Original Article

Consequences of Undervaccination — Measles Outbreak, New York Metropolis, 2018–2019

List of authors.
  • Jane R. Zucker, 1000.D.,
  • Jennifer B. Rosen, Yard.D.,
  • Martha Iwamoto, M.D.,
  • Robert J. Arciuolo, Grand.P.H.,
  • Marisa Langdon-Embry, M.Sc.,
  • Neil Yard. Vora, Thou.D.,
  • Jennifer L. Rakeman, Ph.D.,
  • Beth M. Isaac, Chiliad.P.H.,
  • Antonine Jean, M.P.H.,
  • Mekete Asfaw, A.A.S.,
  • Simone C. Hawkins, M.S.,
  • Thomas G. Merrill, J.D.,
  • Maura O. Kennelly, M.P.H.,
  • Beth Maldin Morgenthau, Yard.P.H.,
  • Demetre C. Daskalakis, Yard.D., Thousand.P.H.,
  • and Oxiris Barbot, M.D.

Abstract

Background

Measles was alleged eliminated in the Us in 2000, just the risk of outbreaks attributable to international importations remains. An outbreak of measles in New York City began when i unvaccinated kid returned abode from State of israel with measles; onset of rash occurred on September 30, 2018, 9 days after the child returned home.

Methods

We investigated suspected cases of measles by conducting interviews, reviewing medical and immunization records, identifying exposed persons, and performing diagnostic testing. Measles–mumps–rubella (MMR) vaccine (given as either MMR or measles–mumps–rubella–varicella vaccine and collectively referred to equally MMR vaccine) uptake was monitored with the employ of the Citywide Immunization Registry. The total direct cost to the New York City Section of Health and Mental Hygiene was calculated.

Results

A total of 649 cases of measles were confirmed, with onsets of rash occurring between September 30, 2018, and July 15, 2019. A majority of the patients (93.4%) were function of the Orthodox Jewish customs, and 473 of the patients (72.nine%) resided in the Williamsburg expanse of Brooklyn, New York. The median age was 3 years; 81.2% of the patients were 18 years of age or younger, and 85.8% of the patients with a known vaccination history were unvaccinated. Serious complications included pneumonia (in 37 patients [five.seven%]) and hospitalization (in 49 patients [7.6%]); among the patients who were hospitalized, 20 (40.8%) were admitted to an intensive care unit. As a result of efforts to promote vaccination, the percentage of children in Williamsburg who received at least one dose of MMR vaccine increased from 79.v% to 91.one% amid children 12 to 59 months of historic period. As of September ix, 2019, a total of 559 staff members at the Department of Wellness and Mental Hygiene (7% of the agency) had been involved in the measles response. The cost of the Department of Health and Mental Hygiene response was $eight.4 million.

Conclusions

Importation of measles and vaccination delays among young children led to an outbreak of measles in New York City. The outbreak response was resource intensive and caused serious illness, particularly among unvaccinated children.

Introduction

Earlier licensure of the kickoff measles vaccine in 1963, approximately 500,000 cases of measles and 500 measles-related deaths were reported annually in the United States.1 Measles was declared eliminated in the U.s. in 2000.two However, the hazard of reintroduction and transmission is a constant threat because of connected measles activity in much of the earth.3-five Periodic measles outbreaks reported in the United states of america show the consequences of this ongoing risk.1,4

In New York City, an international gateway for travel, imported cases of measles are identified on a regular basis, and several measles outbreaks have been reported since 2000. The terminal two outbreaks occurred in 2013 and 2014, with 58 and 25 cases, respectively.6,vii The nearly recent outbreak began when one unvaccinated kid returned home from Israel with measles; onset of rash occurred on September 30, 2018, 9 days subsequently the child returned dwelling house. At that fourth dimension, a large measles outbreak had been occurring in Israel.viii Boosted measles importations from Israel and from parts of Europe to New York City ignited what has go the largest measles outbreak in the U.s. since 1992. Nosotros depict the epidemiologic features of this outbreak; the control measures that were taken, including use of the public health authority; and the importance of the existing public health infrastructure in mounting an effective response.

