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A Limited Measles Outbreak in a Highly Vaccinated US Boarding School

Lorraine F. Yeung, MD, MPH^*,, Perrianne Lurie, MD, MPH, Gustavo Dayan, MD^||, Eduard Eduardo, MPH^¶, Phyllis H. Britz, RN, Susan B. Redd^||, Mark J. Papania, MD, MPH^|| and Jane F. Seward, MBBS, MPH^||

^* Epidemic Intelligence Service, Epidemiology Program Office
Division of Birth Defects and Developmental Disabilities, National Center on Birth Defects and Developmental Disabilities
^|| Viral Vaccine-Preventable Diseases Branch, Epidemiology & Surveillance Division, National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia
Pennsylvania Department of Health, Harrisburg, Pennsylvania
^¶ Columbia University, New York, New York

	ABSTRACT

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Objectives. We investigated a measles outbreak that began in March 2003 in a Pennsylvania boarding school with >600 students to identify all cases, including the source; implement outbreak control measures; and evaluate vaccine effectiveness.

Methods. Measles was suspected in any person at the school with a generalized rash and fever during March 21 to May 28, 2003 and investigated with serologic testing. We reviewed vaccination history from school records and conducted a survey to determine country of measles vaccination. Vaccine effectiveness was calculated using the cohort method.

Results. We identified 9 laboratory-confirmed cases at the school: 8 students and 1 staff member. Among them, 2 had never received any doses of measles-containing vaccine (MCV), 1 received 1 dose of MCV, and 6 received 2 doses of MCV. Three of the 6 who received 2 doses of MCV received both doses outside the United States. The source case had been infected in Lebanon. Two laboratory-confirmed spread cases were identified in New York City. Measles virus of genotype D4 was isolated in cases from the school and New York City. Of the 663 students in the school, 8 (1.2%) had never received any doses of MCV, 26 (3.9%) had received 1 dose, and 629 (94.9%) had received 2 doses before the outbreak. Vaccine effectiveness among students who had received 2 doses of MCV was 98.6%. However, students who received both doses outside the United States had a higher attack rate (3 of 75) than those who received both doses in the United States (3 of 509; rate ratio: 6.8; 95% confidence interval: 1.4–33.0).

Conclusions. This is the largest measles outbreak to occur in a school in the United States since 1998, but it was limited to only 9 cases in a boarding school with >600 students. The limited extent of this outbreak highlights the high level of population immunity achieved in the United States through widespread implementation of a 2-dose measles-mumps-rubella vaccination strategy in school-aged children. States and schools should continue to enforce strictly the 2-dose measles-mumps-rubella vaccination requirement and, in an outbreak setting, consider revaccinating students who received measles vaccine outside of the United States. Continued vigilance by health care providers is needed to recognize measles cases.

Key Words: measles • measles-mumps-rubella vaccine • vaccines • disease outbreaks • immunizations • school • school-aged children

Abbreviations: MCV, measles-containing vaccine • MMR, measles-mumps-rubella • PADOH, Pennsylvania Department of Health • IgM, immunoglobulin M • IgG, immunoglobulin G • VE, vaccine effectiveness • CI, confidence interval

