Abstract
During 2009–2010, a large US mumps outbreak occurred affecting two-dose vaccinated 9th–12th grade Orthodox Jewish boys attending all-male yeshivas (private, traditional Jewish schools). Our objective was to understand mumps transmission dynamics in this well-vaccinated population. We surveyed 9th-12th grade male yeshivas in Brooklyn, NY with reported mumps case-students between 9/1/2009 and 3/30/2010. We assessed vaccination coverage, yeshiva environmental factors (duration of school day, density, mixing, duration of contact), and whether environmental factors were associated with increased mumps attack rates. Ten yeshivas comprising 1769 9th–12th grade students and 264 self-reported mumps cases were included. The average yeshiva attack rate was 14.5% (median: 13.5%, range: 1–31%), despite two-dose measles-mumps-rubella vaccine coverage between 90–100%. School duration was 9–15.5 h/day; students averaged 7 h face-to-face/day with 1–4 study partners. Average daily mean density was 6.6 students per 100 square feet. The number of hours spent face-to-face with a study partner and the number of partners per day showed significant positive associations (p < 0.05) with classroom mumps attack rates in univariate analysis, but these associations did not persist in multivariate analysis. This outbreak was characterized by environmental factors unique to the yeshiva setting (e.g., densely populated environment, prolonged face-to-face contact, mixing among infected students). However, these features were present in all included yeshivas, limiting our ability to discriminate differences. Nonetheless, mumps transmission requires close contact, and these environmental factors may have overwhelmed vaccine-mediated protection increasing the likelihood of vaccine failure among yeshiva students.
Keywords: mumps, mumps transmission, environmental risk factors, high MMR vaccine coverage, mumps outbreak
Introduction
Mumps is a viral infection characterized by parotitis and fever, and can result in orchitis, deafness, or meningoencephalitis.1 In the pre-vaccine era, mumps outbreaks often occurred in congregate settings, including schools and military barracks.2-4 In 1977, the Advisory Committee on Immunization Practices (ACIP) recommended one mumps vaccine dose for routine childhood vaccination,5 and in 1989, recommended two doses of measles-mumps-rubella (MMR) vaccine for improved measles control.6 In the US, the first MMR dose is administered at ages 12–15 mo and the second dose at 4–6 y.7
Following the implementation of the one- and two-dose MMR vaccine programs, reported mumps cases declined to fewer than 500 annually in the US from 2000–2005.2 However, in 2006, an outbreak of 6,584 cases occurred, primarily affecting two-dose vaccinated Midwest college students living in dormitories.8 In 2009, another outbreak began in New York at an Orthodox Jewish boys’ camp that spread to affect 3,502 individuals in the Northeast.9 Brooklyn, New York was most affected with 1,737 (50%) of the total reported outbreak cases.
This outbreak primarily affected two-dose vaccinated adolescent males aged 13–18 y in the Orthodox Jewish community who attended yeshivas.9 Yeshivas are schools where Orthodox Jewish 9th-12th grade males intensively study religious texts. School days typically last ≥ 12 h. A unique yeshiva feature is chevrusa (study partner) style study: one-on-one interaction with a partner where students sit opposite each other at tables with other chevrusa pairs, usually in a large study hall termed a beis midrash.
Our objective was to understand mumps transmission dynamics in this well-vaccinated population. Although inclusion of heterogeneous, lightly-affected schools would have allowed us to elucidate differences explaining transmission, 97% of cases were in the Orthodox Jewish population9 and there were only two non-yeshivas with at least one male mumps case in the targeted grades (9th−12th), limiting the types of schools we could include. Thus, we examined school characteristics and potential environmental risk factors for mumps transmission in selected Brooklyn yeshivas.
Results
Inclusion
Of 93 schools with mumps cases reported to the New York City Department of Health and Mental Hygiene (NYCDOH), 57 did not meet the inclusion criteria (e.g., all-female, not high school level, outside Brooklyn, non-yeshiva) and 23 lacked contact information, leaving 13 (14%) yeshivas that met the inclusion criteria. Of the remaining 13, 11 (85%) completed the classroom survey where students were asked to self-report whether they had mumps-like illness, whether they saw a healthcare provider for mumps symptoms, and whether they stayed home from school for mumps. One yeshiva was subsequently excluded because the cases were not in grades 9–12. Two yeshivas did not respond to multiple attempted contacts. Thus, 10 yeshivas comprising 1769 9th−12th grade students and 264 self-reported mumps cases met the inclusion criteria, completed the classroom survey, and were assessed. Although cases were self-reported, 241 (91%) reported visiting a healthcare provider for their symptoms and 100% were either sent home or stayed home from school.
