Pediatric Infectious Disease Journal:
Risk Factors for Transmission of Mumps in a Highly Vaccinated Population in Orange County, NY, 2009–2010
Kutty, Preeta K. MD, MPH*; McLean, Huong Q. PhD, MPH*†; Lawler, Jacqueline MPH, CPH‡; Schulte, Cynthia RN, BSN§; Hudson, Jean M. MD, MPH‡; Blog, Debra MD, MPH§; Wallace, Gregory MD*
From the *Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA; †Marshfield Clinic Research Foundation, Marshfield, Wisconsin; ‡Orange County Health Department, Goshen; and §Bureau of Immunization, New York State Department of Health, Albany, NY.
Accepted for publication August 21, 2013.
The authors have no funding or conflicts of interest to disclose.
Address for correspondence: Preeta K. Kutty, MD, MPH, MS C25, 1600 Clifton Road, Atlanta, GA 30333. E-mail: firstname.lastname@example.org.
In 2009–2010, we investigated a mumps outbreak among a highly vaccinated Orthodox Jewish population in a village in Orange County, NY, to identify risk factors associated with mumps transmission among persons with 2 doses of mumps-containing vaccine.
Demographic and epidemiologic characteristics were collected on students in grades 6–12 in 3 schools. A mumps case was defined as a student, who self-reported parotitis, orchitis, jaw swelling and/or a mumps-related complication or whose mumps illness was reported to the Orange County Health Department during September 1, 2009, to January 18, 2010. Log-binomial regression analyses were conducted separately for boys and girls as they attended different schools and had different hours of study.
Of the 2503 students with 2 documented doses of mumps-containing vaccine, 320 (13%) developed mumps. Risk of mumps increased with increasing number of mumps cases in the class [≥8 vs. ≤3 cases: boys aRR = 3.1; 95% confidence interval (CI): 2.0–5.0; girls aRR = 2.6; 95% CI: 1.6–4.1] and household (>1 vs. 0 cases: boys aRR = 4.3 95% CI: 3.7–5.6; girls aRR = 10.1 95% CI: 7.1–14.3). Age at first dose, time since last dose, time between first and second dose, school, class size, number of hours at school per week and household size were not significantly associated with having mumps.
Two doses of mumps-containing vaccine may not be as effective in outbreak settings with multiple, prolonged and intense exposure. Additional studies are required to understand why such mumps outbreaks occur and how they can be prevented in the future.
Mumps is the only known cause of epidemic parotitis. The extensive use of the live mumps vaccine, since its licensure in the United States in 1967, resulted in significant reductions in disease incidence and morbidity.1 During the decade before 2009, the average annual incidence of mumps in the United States was 0.34 per 100,000 population; the lowest incidence occurred in 2003 (0.08 per 100,000 population) and the highest occurred in 2006 (2.2 per 100,000 population).2 In 2006, a mumps outbreak among university students in the Mid-western United States resulted in over 6500 reported mumps cases.1,3,4 Since then, mumps outbreaks among highly vaccinated older individuals have been reported in other countries.5,6 Risk factors identified in the mumps outbreaks in the university settings were reported exposure to mumps among dormitory residents and those attending social gatherings.4,5,7–10
During the 2009–2010 US Northeastern mumps outbreak, a village in Orange County (OC), NY, was affected.11,12 In this village, 790 mumps cases were reported during September 24, 2009, through June 15, 2010; median age was 14.1 years and 64% were male. Of the 658 mumps cases with known vaccination history, 83.6% had documentation of 2 doses of mumps-containing vaccine.12 The Orange County Health Department (OCHD), the NY State Department of Health and the Centers for Disease Control and Prevention investigated the outbreak as a public health response that included assessment of risk factors for mumps transmission. In this study, we aim to identify the risk factors associated with transmission of mumps among persons with 2 documented doses of mumps-containing vaccinations.
Study Area and Study Population
The affected village was located in OC, NY, with a population of 20,363 in 2010 and a median age of 10.6 years.13 The average household size was 5.7; twice the national average of 2.6.12,13 The predominantly Orthodox Jewish village is served by 3 private and 1 public school. For this study, students in grades 6 through 12 in the 3 private schools, which had the highest mumps attack rates, were invited to participate.13
Data on risk factors for mumps transmission were collected in parallel with the study on the impact of a third dose measles, mumps, and rubella (MMR) vaccine intervention in this population.13 A survey, distributed to students in grades 6 through 12 in 3 schools, was used to collect information on demographic characteristics, vaccination history, mumps disease history before and during the outbreak (September 24, 2009, to June 15, 2010), exposure history, household and class characteristics and healthcare provider information.