Methods

Identification of Measles Cases

All cases of suspected measles that occur in the v boroughs of New York Urban center are required to be reported immediately to the New York City Section of Wellness and Mental Hygiene.9 All reports are investigated by interviewing the patient or the patient'southward parent or guardian, reviewing medical and immunization records, and identifying the probable source of infection. Persons built-in before 1957 are considered to be immune.x Persons (contacts) are identified as having been potentially exposed to measles if they had been in the aforementioned identify at the aforementioned fourth dimension (or within 2 hours) as a person contagious with measles (e.m., at an outpatient medical facility, apartment building, or school).

The New York City Public Wellness Laboratory performed about of the diagnostic testing for measles. Serum specimens were tested for measles-specific IgM with the use of a qualitative enzyme-linked immunosorbent analysis (ELISA) and for measles-specific IgG with the utilize of a qualitative chemiluminescent immunoassay (the DiaSorin Liaison Measles IgG assay). Measles virus RNA was detected with the apply of a real-time reverse-transcriptase–polymerase-concatenation-reaction (RT-PCR) analysis (TaqMan RT PCR, Applied Biosystems) targeting the measles nucleoprotein factor.11 Genotyping of the measles nucleoprotein gene in measles-positive specimens was performed at the Wadsworth Center Laboratory of Viral Diseases.12

An outbreak case was divers as a patient who had a rash and either laboratory evidence of infection (i.e., detection of measles virus RNA or measles-specific IgM) or an epidemiologic link to a laboratory-confirmed example and in whom the onset of symptoms occurred on or afterwards September 30, 2018. Patients with measles considered to be part of the outbreak included New York Metropolis residents and international visitors to New York City who were either office of the Orthodox Jewish community or resided in, or were traceable to, a neighborhood with customs transmission; domestic visitors to New York City were not included in the count. Certain patients for whom clinical information was not bachelor were included in the example count if the diagnostic tests (RT-PCR assay or assay to detect IgM) were positive and if they otherwise met the criteria described above. Because of the potential for a imitation positive IgM assay, patients who lacked clinical information and had but a positive IgM assay were included only if they were confirmed to be unvaccinated, since the likelihood of a true infection would increase in the absence of vaccination.

No financial or in-kind funding was provided to conduct this evaluation beyond regular urban center revenue enhancement levy funds and routine funding from the Centers for Disease Control and Prevention for surveillance activities and emergency preparedness.

Measles–Mumps–Rubella and Measles–Mumps–Rubella–Varicella Vaccination

In New York City, all vaccine doses administered to persons 18 years of historic period or younger are required to be reported to the Citywide Immunization Registry — a database of birth and immunization records — within fourteen days later on assistants.thirteen,14 The Citywide Immunization Registry was used to obtain the immunization condition of cases and contacts.

For population-level analyses, the percent of children 12 to 59 months of historic period in New York Metropolis who had received 1 or more than doses of measles-containing vaccine (given every bit either measles–mumps–rubella [MMR] or measles–mumps–rubella–varicella [MMRV] vaccine and collectively referred to every bit MMR vaccine; ane% of measles-containing vaccines reported to the Citywide Immunization Registry were not MMR or MMRV vaccine) was calculated on the basis of doses reported to the Citywide Immunization Registry. The percentage of children who had received MMR vaccine was calculated for each New York Metropolis Zero Code. For this calculation, the numerator was the number of children 12 to 59 months of age who had received at least one valid dose of MMR vaccine, had a current address in a New York Metropolis ZIP Code, and were not reported past their caregiver as having moved out of New York City — data we obtained from the Citywide Immunization Registry — and the denominator was the 2018 New York City population estimates, which were modified to create sub-borough–level estimates based on the county-level interpolated intercensal population estimates from the U.S. Census Bureau.fifteen MMR vaccinations in Zilch Code areas where measles had been detected were aggregated to determine neighborhood-level coverage. Coverage was mapped with ArcMap software, version 10.5.1 (Esri). Separately, the number of doses of MMR vaccine administered to children 12 to 59 months of age (on the basis of the criteria described above) was tracked; data were analyzed on a weekly basis, and the numbers of doses were compared with those from the same period in the previous yr. Analyses were performed with the apply of SAS software, version 9.4 (SAS Institute).