Vaccination coverage
In the 10 yeshivas, 9th-12th graders comprised 39 grades and 63 classes (4 yeshivas had multiple classes per grade). All 10 yeshivas had overall one- and two-dose MMR coverage rates between 97–100% and 90–100%, respectively (Table 1). Three (8%) grades had two-dose vaccination coverage rates < 90% (i.e., 82%, 87% and 89%), but all other grades had two-dose coverage rates ≥ 90% (average: 95%).
Table 1. Yeshiva class size, MMR vaccination coverage, attack rates, hours spent in the yeshiva, hours face-to-face with a chevrusa, daily mean density and number of chevrusas per day in Brooklyn yeshivas, 9/1/2009—3/30/2010.
| Yeshiva | Grade | Average Number of Students per class | Two Dose MMR Coverage (% by Grade) | Two Dose MMR Coverage (% by Yeshiva) | Grade Attack Rates (%) | Yeshiva Attack Rates (%) | Hours at School/ Daya | Hours at School/ Week | Hours Face-to-Face with Chevrusa(s)/ Daya | Daily Mean Density (Average Number of Students per 100 Square Feet/Day)a | Number of Chevrusas/ Daya |
|---|---|---|---|---|---|---|---|---|---|---|---|
| A |
9 |
18.3 |
96 |
98 |
4 |
1 |
12.5 |
58.5 |
1 |
8 |
1.5 |
| 10 |
20.3 |
100 |
0 |
12.5 |
58.5 |
3 |
9.8 |
1.5 |
|||
| 11 |
15.5 |
98 |
2 |
12.5 |
58.5 |
4 |
8.7 |
1.5 |
|||
| 12 |
19 |
98 |
0 |
12.5 |
58.5 |
9 |
6 |
1.5 |
|||
| B |
9 |
34 |
97 |
97 |
6 |
8 |
12 |
64 |
6.25 |
4.1 |
3 |
| 10 |
33 |
97 |
9 |
12 |
64 |
6.25 |
4.1 |
3 |
|||
| 11 |
33 |
93 |
3 |
12 |
64 |
6.25 |
4.2 |
3 |
|||
| 12 |
22 |
100 |
18 |
12 |
64 |
6.25 |
3.9 |
3 |
|||
| C |
9 |
28 |
100 |
100 |
7 |
10 |
15.5 |
74.5 |
N.A. |
N.A. |
1 |
| 10 |
25 |
100 |
4 |
15.5 |
74.5 |
N.A. |
N.A. |
1 |
|||
| 11 |
21 |
100 |
10 |
15.5 |
74.5 |
N.A. |
N.A. |
1 |
|||
| 12 |
25 |
100 |
20 |
15.5 |
74.5 |
N.A. |
N.A. |
1 |
|||
| D |
9 |
24 |
96 |
95 |
8 |
11 |
13.5 |
67.5 |
3.75 |
3.1 |
3 |
| 10 |
33 |
94 |
18 |
13.5 |
67.5 |
5.25 |
3.5 |
3 |
|||
| 11 |
37 |
100 |
6 |
13.5 |
67.5 |
5.25 |
3.6 |
3 |
|||
| 12 |
37 |
89 |
11 |
13.5 |
67.5 |
6.75 |
3 |
3 |
|||
| E |
9 |
21.5 |
98 |
95 |
14 |
11 |
12 |
57 |
1.5 |
6.9 |
1 |
| 10 |
24 |
96 |
10 |
12 |
57 |
3 |
9.2 |
1 |
|||
| 11 |
38 |
92 |
5 |
15 |
73 |
9.75 |
5.6 |
2.5 |
|||
| 12 |
24 |
92 |
17 |
15 |
73 |
10.25 |
4.7 |
2.5 |
|||
| F |
9 |
28 |
82 |
90 |
7 |
16 |
14 |
74 |
11b |
5.5 |
3 |
| 10 |
38 |
92 |
18 |
14 |
74 |
11b |
6.3 |
3 |
|||
| 11 |
40 |
93 |
18 |
14 |
74 |
11b |
6 |
3 |
|||
| 12 |
40 |
90 |
18 |
14 |
74 |
11b |
5.8 |
3 |
|||
| G |
9 |
28 |
93 |
93 |
21 |
16 |
13 |
70 |
7 |
5 |
3 |
| 10 |
23 |
96 |
22 |
13 |
70 |
7 |
4.7 |
3 |
|||
| 11 |
14 |
90 |
7 |
13 |
70 |
7 |
4.3 |
3 |
|||
| 12 |
51 |
94 |
12 |
13 |
70 |
7 |
6.3 |
3 |
|||
| H |
9 |
40 |
95 |
98 |
20 |
17 |
9 |
49 |
1.5 |
6.3 |
4 |
| 10 |
40 |
98 |
20 |
10.5 |
55 |
3.0 |
6 |
4 |
|||
| 11 |
18 |
100 |
19 |
13.5 |
67 |
8.5 |
3.4 |
4 |
|||
| 12 |
46 |
100 |
11 |
13.5 |
67 |
8.5 |
4.4 |
4 |
|||
| I |
10 |
25.1 |
96 |
93 |
25 |
22 |
12.5 |
60 |
8 |
9.4 |
3 |
| 11 |
27.5 |
87 |
14 |
12.5 |
60 |
8 |
9.3 |
3 |
|||
| 12 |
30.8 |
96 |
27 |
12.5 |
60 |
8 |
4.1 |
3 |
|||
| J | 9 |
21 |
100 |
96 | 19 |
31 | 12.5 |
64 |
8b |
4.3 |
2 |
| 10 |
22 |
