Mumps is an acute, viral illness that classically manifests with fever and parotitis; 15%–27% of infections are asymptomatic.1–3 Severe complications include encephalitis,4 deafness5,6 and orchitis.7 Mumps vaccine was licensed in the United States in 1967 and recommended for routine use in 1977.8 A second dose of measles–mumps–rubella (MMR) vaccine was recommended for all school-aged children and select high-risk groups in 1989 for measles prevention.9 Due to high 2-dose MMR vaccine coverage, rates of reported mumps in the United States declined by over 99% in 2005 compared with the immediate prevaccine era.10 Annual mumps incidence in the United States was approximately 1 case per million population (0.9−1.2 per million/population) between 2000 and 2005.10 A mumps elimination goal was set for 2010.11
However, from 2006 to 2010, several large mumps outbreaks occurred in primarily 2-dose vaccinated US populations. In 2006, 6584 reported cases occurred, mainly affecting Midwestern college students. Standard control measures (eg, isolation and vaccine catch-up campaigns) were implemented for outbreak control.12 During 2009 to 2010, 3502 mumps cases were reported in a highly 2-dose vaccinated population in an Orthodox Jewish community in the Northeast; this outbreak was the first to use a third dose MMR vaccine intervention for outbreak control.13,14
On February 25, 2010, Guam Department of Public Health and Social Services (DPHSS) was informed of a mumps case in a 2-dose vaccinated 15-year-old male. More cases were subsequently reported, primarily among vaccinated school children aged 9−14 years. The last reported mumps outbreak on Guam occurred in 1958; in the past decade, Guam reported an average of 4 mumps cases annually. As part of the public health response to this outbreak, a third dose of MMR vaccine was administered. We evaluated the outbreak epidemiology and the safety and impact of a third dose MMR vaccine intervention in target populations for outbreak control.
Guam is a US territory with a 2010 population of ~180,692 persons.15 The primary ethnicity on Guam is Chamorro, comprising 37% of the population.15 Guam follows the Advisory Committee on Immunization Practices recommendations for MMR vaccination: the first MMR dose is administered at ages 12–15 months and the second dose at 4–6 years.16
Mumps cases were classified according to the 2008 Council of State and Territorial Epidemiologists mumps case definition.17 On Guam, healthcare providers are mandated by law to report mumps cases to Guam DPHSS. DPHSS instituted active surveillance April 20, 2010, at the peak of the outbreak with schools, daycares, select provider clinics and laboratories reporting mumps cases daily; close contacts of reported cases were investigated. DPHSS collected information on demographics, laboratory results, symptom onset date, mumps-related complications and vaccination history. Vaccination status of all case-patients was verified by healthcare providers; administration dates were noted.
Laboratory criteria for mumps diagnosis included isolation of mumps virus from clinical specimens (ie, either an oropharyngeal or buccal mucosa swab), detection of mumps nucleic acid or detection of mumps IgM antibody measured by qualitative assays. All culture, reverse transcription-polymerase chain reaction tests,18 mumps virus sequencing and genotype analysis19,20 were conducted by the Centers for Disease Control and Prevention (CDC). IgM tests were conducted at CDC and state and commercial labs.
The outbreak period was defined as December 1, 2009, to December 31, 2010. We calculated mumps attack rates (ARs) for the population overall and by sex, age and ethnicity. AR denominators were obtained from the projected 2010 Guam census data.15 Because census age groupings did not correlate with the age group most affected by the outbreak, we created a 9-year to 14-year age group category by adding one-fifth of the 5-year to 9-year census age group to the 10-year to 14-year census age group.
Third Dose MMR Vaccine Intervention
Public schools were eligible for the third dose intervention if they had >90% 2-dose MMR vaccine coverage, ongoing mumps transmission (ie, mumps cases in the preceding 2 weeks) and a mumps AR of >5/1000. Students in the intervention schools were eligible if they were in the age group with the highest AR (aged 9−14 years), had a history of 2 MMR vaccine doses, had not previously received a third MMR vaccine dose and had no history of mumps. Students who were not up-to-date with the recommended 2 doses of MMR vaccine were offered appropriate vaccinations. School vaccination coverage was assessed by reviewing school vaccine records.