Resource Mobilization

To ensure a robust public health response, the Department of Wellness and Mental Hygiene expanded its outbreak response on the basis of the epidemiologic features of the outbreak. These efforts culminated in the full agency-wide emergency activation of its Incident Command System on March 27, 2019.16

Cost Evaluation

The total directly cost to the Department of Health and Mental Hygiene was calculated equally the sum of inputs (i.e., supplies, materials, equipment, and services) and personnel (i.east., bacon). The personnel cost included overtime pay too as the salaries of temporary-agency personnel and staff members of the Section of Wellness and Mental Hygiene for time devoted to the outbreak response during regular business hours.

Results

Details of the Outbreak

Numbers of Outbreak-Associated Cases of Measles.

Shown are the numbers of cases of measles co-ordinate to the date of onset of rash and the neighborhood of residence in New York City. Dates are based on the post-obit hierarchy, according to bachelor data: appointment of onset of rash, date of laboratory report, and date of provider report.

 Age Group and Vaccination Condition of Patients with Measles Infection.

As of September 3, 2019, when the outbreak was declared to be over (two incubation periods [42 days] later on the infectious menses of the final case ended), 649 cases of measles were confirmed, with onsets of rash occurring between September xxx, 2018, and July 15, 2019 (Figure 1). The median age of the patients was iii years (range, 1 month to 70 years), and 60.1% were male. A total of 81.2% of the patients were xviii years of historic period or younger, and 85.8% of the patients with a known vaccination history were unvaccinated (Tabular array ane).

A majority of the patients (93.4%) were office of the Orthodox Jewish customs and resided in the Williamsburg (473 patients [72.9%]) or Civic Park (121 patients [18.6%]) neighborhood of Brooklyn. Most of the patients in both neighborhoods were children, but in Borough Park, the median age shifted from 1 twelvemonth (during the period from October 2018 through January 2019) to 13.5 years (during the period from February 2019 through July 2019). The median age of the patients in Williamsburg was 3 years. In April 2019, the outbreak spread from Borough Park to neighboring Sunset Park, Brooklyn, where limited measles transmission occurred. Limited transmission as well occurred in Crown Heights, Brooklyn (viii patients [1.ii%]), where half the cases were in persons 18 years of age or older. Additional affected patients resided in other New York Metropolis neighborhoods simply generally were associated with exposure that linked back to Williamsburg, Borough Park, or other areas outside New York Urban center where measles was present. Amongst the 43 patients (6.six%) who were not part of the Orthodox Jewish community, a majority (38 patients) were Latino.

Complications in Patients with Measles Infection.

Complications amid the 649 patients included diarrhea (14.2%), otitis media (9.7%), and pneumonia (v.7%). No deaths were reported (Table 2). Among 49 patients (seven.6%) who were hospitalized, twenty (40.viii%) were admitted to an intensive unit care, x (20.4%) underwent noninvasive mechanical ventilation, and 40 (81.six%) had more than than i complication (Table S1 in the Supplementary Appendix, available with the total text of this article at NEJM.org). Among 37 children who were hospitalized with measles, 35 (94.6%) were confirmed to be unvaccinated; of the remaining children, neither of whom had an underlying medical status, 1 kid had received one dose of MMRV vaccine and the other child had an unknown vaccination condition. The vaccination status was unknown for all 12 hospitalized adults. Measles was reported in iii pregnant persons at 14 weeks, 33 weeks, and 34 weeks of gestation; no complications associated with measles occurred, and all the infants were born good for you and tested negative for measles. 1 hospitalized child was immunocompromised. Three of 5 patients built-in before 1957 were hospitalized.