Measles is a highly contagious rash illness that has been vaccine-preventable in the United States since 1963. In the prevaccine era, most measles cases occurred in children who were younger than 10 years, with the highest age-specific incidence among children aged 2 to 4 years.¹ Although routine immunization rapidly decreased measles incidence in preschool children, controlling measles in school-aged children was a public health challenge because of high contact rates in school settings. State public health programs responded to this challenge by establishing requirements for measles vaccination for school entry. During 1966–1970, fewer than half of the states in the United States had school immunization requirements. In 1977, 82% of 57345 reported measles cases occurred in children who were 5 to 19 years of age. In 1978, the incidence of measles in states that strictly enforced school immunization requirements was 90% lower than states that did not enforce requirements.² Therefore, a nationwide childhood immunization initiative commenced with major emphasis on enactment and enforcement of school immunization requirements. By 1981, all states had put into place the requirement of 1 dose of measles-containing vaccine (MCV) most commonly administered as measles-mumps-rubella (MMR) vaccine for initial school entry.³ In the 1980s, measles was less common among school-aged children and adolescents; however, sporadic outbreaks continued to occur even in schools with very high 1-dose MMR vaccine coverage. This prompted the 1989 recommendation for a second dose of MMR vaccine for school-aged children.⁴ Throughout the 1990s, the 2-dose requirement for school-aged children was gradually implemented, with an estimated 82% of school-aged students throughout the United States covered by a requirement in 2001. In a recent survey, measles vaccine coverage was assessed among elementary school students in 28 states and among middle school students in 25 states. The median immunization coverage level for the second dose of measles vaccine was 97% (range: 56%–99%) for students who were entering elementary schools and 98% (range: 62%–99%) for students who were entering middle schools. The increase in 2-dose MMR vaccine coverage coincided with a decrease in measles incidence in school-aged children.⁵ Measles outbreaks in school-aged children decreased from 13 outbreaks with 664 cases in 1993–1995 to 9 outbreaks with 53 cases in 1999–2001.⁶ In 2002, 44 measles cases and 3 outbreaks were reported,⁷ and none of the outbreaks involved school-aged children (Centers for Disease Control and Prevention, unpublished data).

In Pennsylvania, the 2-dose requirement for school entry was implemented in 1997. By 2000, all grades (kindergarten through 12th grade) were covered by the requirement.⁸ In April 2003, the Pennsylvania Department of Health (PADOH) reported an outbreak of measles in a boarding school in eastern Pennsylvania.⁹ The Centers for Disease Control and Prevention was invited by PADOH to collaborate in the outbreak investigation. The objectives of this investigation were to identify all cases, including the source; implement outbreak control measures; and evaluate vaccine effectiveness.

	METHODS

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Case Definition and Case Finding
The outbreak setting was an all-male private boarding school in Pennsylvania with 663 students from seventh grade to junior college. We investigated and classified cases during the outbreak period, defined as between March 21 and May 28, 2003. A suspected case of measles was any person with a fever and a generalized nonvesicular rash. A confirmed case of measles had laboratory evidence of infection that included positive serology for measles immunoglobulin M (IgM), a 4-fold rise in serum immunoglobulin G (IgG) from the acute to convalescent samples, or a clinical specimen with a positive measles virus culture or positive polymerase chain reaction for measles virus.

At the school, case patients were identified through the school health center and review of the student absentee list. We also interviewed all case patients using a standard questionnaire and reviewed their medical charts to determine the presence of symptoms and complications, onset date and duration of illness and rash, duration of hospitalization, days of school or work missed, travel history, and potential contacts. In addition, we attempted to contact case patients' health care providers to verify vaccination histories. All suspected case patients were examined, and laboratory tests were performed. Laboratory confirmation was obtained using serology and viral testing. We collected acute- and convalescent-phase sera for measles IgM and IgG enzyme-linked immunosorbent assay testing and throat swab and urine samples for viral detection and genotyping using reverse transcriptase polymerase chain reaction.

Active surveillance to identify measles cases was conducted at neighboring hospitals and doctors' offices and through monitoring the state's electronic reporting system. To raise awareness of the outbreak, the school issued a "health alert" to its community. Pennsylvania health care providers and public health personnel were informed of the outbreak through the Pennsylvania Health Alert Network. The local media also disseminated information to the community. In addition, all states were notified through the national Health Alert Network and Epidemic Information Exchange.

Measles Vaccination Status
We reviewed vaccination records for all students and staff members. Students who lacked documentation for 2 valid doses of MCV (those received after 12 months of age or at least 1 month apart) were vaccinated during the outbreak. We conducted a survey to determine country of measles vaccination, and students with 2 doses of MCV were classified further according to where they received vaccine: (1) 2 doses in the United States, (2) 2 doses outside the United States, and (3) 1 dose in the United States and 1 dose outside the United States. Staff members were classified as vaccinated when they had received 1 dose of MCV and as immune when they were born before 1957.