Vaccination status of students participating in the study was confirmed either through immunization card review by parents or immunization staff, or review of DPHSS and school vaccine registries. For students with unknown or incomplete vaccination status, verification was obtained from healthcare providers.
This study was approved by the CDC and Guam Memorial Hospital Institutional Review Boards. Written informed parental consent and student assent were obtained.
Baseline and follow-up surveys captured demographic characteristics, vaccination history, mumps history, clinical features and complications of mumps, number of people in the household and number of bedrooms in the house. Follow-up surveys also captured possible adverse events after immunization. Baseline surveys were distributed to all eligible students during the third dose MMR vaccine intervention from May 18 to May 21, 2010. Follow-up surveys were distributed from October 4 to October 15, 2010, to the original eligible cohort.
Mumps cases were identified by parental report on baseline and follow-up surveys. To ensure completeness in ascertaining cases, we supplemented our survey case count with confirmed cases reported to Guam DPHSS. If students were not reported as a case to DPHSS, did not report mumps in the baseline survey and did not return a follow-up survey, they were categorized as noncases in our analysis.
Using the exact date of the vaccination clinic at the case-students’ school, we compared mumps ARs after the intervention between eligible students aged 9–14 years who received the third MMR vaccine dose with nonrecipients (ie, students with documentation of ≤2 doses of MMR vaccine) from postintervention day 22 through day 228 (ie, December 31, 2010, the end of the study period). We excluded the 21 days (1 incubation period) after the intervention from the analysis (May 22 to June 11, 2010) because persons infected prior or during the intervention may have been incubating mumps during this timeframe.1,21
All vaccine recipients were monitored 30 minutes postintervention to evaluate immediate adverse events. The follow-up survey contained questions on adverse events that may have occurred up to 2 weeks postintervention, including any serious adverse events resulting in permanent disability, hospitalization, life-threatening illnesses or death.22
All data were analyzed with SAS 9.2 (Cary, NC). Denominators for school ARs were calculated using school enrollment data. We compared postintervention mumps ARs between students who received the third dose of MMR vaccine with those who did not using Fisher's exact test. P values of <0.05 were considered significant. Relative risks (RRs) and 95% confidence intervals (CIs) were calculated. Crowding was assessed by dividing the number of household members by bedrooms in the house. Two-independent samples t tests were used to compare differences between the means for household size and crowding between ethnic groups.
The first case of mumps was reported to DPHSS on February 25, 2010, but the index case-patient was retrospectively identified as having parotitis onset December 7, 2009. The index case-patient was a Guam resident who imported mumps from the island of Pohnpei where mumps was known to be circulating. Between December 1, 2009, and December 31, 2010, 505 cases of mumps were reported (Fig. 1) with a median age of 12 years (range: 2 months to 79 years; Table 1); 50% were males. There were 5 (3.3%) reports of orchitis among postpubertal males with 3 additional reports of orchitis among prepubertal males aged 3, 7 and 9 years. There were 2 hospitalizations for mumps-related illness; 1 was for supportive care of orchitis and the other was misdiagnosed as neck cellulitis but was later confirmed as mumps parotitis. No deaths were reported.
Children aged 9–14 years had the highest overall AR (8.4/1000), followed by those aged 5−8 years (5.3/1000), 15−19 years (3.9/1000) and 0−4 years (3.7/1000). Adults 40 years and older had the lowest AR (0.5/1000). Correspondingly, all age groups <40 years were statistically more likely to have reported mumps case-patients than adults 40 years or older, and children aged 9−14 years had a 16 times higher risk (RR = 16.3, CI: 11.2–23.5). Compared to persons self-reporting “other” ethnicity, which comprised 32% of the Guam population, persons who reported their ethnicity as Pohnpeian or Chuukese had a markedly elevated risk of mumps (Pohnpeian [RR = 54.7, CI: 39.2−76.3] or Chuukese [RR = 19.7, CI: 14.5−26.9]). In contrast, persons reporting Filipino ethnicity did not have an elevated risk and those reporting Chamorro ethnicity had a mildly elevated risk (Table 1). Ninety-six percent of mumps case-patients aged 9–14 years were vaccinated with 2 doses of MMR vaccine, followed by 90% of case-patients aged 5–8 years and 88% of case-patients aged 15–19 years (Table 2).