Among the 649 cases of measles, 564 (86.nine%) were confirmed on the basis of laboratory testing, including xx in persons for whom in that location was no clinical information, and 85 (13.one%) were confirmed on the basis of epidemiologic linkage to another laboratory-confirmed instance. Genotype D8, one of the virtually common genotypes circulating worldwide,iv was identified in all 355 outbreak-related patients in whom genotyping of the measles virus strain was performed. X confirmed cases of measles identified during the outbreak period were non considered to be part of the outbreak, because they occurred in persons who were not part of the Orthodox Jewish community and they were non traceable to a neighborhood with community manual: six cases were internationally imported or had links to international importations (ane of which was genotype B3 [distinct from that of the outbreak]), 1 case not internationally imported was genotype B3 and one case was epidemiologically linked to this case, and 2 cases had no geographic or epidemiologic clan with the outbreak. An additional 33 patients were investigated for measles but were non counted as having confirmed cases because they had previously received MMR vaccine and the measles vaccine strain (genotype A) was detected.

Manual Settings of Patients with Measles Infection.

Transmission commonly occurred in settings including the home (through contact with immediate and extended family unit members, friends, and neighbors), schools, and childcare programs. Measles was acquired from outside New York Urban center in 11 patients; these locations included State of israel (4 patients), the United Kingdom (2 patients), Ukraine (1 patient), New York exterior New York Urban center (three patients), and New Jersey (1 patient). A total of forty.8% of the patients were idea to have acquired the disease through community-wide transmission, with no single betoken source reported; the manual setting could non exist identified for four.8% of the patients (Table 3).

Control Measures

More than 20,000 named contacts were identified, including an estimated 1000 exposures among infants younger than 1 year of age, 400 exposures among pregnant persons, and 100 exposures amongst potentially immunocompromised persons. Endeavor was made to inform contacts about the exposure either past personnel at the location of exposure (e.g., a schoolhouse or medical facility) or by the Department of Health and Mental Hygiene, and the contacts were referred for postexposure prophylaxis with MMR vaccine, allowed globulin, or home quarantine, as indicated.10

Unvaccinated children were identified with the use of the Citywide Immunization Registry; the Section of Health and Mental Hygiene and medical facility personnel and so used this information to contact patients or their parents nearly making an engagement for MMR vaccination and to guess MMR vaccination coverage at the wellness care facility level. Recommendations for MMR vaccination were revised for persons residing in, or regularly spending time in, neighborhoods of New York City in which ongoing measles transmission was nowadays. The recommendations included an early, additional dose of MMR vaccine for infants vi to eleven months of age (which did not count toward the routine two-dose serial), an early on second routine dose of MMR vaccine for children i to 4 years of historic period, and 2 doses of MMR vaccine for adults born in 1957 or later who did not have documentation of previous vaccination with two doses of a measles-containing vaccine or whose vaccination condition was unknown.

On December half-dozen, 2018, schools and childcare programs in Williamsburg and Borough Park were notified that all children without historic period-appropriate MMR vaccination or proof of measles immunity,x including those with medical or religious exemptions, were to be prohibited from attention school and childcare programs. Weekly audits of 101 facilities were conducted to ensure adherence to the required exclusions. Under an order of the commissioner of the Department of Wellness and Mental Hygiene, programs that did not attach to the requirements were subject to fines, closure, or both. Twelve programs, including three schools and nine childcare programs, were closed temporarily during the response. An emergency order, which required MMR vaccination or proof of measles immunity for all persons living, working, or going to schoolhouse in the four affected Williamsburg Naught Code areas, was issued on April 9, 2019.17 A total of 232 summonses were issued past the Section of Health and Mental Hygiene to individual persons for non adhering to the emergency order. Boosted control measures are described in the Supplementary Appendix.

Vaccination Coverage

Numbers of Doses of MMR Vaccine Administered to Children 12 to 59 Months of Age in Williamsburg, Brooklyn.

