward shift in peak age-specific attack rate (5–9-year olds to 18–24-year olds, then back), and two-dose vaccine failure (63% of case-patients had received two doses).

To construct a historical context in which to understand the recent outbreak, we reviewed US mumps surveillance data, vaccination coverage estimates, and relevant peer-reviewed literature for the period 1917–2008.

Many of the unexpected features of the 2006 mumps outbreak had been reported several times previously in the US, e.g., the 1986–1987 mumps resurgence had extremely abrupt onset, rural geographic focality, and an upward-then-downward age shift. Evidence suggested recurrent mumps outbreak patterns were attributable to accumulation of susceptibles in dispersed situations where the risk of endemic disease exposure was low and were triggered when this susceptible population was brought together in crowded living conditions. The 2006 epidemic followed this pattern, with two unique variations: it was preceded by a period of very high vaccination rates and very low disease incidence and was characterized by two-dose failure rates among adults vaccinated in childhood.

Data from the past 80 years suggest that preventing future mumps epidemics will depend on innovative measures to detect and eliminate build-up of susceptibles among highly vaccinated populations.

Introduction

Mumps is an infectious viral disease, classically manifested by inflammation of salivary glands and fever [1]. Mortality is rare, but aseptic meningitis can affect 10% of case-patients [2]. Mumps is an important cause of pediatric deafness, and up to 37% of post-pubertal males develop orchitis, 13% of whom have impaired fertility [1]. In the absence of vaccination, most persons have been infected by young adulthood [2]. In 1967 a live, attenuated mumps virus vaccine was licensed in the United States, and by 2005 high two-dose childhood vaccination coverage reduced disease rates by >99% [3], [4].

In 2006 the US experienced a multi-state outbreak involving 6584 reported cases, with the highest attack rate among persons 18–24 years of age, many of whom were college students [4]. In affected colleges, most case-patients had received a second dose of the measles–mumps–rubella vaccine (MMR) ≥10 years previously [5], [6]. This was the first large-scale US mumps outbreak among two-dose vaccinees.

Waning immunity appeared to play a role in facilitating this outbreak, consistent with effectiveness data from the United Kingdom [7] and serological data from Finland [8]. However, certain epidemiologic features were unexpected. The onset was sudden – a >50-fold rise in case counts within a 30-day period, followed by a sudden decrease, so that three-quarters of the epidemic's total cases occurred within 3 months [4]. After a decade in which the geographical distribution of mumps cases had been proportional to population, 85% of case-patients during the 2006 epidemic came from eight rural states located in the central US, followed by a return to an unremarkable geographic pattern [4]. In parallel, the peak age-specific attack rate shifted suddenly from primary school children to the college age group, then began moving back toward primary school children [4], [9].

Previous resurgences of vaccine-preventable diseases in the United States had not shown these characteristics. The 1989–1991 measles resurgence had been preceded in the mid-1980s by a rising tide of incidence and increasing mean age of disease acquisition [10]. Lasting for 3 years, the measles resurgence saw outbreaks distributed widely across the US, but incidence was most intense in urban, rather than rural, areas [10]. The pertussis resurgence of the 1990s differed markedly from measles in many respects, but it too was widely distributed across the US, without any clear rural focality, and showed a slowly progressive pattern, both in terms of incidence and changing age-distribution [11].

We reviewed the history of mumps disease reports in the US to assess whether the 2006 resurgence patterns should have been unexpected – or whether they reflected recurrent phenomena that might shed light on the behavior of the mumps virus in the population, thereby helping us to anticipate and prevent future epidemics.

Section snippets

Data sources

National notification of mumps cases was begun in 1922, discontinued in 1950 (though some states continued to report voluntarily), then restored in 1968 [12]. Where incidence was unavailable (1922–1967), we used the method of Sistrom and Mergo to scan graphic data four times, recorded the average value, and then used a cubic spline to interpolate missing values [12], [13]. In 1968, printed monthly case counts by state were available. Beginning in 1977, case-patients’ age group was increasingly

Pre-vaccine Period: 1917–1967

Irregular epidemic cycles of relatively moderate amplitude (mean peak/trough 1.6, range 1.1–2.5) had a periodicity of approximately 3 years, and a superimposed secular trend peaked during World War II (Fig. 1A). By age 14 years, approximately 90% of urban children had been infected, with peak incidence at age 5–9 years [12], [16], suggesting that millions of cases occurred each year, but reported incidence was much lower (50–251/100,000). Cases were reported throughout the year, with highest

Discussion

Many of the unexpected features of the 2006 mumps resurgence had occurred before in the history of mumps activity in the United States. Both the 1986–1987 and 2006 resurgences were immediately preceded by historic low points in disease activity. Both resurgences had extremely abrupt onsets, with incidence rising 10- to >100-fold over baseline within a month. In both resurgences, a few states contiguously located in the central US contributed most cases. In both the 1986–1987 and 2006

Acknowledgments

The authors wish to thank Janaki Kari, MS and Randall Young, MA for producing maps; Angelia Eick, PhD and Steven Tobler, MD for advising on military incidence; Hayley Hughes, MPH for providing military vaccination policies; Kathleen Gallagher, DSc and Gregory Armstrong, MD for supervisory guidance; and Jane Seward, MBBS for subject-matter expertise. We also express appreciation to all US state and local health departments for collecting and submitting surveillance data.

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    The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention, US Department of Health and Human Services.

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