95 |
32 |
12.5 |
64 |
8b |
4.6 |
2 |
|||
| 11 |
23 |
96 |
30 |
12.5 |
64 |
8b |
4.5 |
2 |
|||
| 12 | 19 | 95 | 42 | 12.5 | 64 | 8b | 4 | 2 |
N.A. means scheduling data not available. a A day is based off of the Monday-Thursday schedule (Fridays are half days, there is no school on Saturday and Sunday is a shortened day). b Yeshivas F and J utilized the chevrusa system in the classroom, in addition to the beis midrash.
Yeshiva characteristics
Duration and mixing
On average, school lasted 12.7 h/day (range: 9–15.5 h) Monday through Thursday, with half days on Fridays, no class on Saturdays and shortened days on Sundays. School weeks averaged 63.0 h (range: 49–74.5 h). We obtained schedules from 9 (90%) yeshivas. On average, 9th-12th graders spent: 6.2, 3.7, 3.4 and 2.0 h/day in the classroom, respectively, where they predominantly faced forward; 3.0, 5.8, 6.6 and 7.9 h/day studying in the study hall (beis midrash), respectively, where they sat face-to-face with a study partner (chevrusa); 1.7 h/day facing forward during prayers in the beis midrash; and 1.2 h/day in the cafeteria.
On average, students spent 7 h/day face-to-face with their chevrusas (range: 1–11 h) and changed chevrusas 2.5 times/day (range: 1–4 times). Mixing occurred within classes (e.g., chevrusas were from the same class). Although all students gathered in the beis midrash, and multiple grades often ate in the cafeteria concurrently, students sat with their own class and mixing among grades rarely occurred.
Approximately 850 (48%) students in 4 yeshivas rode school buses daily. Three yeshivas reported that buses carried students from several grades concurrently; none carried students from multiple schools.
Density
Yeshivas had an average of 26.5 students per classroom. When all students gathered in the beis midrash for study hall and prayers, an average of 195 students were in the same room. Average room densities for the classroom, study hall, prayer time and cafeteria were: 5.8, 6.2, 7.1 and 8.4 students per 100 square feet, respectively. Average daily mean density was 6.6 students per 100 square feet.
Ventilation
Nine yeshivas provided ventilation data. Five (56%) used central heating, 9 (100%) had windows that could open and 8 (89%) had central air conditioning, of which 3 also used fans.
Prevention Measures
Seven (70%) yeshivas increased sanitization practices during the outbreak, 9 (90%) communicated with parents or students about mumps (e.g., letters, school announcements) and all yeshivas sent symptomatic students home. None of the yeshivas cancelled or postponed classes.
Attack rates
The average mumps attack rates in the yeshivas was 14.5% (median: 13.5%, range: 1–31%); 8 (80%) yeshivas had attack rates ≥ 10%. Tenth and twelfth grades had the highest mean attack rates at 18% each; ninth and eleventh grades had mean attack rates of 11% each. Class attack rates ranged from 0–42%. Class attack rates in Yeshiva A, which had the lowest yeshiva attack rate (1%), ranged from 0–13%, whereas class attack rates in Yeshiva J, which had the highest yeshiva attack rate (31%), ranged from 19–42%.