School and childcare exclusion letters were issued on December six, 2018, on Dec 21, 2018, and on Jan 9, 2019. Updated exclusion guidance was issued on February 13, 2019, to permit some students in kindergarten through 12th class to attend school. Schools and childcare facilities were notified of updated exclusion requirements on April 2, 2019. Adapted from the New York City Department of Health and Mental Hygiene Citywide Immunization Registry; data are as of September 1, 2019. The measles–mumps–rubella (MMR) vaccine was given as either MMR or measles–mumps–rubella–varicella vaccine and collectively referred to as MMR vaccine.

From October 1, 2018, through September i, 2019, a total of 188,635 doses of MMR vaccine were administered to children 12 to 59 months of historic period by medical providers citywide in New York City, and 11,964 doses were administered in Williamsburg; there were 23,320 more doses citywide and 4216 more doses in Williamsburg than the respective doses administered in the same time period during the previous year. The percentage of children 12 to 59 months of historic period in Williamsburg who received at least one dose of MMR vaccine increased from 79.5% to 91.1% between October 1, 2018, and September i, 2019. In addition to expected peaks in MMR vaccinations associated with adherence to vaccination requirements for the commencement of school, several outbreak-related interventions were associated with an increase in MMR vaccinations (Figure 2).

Cost Evaluation

As of September nine, 2019, a total of 559 staff members at the Department of Health and Mental Hygiene (vii% of the staff members in the agency) had worked on the measles response in time-express waves. At the meridian of the agency'south participation in belatedly May 2019, a total of 261 staff members were supporting the measles response. As of August 31, 2019, $viii.4 million had been spent on the response: $1.5 meg in inputs and $6.ix million in personnel.

Give-and-take

This measles outbreak is the largest reported in the United states since 1992.18 The outbreak occurred considering of multiple importations of measles into a community that had been targeted by antivaccination groups, resulting in a large undervaccinated and susceptible population of young children, primarily between 1 and iv years of historic period.19 We and others take observed previous outbreaks of vaccine-preventable diseases among persons with low vaccination coverage.seven,twenty-22

During focus groups conducted past the Section of Health and Mental Hygiene after a mumps outbreak in 2009–201023 in this same community, mothers expressed concern well-nigh vaccines and autism, vaccine safety, and whether children are receiving too many vaccines likewise early in life. Antivaccination sentiments were deepened when an organization targeted this customs with misleading materials regarding the risk of vaccination.xix To address these concerns, the Section of Wellness and Mental Hygiene reprinted and mailed two booklets that provided authentic information well-nigh vaccines to 29,000 households in Borough Park and Williamsburg, and a campaign was launched to gainsay vaccine myths in affected communities.24,25

Interrupting measles manual was challenging because of the complexity of the outbreak, including numerous bondage of transmission fueled by importation, nonadherence to the school and childcare centre exclusions mandated by the Department of Health and Mental Hygiene, and manual in schools and childcare centers with loftier numbers of religious exemptions to vaccination. Anecdotal reports suggested that parents were property "measles parties" to deliberately expose their unimmunized children to measles. In addition, in some cases, the diagnosis of measles was made several weeks to months after illness had begun, when the children's parents brought them to a medical provider for serologic testing so they could return to school. Delayed identification of measles in these situations hindered the ability of the Section of Health and Mental Hygiene to implement real-time control measures.

The complications reported during this outbreak are a reminder of the seriousness of measles. The observed percentage of patients with complications is consistent with that seen historically. From 1985 to 1992, diarrhea was reported in 8% of patients, otitis media in 7%, pneumonia in 6%, and death in less than one%.i In dissimilarity, agin events after measles vaccination are estimated to occur at a rate of 30.5 adverse events per 1000000 doses distributed (<0.001%).26