For the risk transmission study, we considered mumps cases that were identified during September 24, 2009, to January 18, 2010; the third dose MMR vaccine intervention commenced on January 19, 2010. A mumps case was identified in 2 ways: (1) reports of illness of parotitis, orchitis, jaw swelling and/or a complication related to mumps in a student during the study period from the survey and/or (2) notifications to the OCHD classified by using the 2008 Council of State and Territorial Epidemiologists definitions during the study period.14 Mumps vaccination status, including number of doses and dates of vaccination, was obtained using records from the healthcare provider, school and parent report. This study was reviewed and approved by the Institutional Review Boards at the Centers for Disease Control and Prevention and NY State Department of Health.
For this analysis, only individuals with 2 documented doses of mumps-containing vaccine were included. In addition, students were excluded if they had missing information on class and grade or if they had received MMR vaccine during the study period, including those who received a third dose.
Risk factors for mumps disease were evaluated using log-binomial regression to account for clustering of students in classrooms using an independent correlation structure (PROC GENMOD procedure) in SAS 9.3 (SAS Institute Inc., Cary, NC). Factors associated with mumps disease in univariate analyses (P < 0.1) were tested in the multivariate model. To identify independent risk factors for mumps disease, backwards elimination was used (P < 0.05). Interaction and correlation between the variables were assessed and when variables were highly correlated, only 1 of the correlated variables was included in the final model. We used the Cochran-Armitage Trend Test to assess for trend. All analyses were stratified by gender; the boys and girls attended different school buildings and had different hours of study.11
Of the 2688 grade 6–12 students in the 3 schools, 2503 (93%) had 2 documented doses of mumps-containing vaccine and were eligible for this study; 54% were girls. The median age of the students was 13 years (range: 9–21 years). Of the 2503 students with 2 documented dose of mumps-containing vaccine, 320 (13%) self-reported or were identified as having mumps. There were 3 (0.9%) students in OCHD notifications who did not report having mumps in the surveys and 112 (35%) through the survey. The percent of mumps cases among boys was 17% and 9% among girls. The median number of students in each class for the boys was 27 (range: 3–86) and for the girls was 29 (range: 16–57). The median number of cases in a class, irrespective of gender, was 4 (range: 0–20). Students excluded from this study included 104 who had received MMR vaccine during the study period; 72 who had 0 or 1 documented doses of mumps-containing vaccine as of September 1, 2009; 4 who had missing data on class, grade or disease status; 3 with invalid vaccine dates and 2 with prior history of mumps disease (Fig. 1).
Risk Factors for Mumps Disease Among Boys
Among boys, grade, reported face-to-face (f2f) contact with a mumps case, number of mumps cases in the class and number of cases in the household were associated with having mumps in univariate analyses (Table 1). Case were more likely to be in grades 8 [relative risk (RR) = 1.6; 95% confidence interval (CI): 1.1–2.3], 10 (RR = 1.9; 95% CI: 1.6–2.2) and 12 (RR = 2.3; 95% CI: 1.8–3.0) compared with those in grades 6 and 7 (Table 1). Compared with those who did not report contact with a mumps case, students who reported face to face contact with a mumps case (RR=1.5; 95% CI: 1.1–2.0) were more likely to have mumps. Students in classes with >3 mumps cases were at an increased risk of mumps compared with those in classes with ≤3 cases; 4–7 mumps cases and ≥8 mumps cases in a class were 2.5 (95% CI: 1.6–4.1) and 3.8 (95% CI: 2.3–6.1) times more likely to have mumps, respectively (Table 1). There was also an increased risk of mumps with increasing number of reported mumps cases in the household. Students living in households with 1 case were 2.9 (95% CI: 2.1–4.0) more likely to have mumps and those living in household with >1 case were 4.7 (95% CI: 3.7–5.8) more likely to have mumps compared with those living in households with no reported cases. Trend analyses were significant (P < 0.0001) for both number of cases in a class and household (Table 1). Age at first dose, time since last dose, time between first and second dose, school, class size, number of hours at school per week and household size were not significantly associated with having mumps.
In multivariate analyses, only the number of mumps cases in a class and number of mumps cases in the household were independently associated with having mumps. The risk of mumps increased with increasing number of mumps cases in the class [4–7 mumps cases: adjusted relative risk (aRR) = 2.4; 95% CI: 1.5–4.0; ≥8 cases: aRR = 3.1; 95% CI: 2.0–5.0] as well as with increasing mumps cases in the household (1 mumps case: aRR = 2.7; 95% CI: 2.0–3.6; >1 mumps case: aRR=4.3; 95% CI: 3.7–5.6; Table 2).