Of 505 case-patients, 309 (61%) had sera tested for mumps IgM; 60 (19%) tested IgM positive. Twenty-eight (82%) of 34 viral specimens tested positive by reverse transcription-polymerase chain reaction, of which 14 (41%) also tested positive by culture. (The difference in positive results between reverse transcription-polymerase chain reaction and culture is likely because 2 of the 3 shipments of specimens were not frozen on arrival compromising specimen quality. In the only shipment that arrived frozen, 11 of 14 specimens were positive by culture.)Sequence analysis of mumps viruses identified mumps genotype G as the outbreak strain.
There are 64 public and private schools on Guam (preschool through high school). Seven (11%) schools (4 elementary and 3 middle schools) met the inclusion criteria with ARs ranging from 8.4 to 31.5/1000 among children aged 9−14 years (ie, grades 4−8). These 7 schools were in the north and central regions of Guam, the most densely populated part of the island. The high mumps ARs of these 7 schools reflected the distribution of cases on Guam, as a majority of the island’s case-patients occurred in this age group and resided in the north and central regions. All 7 schools had 2-dose MMR vaccine coverage between 99% and 100%.
MMR Vaccine Third Dose Intervention
The third dose intervention was implemented in the highest AR schools in the most affected age group (students aged 9–14 years), but occurred after the outbreak peaked (Fig. 2); 186 (37%) of the 505 outbreak cases occurred after the intervention. There were 3364 students in grades 4−8 in the 7 selected schools, of whom 3239 were eligible for the third dose intervention. Of those eligible, 1068 (33%) received a third dose of MMR vaccine. At least 1 survey was returned by 2434 (75%) eligible students, with 1236 (38%) returning a baseline and 2032 (63%) returning a follow-up survey. All 1068 vaccinees returned a baseline survey and 734 (69%) returned a follow-up survey (Fig. 3). Nonrespondents were statistically more likely to be male (P = 0.0024) and in grades 7−8 (P < 0.0001) compared with survey respondents. Despite differences between survey respondents and nonrespondents, respondents reported similar demographic characteristics proportionally compared with the Guam general population with 1220 (50%) males, 1006 (41%) self-reporting Chamorro ethnicity and 1761 (77%) responding they had insurance. Students who received the third dose were statistically more likely to be without health insurance (P = 0.008), female (P < 0.0001) and in grades 4–6 (P = 0.0002), compared with nonvaccine recipients.
The mean household size among respondents was 6.2 members (range: 2−26). Chuukese respondents had the largest household size with a mean of 7.3 members (range: 2–26), followed by Pohnpeian respondents with a mean of 7.0 members (range: 2–17), Chamorro respondents with a mean of 6.2 members (range: 2–18) and Filipino respondents with a mean of 5.7 members (ranges: 2–16). The mean number of household members among Chuukese and Pohnpeian respondents was significantly higher than among Chamorro and Filipino respondents (P < 0.05).
The average crowding index among respondents was 2.3 persons per bedroom. Pohnpeian and Chuukese households had the highest crowding indices with a mean of 3.1 and 3.0 persons per bedroom (ranges: 1–10 and 1–13, respectively), compared with Chamorro and Filipino households which had crowding indices of 2.2 and 2.1 persons per bedroom (ranges: 0.3–14 and 0.7–14, respectively). The mean crowding index in Pohnpeian and Chuukese households was significantly higher than in Chamorro and Filipino households (P < 0.0001).