The class with the highest attack rate (42%) had 95% two-dose vaccination coverage. Eleven classes had 0 case-students, all in Yeshiva A; two-dose MMR vaccination coverage in these 11 classes was 96–100%.
Analysis
We included data from the 9 yeshivas for which we had scheduling information. When accounting for clustering, the number of hours spent face-to-face with a chevrusa and the number of chevrusas per day showed significant positive associations (p < 0.05) with classroom mumps attack rates in univariate analysis, but these associations did not persist in multivariate analysis (Table 2). The number of hours per school day and mean density were not significant in univariate analysis. The results were similar when we used continuous and categorical variables.
Table 2. Univariate and multivariate analyses assessing independent factors associated with classroom mumps attack rates in Brooklyn yeshivas, 9/1/2009—3/30/2010.
| Yeshiva Characteristics and Environmental Factorsa | Unadjusted Risk Ratio (95% CI) | P value | Adjusted Risk Ratio (95% CI)b | P value |
|---|---|---|---|---|
| Hours at school/day |
0.92 (0.83– 1.01) |
0.076 |
– |
– |
| Mean density |
0.01 (0– 105.87) |
0.338 |
– |
– |
| Hours face-to-face/day |
1.10 (1.02– 1.18) |
0.009 |
0.92 (0.81– 1.04) |
0.165 |
| Number of chevrusas/day | 1.48 (1.15– 1.89) | 0.002 | 1.46 (0.72– 2.94) | 0.291 |
a We excluded ventilation data because the outbreak occurred during winter when windows were closed and air conditioning was off. b Hours at school per day and mean density were not included in the final model because they were not significant in the univariate analysis.
Discussion
The yeshiva setting was characterized by close contact: students averaged 7 h of face-to-face exposure to an average of 2.5 chevrusas per day. Close contact is essential for mumps transmission; mumps spreads through respiratory droplets or secretions.1 To become infected, a person must be within three feet of an infected person or have direct contact with his or her secretions.10,11 Although in multivariate analysis we did not find a significant association between classroom mumps attack rates and face-to-face time or number of chevrusas/day (factors that may be critical determinants for spread of mumps among vaccinated persons), we postulate that these factors did not vary sufficiently across the included yeshivas to allow significant differences to be discriminated. Nonetheless, the dynamics of prolonged face-to-face exposures with multiple chevrusas may have created a high enough force of infection to overwhelm vaccine-mediated protection and may have increased the likelihood of vaccine failure among yeshiva students.
Yeshiva students attended school on average 12.7 h/day with an average of 26.5 students per classroom, compared with an average of 6.7 h/day and 18.4 students per classroom for other private US secondary schools.12,13 Although neither school day duration nor density were significant risk factors in univariate analysis and are more indirect indices of close contact than face-to-face time or number of chevrusas/day, the yeshivas we evaluated had a school day that was approximately twice as long with 31% more students per classroom than other US private secondary schools which could have played a role in mumps transmission.12,13
This paper describes class attack rates that were as high as 42%, despite high two-dose MMR vaccine coverage. Even with opportunities for mumps introductions in the surrounding non-Orthodox community, the exposures were likely less frequent and less intense than in yeshivas, so the high vaccination coverage generally provided adequate population immunity for protection.9 These findings are consistent with a large mumps outbreak in Israel in 2009 where most cases also occurred among well-vaccinated Orthodox Jewish adolescent males with minimal spread to the broader community, despite regular mixing with non-Orthodox Jews.14 Mumps outbreaks have also occurred in other international settings among highly vaccinated populations.15-17
Two MMR vaccine doses provide 66–95% vaccine effectiveness against mumps.18,19 The two-dose policy has reduced mumps incidence by > 99% compared with the pre-vaccine era.2 Despite high two-dose MMR vaccine coverage, the average yeshiva attack rate was 14.5% which was 10% higher than the 4.6% attack rate among two-dose vaccinated college students living in affected dormitories in the 2006 US mumps outbreak,20 and almost as high as attack rates during the one-dose era.21 Although it is possible that lesser-vaccinated grades seeded the outbreak (3 [8%] grades had two-dose MMR coverage < 90%), none of these had the highest grade-level attack rates, nor were they in yeshivas with the highest attack rates.