Risk Factors for Mumps Disease Among Girls
Among girls, the school attended, contact with a mumps case, number of mumps cases in the class and number of cases in the household were associated with having mumps in univariate analyses (Table 1). Girls who went to schools A and B were more likely to have mumps compared with those who went to School C (School A: RR = 2.1 95% CI: 1.1–4.0 and School B: RR = 2.3; 95% CI: 1.4–3.8). Contact with a mumps case, irrespective of reported f2f contact, was associated with an increased risk of mumps compared with no reported contact with a mumps case (f2f: RR = 2.8; 95% CI: 1.8–4.3; contact, but not face-to-face: RR = 2.0; 95% CI: 1.2–3.3 and contact, but uncertain about f2f contact: RR = 2.6; 95% CI: 1.6–4.1). Similar to the boys, girls in classes >3 mumps cases were at an increased risk of mumps compared with those in classes with ≤3 cases (4–7 mumps cases: RR = 2.3; 95% CI: 1.7–7.8; ≥8 mumps cases: RR = 3.8; 95% CI: 2.3–6.2; Table 1). Also, those with 1 or more reported mumps cases in the household were at increased risk of mumps compared with those in households with no reported mumps cases (1 case: RR = 4.9; 95% CI: 3.1–7.8; >1 mumps cases: RR = 11.5; 95% CI: 8.3–16.1; Table 1). Trend analyses were significant (P < 0.0001) for both number of cases in a class and household. Lastly, girls who had received the first dose of mumps-containing vaccine after 24 months of age had an increased risk of mumps (RR = 1.7; 95% CI: 1.1–2.5). Grade, time since last dose, time between first and second dose, number of hours at school, class size and household size were not significantly associated with having mumps.
In the multivariate analysis, similar to the boys, only the number of mumps cases in a class and number of mumps cases in the household were independently associated with having mumps for girls. The risk of mumps increased with increasing number of mumps cases in the class (4–7 mumps cases: aRR=1.8; 95% CI: 1.4–2.5; ≥8 cases: aRR = 2.6; 95% CI: 1.6–4.1) and more mumps cases in the household (1 mumps case: aRR = 4.8; 95% CI: 3.0–7.5; >1 mumps case: aRR = 10.1; 95% CI: 7.1–14.3; Table 2).
In recent years, mumps has become a challenging disease for public health professionals with mumps outbreaks being documented among highly vaccinated populations4,5,7–11,15–17 and the demonstration of shedding of mumps virus by individuals18 with documented 2 doses of MMR vaccine, who reported parotitis. Although less infectious than measles and varicella viruses, mumps virus is transmitted by inhalation of infectious respiratory droplets, direct contact with nasopharyngeal secretions and possibly through contaminated fomites.19–21 The findings in our study indicate that among highly vaccinated 2-dose populations, intense exposures to 1 or more mumps cases in high-density settings such as schools and households may increase the risk of mumps transmission. It is possible that such risk factors may overcome vaccine-induced immunity resulting in the persistence of transmission of the disease.
Because similar reported mumps outbreaks among highly vaccinated populations have tended to occur in high-density settings such as universities and schools, we examined several variables that attempted to look at level of exposure in this study.5,16 We found that exposure to increasing number of mumps cases was associated with transmission. However, f2f contact, hours spent in school and number of students in a class were not found to be risk factors in this study. Similar findings were observed in a study conducted in NY City affecting a similar population but among young male adolescents (grade 9–12 students).22 However, in both studies, the comparison groups were within the same gender and not compared with the traditional public schools. In addition, it is also possible that because we looked at a distinct population where exposure is probably homogeneous, we may not have been able to identify other important factors of “intense” exposure that may have increased the risk of transmission in this population. An alternative explanation may be the role of asymptomatic individuals who may have been a source of transmission in such closed settings.9,15
In the OC village mumps outbreak described here, we were unable to assess directly the effect of gender behavior as the analyses were stratified. However, the mumps attack rates were higher in boys than girls. This was not surprising considering that the boys, particularly older boys, spent longer hours in schools and in some instances followed the chevrusa (study partner) style of studying where a one-on-one interaction with partners sitting opposite each other at tables in large crowded study halls occurs.11,22 This behavior may have likely facilitated mumps transmission as the prodromal symptoms of mumps are known to be nonspecific and the viral loads are high before parotitis onset.1,23 The girls followed a more traditional style of studying followed by the public school system where fewer hours were spent in school. In comparison, the mumps attack rate among the females was higher in the 2006 US mumps outbreak. Factors that may have contributed to the gender difference in that outbreak were probably gender distribution in postsecondary institutions, behavior patterns, and perhaps differential reporting patterns.4,9
In the absence of continued natural exposure, waning of vaccine-induced immunity has been postulated to be 1 of the many possible causes of mumps outbreaks among vaccinated individuals.7,9,24 In this study, we were unable to assess adequately whether waning immunity played a role as most students were vaccinated at the same time and it was difficult to separate any effect of time since vaccination and age of vaccination. It may be less likely that waning immunity played a significant role as the median age group was lower than the previous college outbreaks. In a study conducted in NY City in a similar population, time since receipt of last MMR vaccination was also not a significant factor.25 Mumps antibody levels have been shown to decrease over time in seroepidemiologic studies26–29 among highly vaccinated population that may increase the risk of clinical disease after exposure.30,31 In the US population, the overall age-adjusted seroprevalance of mumps IgG antibody during 1999–2004 was 90% indicating the potential risk for mumps outbreak in populations with lower seroprevalence.32 However, there are currently no established immunologic correlates of mumps protection, which makes interpretation difficult. Lower levels of neutralizing antibodies have been observed among individuals who received the second dose of MMR vaccine at least 15 years before.33 We could not assess herd immunity levels because population serologic testing was not conducted.