Six students eligible for the third MMR dose from 4 different intervention schools were diagnosed with mumps in the postintervention period; 5 (83%) did not receive the third MMR dose and 1 (17%) received the third MMR dose (Table 3). The student with mumps who received the third dose of MMR vaccine was IgM negative and IgG positive. The mumps AR was 2.6-fold lower in those who received the third MMR dose compared with those who did not (0.9/1000 versus 2.3/1000, RR = 0.4, CI: 0.05−3.5, P = 0.67); this difference was not statistically significant (Fig. 4).
No immediate adverse events were reported. During the 2 weeks postvaccination, 32 (6.0%) students reported an adverse event; the most frequent self-reported events were: joint aches (2.6%), pain, redness and swelling at the injection site (2.4%) and dizziness (2.4%; Table 4). No serious adverse events were reported, and no medical attention was sought related to these events.
The Guam mumps outbreak was the third largest in the United States and its territories since 2005, and the second outbreak where a third dose of MMR vaccine was administered, thus providing an opportunity to evaluate the impact and safety of a third dose MMR vaccine intervention in mumps outbreak control. Although the intervention occurred after the outbreak peaked, the AR in students who received the third dose of MMR vaccine was 60% lower than students with ≤2 doses during the postintervention period. Perhaps due to the smaller number of mumps cases that occurred at this stage of the outbreak, the difference in ARs was not statistically significant. Nonetheless, the effect of a third dose in boosting immunity and increasing vaccine effectiveness is biologically plausible; rapid anamnestic antibody responses after third MMR vaccine doses have been reported.23
Mumps outbreaks have occurred in other populations with high 2-dose vaccination coverage, including tradition-observant Orthodox Jewish adolescent school students,24 Midwestern college-age students12 and international settings.25–27 Some of the potential contributors in those outbreaks, including high population density and high contact rates, may also have contributed to the outbreak in Guam. Guam families typically live in crowded environments with large extended families (ie, Guam has a crowding index of 3.9 persons/household compared with 2.6 persons/household on the US mainland; survey respondents had an average of 6.2 family members).15 Due to high contact rates among students, the importance of schools as high-risk transmission settings for mumps and other outbreaks of vaccine-preventable diseases has been well documented.12,28
Compared with other 2-dose mumps outbreaks, some epidemiological features of this outbreak were unusual. Children aged 9–14 years were disproportionately affected; this was a younger age group than described in similar outbreaks.12,24 Cases occurred in all ethnic groups, but the highest ARs occurred in the ethnic minority populations with the most household members and highest household crowding indices. We are unable to explain this epidemiological finding but postulate that contributing factors may include higher household density and/or genetic effects.
Although this outbreak occurred in a highly vaccinated population, there were lower transmission rates and fewer mumps-related complications than would be expected in the absence of appropriate vaccination. Orchitis was reported among 3.3% of postpubertal males. This is consistent with lower rates of complications in fully vaccinated persons and with findings from the Northeast outbreak,13,24 but much less than prevaccine rates of 30% (range 19%−44%) although the younger median age of postpubertal cases in this outbreak should be considered when interpreting this comparison.2,29–32 The occurrence of 3 reports of orchitis in prepubertal males was unusual because there have only been 12 previously documented reports of prepubertal mumps orchitis.33,34 However, 2 of the 3 cases were reported by parents, and the third patient was hospitalized for orchitis with no documented parotitis or laboratory confirmation. Previous studies have documented that mumps can present as orchitis in the absence of parotitis.2,7
It was not surprising that only 19% of 309 cases showed an IgM response. Case-patients who mount a secondary immune response to mumps, as seen in most previously vaccinated persons, may not have an IgM response or it may be transient and not detected depending on the timing of specimen collection.35 Commercial IgM tests are less sensitive than mumps IgM capture assays (CDC unpublished data), and this also likely contributed to the low rate of IgM detection in this study.
Genotype G, the outbreak strain, was identified in the 2006 and 2009 to 2010 outbreaks in the United States, the outbreak in Canada in 2005 to 2006, the United Kingdom in 2004 to 2005 and is seen globally, although this lineage was different from the Northeast outbreak. Mumps is endemic throughout the world; only 62% of countries vaccinate against mumps.36 It is possible that since the last reported mumps outbreak on Guam in 1958 and before this outbreak, mumps cases were imported on the island from international visitors but went undetected; this may explain why older children and adults were less affected. Nonetheless, although over 1 million international passengers visit Guam annually,37 the index case-patient was a Guam resident who traveled to another Pacific island where mumps was known to be circulating.