Based on the age range of the students in the yeshivas included in this analysis (i.e., 13–18 y) and the ACIP guidelines for the standard age for receipt of the second MMR vaccine dose, it is likely that these students received their most recent dose between 7–14 y prior. Nonetheless, waning immunity did not seem to contribute to this outbreak,9 because the outbreak did not readily spread to older persons. Strain difference between the vaccine (genotype A Jeryl Lynn) and circulating mumps virus (genotype G) also did not seem to play a role, because generally, mumps did not spread to the broader population.9 Opening windows and doors may help reduce mumps transmission.22 However, we excluded these factors in the model, because the outbreak occurred during winter when windows were closed.
This analysis had limitations. We did not evaluate schools with zero reported mumps cases as a comparison (e.g., public or girls schools), because our objective was to understand characteristics of schools with mumps transmission. Upon identifying yeshivas with reported cases on NYCDOH’s list, we planned to compare yeshivas with high vs. low attack rates. However, after obtaining accurate case counts from surveying the included yeshivas, all but one had a high attack rate. The low attack rate school (Yeshiva A) had characteristics similar to high attack rate schools (e.g., long school days, multiple chevrusas, high density). We assessed whether there were differences between higher grades (11th and 12th) that generally had longer school days and spent more time face-to-face with chevrusas vs. lower grades (9th and 10th), but there was likely too much overlap in environmental conditions among grades to provide meaningful differences. A power analysis was not done at the onset, because this was deemed to be an outbreak response. Thus, we planned to enroll all yeshivas that met the inclusion criteria. As in any outbreak, tools are inadequate to monitor individual-level exposures to infectious respiratory agents, such as mumps; thus, this analysis was ecologic. However, due to the limitations of an ecological design, we were unable to report individual-level data, such as identify who the classroom index case-students were, report the severity of their illness (as a proxy for infectiousness), document who were linked as chevrusas, compare the attack rate among students who had zero or 1 dose of MMR vaccine, or identify who was uniquely exposed to whom. Yeshivas also did not provide mumps onset dates of case-students which limited our ability to assess transmission patterns (i.e., whether classrooms had one wave or several subsequent waves of mumps infection). We did not have age data on individuals to determine if older students were affected more frequently, potentially as a result of waning immunity; however, grade was considered a proxy for student age. To study risk factors for spread of mumps within yeshivas, it was necessary to restrict our analysis to yeshivas that had mumps exposure (i.e., any reported cases within a yeshiva). While this resulted in a limited number of included yeshivas, initial introduction of mumps was likely to be a primarily stochastic event, based on networks within the affected community. Nonetheless, we do not believe that this restriction introduced important bias. We potentially missed yeshivas, because healthcare providers may not have reported all cases to the NYCDOH and schools were not always identified when cases were reported. Additionally, two yeshivas did not respond to our survey and 23 lacked contact information.
Despite these limitations, this evaluation is important given the paucity of literature providing detailed descriptions of settings where mumps transmission has occurred in two-dose vaccinated populations. Mumps outbreaks in two-dose vaccinated populations are an important phenomenon that have been reported in Western countries over the past 6 y,8,14,15,17 and their occurrence underscores the importance of this type of in-depth risk factor analysis. Additionally, this paper takes a novel approach to assessing mumps transmission risk factors, carefully measuring parameters relating to exposure at the yeshiva, grade and class levels. The negative findings in our investigation underscore the inadequacies of our current tools in measuring and understanding mumps transmission.
This investigation also highlights the challenges of mumps outbreak control with current vaccination policies in highly vaccinated two-dose populations. Yeshivas followed NYCDOH guidance and sent symptomatic students home for five days. However, mumps can spread before parotitis onset and from persons with asymptomatic infections (~30% of those infected are asymptomatic).1 The Centers for Disease Control and Prevention (CDC) recommends reducing opportunities for close contact during mumps outbreaks in highly vaccinated populations.11 However, this strategy might not always be effective in decreasing transmission, nor is it always feasible. Two MMR doses are sufficient to prevent mumps in most settings, as evidenced by the broader community remaining generally protected from mumps during this outbreak. The unique yeshiva setting, with the densely populated environment and prolonged face-to-face contact, may have led to a viral inoculum that overcame immunity, resulting in vaccine failure. However, had vaccination coverage not been so high, there would likely have been many more mumps cases, with disease that was more severe.9,23 Maintaining high MMR vaccination coverage remains the most effective way to prevent future outbreaks and limit their spread.