Another postulated cause for transmission of mumps in a highly vaccinated population is the lower vaccine effectiveness of the mumps vaccine. The 2-dose vaccine effectiveness for mumps ranges from 66% to 95%24,34–40 indicating that the mumps component is less efficacious than the measles or rubella components of the vaccine, but still effective for most people. In some instances, vaccine effectiveness for 2 doses has been documented to be similar to that of 1 dose of mumps vaccine (62–91%).9,40 Another explanation may be the possibility of lower mumps vaccine effectiveness among household contacts, who have intense exposure compared with school or community contacts as indicated by a study conducted during a mumps outbreak in The Netherlands.39 In our study, of the eligible students with documented 2 doses of mumps-containing vaccine, only 13% reported having mumps or were identified as having mumps before the third dose intervention indicating that many in the community were protected. In addition, the disease did not spread to the surrounding communities. It has also been shown that those who received 2 doses of MMR vaccine had fewer complications due to mumps than those who were unvaccinated.11 Of significance, with the introduction of the mumps vaccine, the rate of mumps has significantly declined in the United States. Living in a world of global mobilization with mumps continuing to be endemic in many countries, importations continue to be a risk for countries that have eliminated or have nearly eliminated mumps. Hence it is important that the 2-dose vaccine coverage continues to be maintained.
The genotype identified in the OC outbreak was genotype G, similar to the rest of the US Northeastern mumps outbreak. The same genotype was also identified in the 2006 US Mid-western mumps outbreak. The mumps vaccine in the United States contains the genotype A Jeryl-Lynn strain which has been thought to neutralize other genotypes at a lower titer.31,41 During our investigation, neutralization studies were not conducted. There was no evidence that other factors such as handling changes and vaccine lots, which are considered to be risk factors for vaccine failure, played a role in this outbreak.
Our study had several limitations. There may have been misclassification of cases as surveys were based on self-report of signs and symptoms; 35% of the mumps cases were self-reported. However, mumps is the only known cause for epidemic parotitis and the heightened awareness of the disease in this community during the outbreak and the high response rates may have limited the misclassification.13 In addition, active surveillance was instituted once the outbreak was declared12; we were able to identify 3 cases that were not reported in the surveys. As our study did not include serologic testing, any asymptomatic cases, which may have been important in transmission, were not identified. Given the nature of the community and the study design it is likely that these students were exposed to multiple sources and for extended periods. Finally, misclassification of vaccine status was possible and individuals who received 2 doses of mumps-containing vaccine may have been excluded.
In this population of highly vaccinated students, we found that exposure to increasing number of mumps cases was associated with an increased risk of developing mumps. Although 2 doses of mumps-containing vaccine is effective in preventing mumps for most exposed persons, our findings suggest that the vaccine may not be as effective if there are multiple, prolonged and intense mumps exposures. To address this issue, the Centers for Disease Control and Prevention has issued guidance for considerations for use of a third dose of MMR vaccine in specifically identified target populations along with criteria for public health departments to consider while making a decision. If a third dose of MMR vaccine is provided, public health officials are encouraged to investigate and report additional information on effectiveness and impact.1 Nevertheless, mumps outbreaks among highly 2-dose vaccinated populations are infrequent. Additional studies are required to understand the epidemiology of these outbreaks, to examine the persistence of 2-dose mumps vaccine-induced immunity and assess the potential risk factors for transmission. These studies will aid in preventing or controlling future mumps outbreaks.
The authors thank the leadership and school administrations of the village in OC, NY; all the students and their parents who participated in the study; the staff of the affected schools and the medical clinics that serve the affected community for providing assistance with case finding/documentation and access to vaccination records and the study staff from the NY State and OCHD for providing logistic and clinical support.
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mumps; outbreak; risk factors; transmission
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