MMR vaccine in the United States contains the Jeryl-Lynn mumps strain.16,38 In postlicensure studies, vaccine effectiveness against clinical mumps has a median effectiveness of 78% (range: 49%–92%) for 1 dose of mumps vaccine and 88% (range: 66%−95%) for 2 doses of mumps vaccine.39–41 Thus, although reported mumps cases in the United States were 99% lower in 2010 compared with the prevaccine era, sustained transmission of mumps in highly vaccinated 2 dose populations occurs in rare circumstances.12,24 We were unable to evaluate 2-dose vaccine effectiveness during the outbreak in Guam due to the extremely high 2-dose coverage. Effectiveness of 3 doses of mumps vaccine has not been evaluated.
Our findings are subject to limitations. Many families did not visit a healthcare provider for subsequent ill family members, likely leading to underreporting. There were anecdotal reports from community leaders that there were large numbers of unreported cases despite active surveillance. Although transmission was still occurring, the intervention occurred after the outbreak peaked. The small numbers of mumps cases in the targeted population postintervention limited our ability to draw firm conclusions about the impact of the third dose intervention. There were statistically significant differences between survey respondents and nonrespondents, as well as among survey participants who received the third dose of MMR vaccine and those who did not. However, these differences are unlikely to bias the effect of a third dose of MMR vaccine. Census data were not available to explore crowding indices by ethnicity among the Guam general population.
Implementing the third dose intervention in the school setting allowed us to verify vaccination records while targeting specific age groups in the most highly affected regions. However, the third dose was only administered to 5.3% of all students aged 9–14 years making it difficult to draw conclusions about the impact of the intervention at the population-level. More studies are needed to find the optimal time to implement a third dose MMR vaccine intervention. In the past 5 years in the United States, we have experienced mumps outbreaks that have persisted for a couple generations but have resolved without offering the third dose intervention.42 However, the outbreak among the Orthodox Jews in the Northeast and this outbreak persisted for months.14 With delayed reporting in many outbreak contexts, it is often difficult to ascertain when the peak of the outbreak is occurring, which makes it challenging to know whether the outbreak will resolve on its own or whether a third dose intervention is warranted.
Mumps outbreaks can cause a substantial economic and resource burden on affected families and the public health sector,43 and targeted interventions may be a useful public health approach in select high-risk transmission settings. The results of our study suggest that the administration of a third dose of MMR vaccine may be an effective method of controlling mumps outbreaks in 2-dose vaccinated populations in specific settings. For future mumps outbreaks in primarily 2-dose vaccinated populations, the focus should be on ensuring that everyone is up-to-date with the recommended 2-dose vaccination schedule, as well as enforcing isolation measures and encouraging appropriate hygiene practices. Our findings support the need for additional evaluations that use third doses of MMR vaccine for mumps outbreak control in highly 2-dose vaccinated populations and underscore the importance of initiating the intervention early in the outbreak.
We would like to extend our thanks to Albert Barskey, Stephanie Bialek, Scott Grytdal, Mike Hudges, John McKenna, Carolyn Parry, Rose Vibar, Gissela Villarruel, Jennifer Yara and the students (Tina Cruz, Kristan Leon Guerrero, Noemi Ramirez and P. J. Siquig) for their assistance during the field investigation. We would like to thank all the outreach coordinators of the Department of Education on Guam, Student Support Services Division, especially Doris Bukikosa, for their tireless efforts in helping us reach students during the follow-up survey. We also extend our thanks to Robert Haddock for his historical knowledge of mumps outbreaks on Guam. Finally, we would like to thank the public health nursing staff, especially Margarita Gay, for helping us with the school vaccination clinics.
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Keywords:© 2013 Lippincott Williams & Wilkins, Inc.
mumps; outbreak control; third dose measles–mumps–rubella intervention; vaccine preventable disease; immunization