Methods
Inclusion criteria
We used mumps cases reported to NYCDOH to ascertain which yeshivas had mumps between 9/1/2009, when school resumed after summer break, and 3/30/2010, when school stopped for Passover. Since Brooklyn had the most reported cases, eligible all-male yeshivas were required to be located there and have: 1) at least one reported case in a student in the most affected age group (13–18 y in grades 9–12); 2) ≥ 80 students in grades 9–12; 3) ≥ 3 grades (i.e., 9th-11th or 10th-12th) to allow for comparison between upper and lower grades; and 4) two-dose MMR vaccine coverage ≥ 90% prior to 9/1/2009. On the NYCDOH list of reported cases, school information was available for 238 (60%) male mumps case-students aged 13–18 y, but not all of them attended yeshivas that met the inclusion criteria.
Vaccination coverage assessments
Vaccination status was determined through school record reviews by NYCDOH. Two-dose vaccination coverage was calculated by determining the number of students with ≥ 2 valid doses divided by the total number of students enrolled. MMR vaccine doses were considered valid if the first dose was given on or after the first birthday, the second dose at least 28 d later and if dates were recorded.7
Classroom survey
All yeshivas that met the inclusion criteria were sent classroom surveys that asked administrative staff to report the number of students, classrooms and grades in the yeshiva. Students were asked to self-report whether they had mumps-like illness, which was defined as fever and swelling in the jaw or cheeks, from 9/1/2009 –3/30/2010; they also reported whether they saw a healthcare provider for mumps symptoms and stayed home from school for mumps.
School-based environmental factors survey
We documented average school day length; time spent in the classroom, beis midrash, cafeteria and prayers; room dimensions, which we calculated by measuring the length and width; room arrangement (i.e., face-to-face with a chevrusa or facing forward); mixing (e.g., number of chevrusas, integration of grades in school or on buses); type of school ventilation system; and school prevention measures. Dimensions of one classroom per grade were measured and used to impute dimensions for classes of similar enrollment within each school.
Data analysis
Data were analyzed in SAS 9.2 (SAS Institute Inc., Cary, NC). We calculated room density by dividing the number of students in the room by the square footage. To calculate daily mean density per class, we multiplied the density of each setting (e.g., classroom, study hall) by the proportion of hours the class spent in that room per day; we then summed the weighted density for each setting.
We examined the relationship between the mumps attack rate in each class, daily mean density, number of hours per school day, number of chevrusas a student had per day and total hours that students spent face-to-face with their chevrusas. Univariate analyses were conducted; variables significantly associated at the p < 0.05 level were used in multivariate analysis. We used generalized estimating equations to account for clustering of yeshivas and grades. Multicollinearity and interaction between variables were assessed.
Human ethics determination
The project titled “Environmental Factors Potentially Associated with Mumps Transmission in Yeshivas during a Mumps Outbreak among Highly Vaccinated Students— Brooklyn, New York, 2009−2010” was reviewed by the National Center for Immunization and Respiratory Diseases (NCIRD) Human Subjects Contact and determined to be Public Health Practice: Outbreak Response. Since the project was not considered to be research, no further action was required by CDC for human subjects protections in accordance with federal regulation for the protection of human subjects in research.
Acknowledgments
The authors would like to thank the Rabbis at the yeshivas for taking the time to meet with us; Craig Borkowf, Quantitative Sciences and Data Management Branch, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Centers for Disease Control and Prevention (CDC); Manoj Gambhir, PhD, MRC Centre for Outbreak Analysis and Modeling, Imperial College London and Modelling Unit, National Center for Immunization and Respiratory Diseases, CDC; Ayaan Gedi, MPH and the Program Support Unit; Mekete Asfaw, Luis Baez, Margaret Doll, Kisha Cummings and the Surveillance Unit, Bureau of Immunization, New York City Department of Health and Mental Hygiene; and Eileen Birmingham, MD, MPH, Johns Hopkins Bloomberg School of Public Health.
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. No external funding sources were used to gather the data, analyze the data or write up the findings.
Disclaimer
The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the CDC, US (Department of Health and Human Services).
Previous presentations
This article has not been presented previously at a meeting or conference.
Footnotes
Previously published online: www.landesbioscience.com/journals/vaccines/article/22415
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