To command this outbreak, the Department of Wellness and Mental Hygiene implemented several unique policy decisions. The exclusions of all unvaccinated children in schools and childcare programs affected by the outbreak in Williamsburg and Civic Park were justified, given the importance of these settings for transmission. In one school, i contagious student led to more than 25 infections in other students and to further spread to multiple other persons outside the school. Overall, in addition to the ix.7% of persons who acquired measles in a schoolhouse or childcare facility, an additional 48 persons caused measles from school or childcare attendees. The Section of Wellness and Mental Hygiene required vaccination amid persons living in a specific geographic surface area. The Board of Wellness of New York Urban center agreed with this approach and voted to support the agency'southward strategy.27 Furthermore, the Supreme Courtroom of Kings County upheld the authorization of the Section of Wellness and Mental Hygiene to require vaccination.28,29 Although some people had questioned whether requiring vaccination would be effective,30 the success of these two approaches is evidenced by the increase in MMR vaccination and the decrease in measles cases seen subsequently the implementation of these strategies.

The importance of existing infrastructure in implementing an effective measles outbreak response cannot be overstated. The Citywide Immunization Registry was established in 1996, and decades of investment take produced an immunization information system with high provider participation and quality data.31,32 After September eleven, 2001, the Department of Health and Mental Hygiene leveraged federal public health and health care organisation preparedness funds to invest in staff, create and exercise response plans, and develop a strong incident control structure, all of which provided a mechanism to speedily mobilize resources. The cost of $eight.iv million underestimates the total cost of the outbreak and is limited to the public wellness response of the Department of Health and Mental Hygiene; it does non account for costs to medical facilities, other agencies, patients, and the affected communities and does non include the in-kind costs of staff members at the Section of Wellness and Mental Hygiene who are funded by outside agencies or the indirect costs of taking staff away from routine duties. The adding of costs incurred for staff working on the measles response during regular business organisation hours was dependent on staff remembering to document time designated for the measles outbreak.

Measles is one of the nigh contagious infectious diseases.33 Fifty-fifty a single person with measles tin lead to a large outbreak when the virus is introduced into an area with vaccination coverage below that which would exist needed to maintain herd immunity. In a globally mobile world, an alphabetize of suspicion for measles should be maintained when a person presents with a clinically compatible illness so that the implementation of immediate control measures and diagnostic testing tin can brainstorm if needed. Global efforts to control or eliminate measles may reduce the brunt of measles both abroad and in the United states of america.three Combatting antivaccination misinformation at the local, national, and global level must remain a priority.34 In New York Urban center, the express manual of this outbreak across the Orthodox Jewish community highlights the effectiveness of a high-quality, national ii-dose MMR vaccination program in maintaining high population-level immunity.

Funding and Disclosures

Disclosure forms provided by the authors are available with the total text of this article at NEJM.org.

Drs. Zucker and Rosen and Drs. Daskalakis and Barbot contributed equally to this article.

The findings and conclusions in this report are those of the authors and practice non necessarily represent the official position of the New York City Department of Health and Mental Hygiene or the Centers for Illness Control and Prevention.

Nosotros thank the dedicated staff at the New York City Department of Wellness and Mental Hygiene; the provider community; our partners and stakeholders in the customs; Patrick Bryant, Sara Griesemer, and Tugba Yildirim of the Wadsworth Center Laboratory of Viral Diseases for the genotyping of measles specimens; the staff at the Segmentation of Viral Diseases, National Heart for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, particularly Kiana Anthony, Heather Colley, and Christine Badeau, for serologic testing and Manisha Patel and Paul Gastañaduy for their guidance; and the New York Country Section of Health for their ongoing collaboration and updates on measles activity in the residue of New York State.

Author Affiliations

From the New York City Section of Health and Mental Hygiene, New York (J.R.Z., J.B.R., M.I., R.J.A., Grand.L.-Eastward., N.Thou.5., J.L.R., B.Thousand.I., A.J., K.A., South.C.H., T.Thou.Thou., M.O.Grand., B.M.M., D.C.D., O.B.), and the Centers for Disease Command and Prevention, Atlanta (J.R.Z., N.M.V.).

Address reprint requests to Dr. Zucker at the New York Metropolis Department of Wellness and Mental Hygiene, Bureau of Immunization, 42-09 28th St., CN21, Rm. v-97, Queens, NY 11101, or at [electronic mail protected].

Supplementary Textile

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