Vaccine Effectiveness Among Students With Two Doses of MCV
Students who were vaccinated during the outbreak were excluded from the analysis. We calculated overall vaccine effectiveness (VE) among all 2-dose vaccinees and separately among US and outside-US vaccinees. VE was calculated using the cohort method according to the formula VE = 1– relative risk.¹⁰ Relative risk = attack rate among vaccinated students/attack rate among unvaccinated students.

Statistical Analyses
A 1-tailed Wilcoxon rank sum test was used to assess differences in duration of rash and days of school or work missed among vaccinated and unvaccinated patients at the school. A 1-tailed test was used because our a priori hypothesis was that having received vaccine would result in less severe symptoms (shorter duration of rash and fewer school or work days missed). P < .05 was considered statistically significant. Rate ratios and 95% confidence intervals (CIs) were calculated using exact procedures. Statistical analyses were performed using SAS software 8.0 (SAS Institute, Cary, NC) and StatXact 6 (Cytel Software Corp, Cambridge, MA).

	RESULTS

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Case Descriptions
At the school, 12 suspected measles case patients were identified and investigated between March 21 and April 15, 2003. Nine of them had positive serology and were confirmed to have measles; the other 3 were ruled out using IgM and acute and convalescent IgG titers. Eight cases occurred in students, and 1 case occurred in a staff member who worked in a dormitory (Fig 1). The source case was a 17-year-old Middle-Eastern student who traveled to Beirut, Lebanon, at the end of February 2003. He returned to the United States on March 15 and 1 day later began to feel ill with fever, headache, and cough. On March 21, he developed a generalized maculopapular rash and was taken to a local emergency department, where he received a diagnosis of a viral exanthem. On return to school on the same day, he was admitted to the school health center.

View larger version (21K): [in this window] [in a new window]   Fig 1. Number of patients with laboratory-confirmed measles (N = 11), by date of rash onset and number of MCV doses received previously, Pennsylvania and New York City (NYC), March to May 2003.

The most severe cases occurred in the 2 unvaccinated students, 13-year-old twins; each was hospitalized for 3 days for dehydration. They also had the longest duration of illness with rash lasting 9 days and 11 days, respectively, and they both missed 8 school days (Table 1). No other serious complications were reported. Compared with unvaccinated case patients, vaccinated case patients had shorter median duration of rash (5 vs 10 days; P < .05) and fewer days of school or work missed (5 vs 8 days; P < .05).

Measles Vaccination Status
Among the 663 students enrolled at the school at the start of the outbreak, 629 (94.9%) had received 2 doses of MCV; 26 (3.9%) had received 1 dose of MCV, 10 of whom had received their first dose before 12 months of age and therefore this dose was considered invalid; and 8 (1.2%) had not received any. Among these 8 students, 4 had not been vaccinated because of religious or philosophical exemptions. All students and staff who were not able to provide evidence of immunity were either vaccinated with the MMR vaccine or excluded and isolated from the campus during the outbreak. Apart from the 2 unvaccinated case patients, among the 6 remaining unvaccinated students, 5 were vaccinated and 1 refused vaccination and was excluded from the campus (he was later found to have positive serology and was readmitted to the school). Thirty-three students were vaccinated during the outbreak: 5 received the first dose, 26 received the second dose, and 2 mistakenly were given a third dose. The attack rates in unvaccinated students was 66.7% (2 of 3), in those who had received 1 dose of MCV before the start of the outbreak was 0% (0 of 26), and in those who had received 2 doses of MCV was 1.0% (6 of 627). The attack rate in students who had received both doses of MCV in the United States was 0.6% (3 of 509) and in those who had received both doses outside the United States was 4% (3 of 75).

VE Among Students With Two Doses of MCV
VE among the 627 students who had received 2 doses of MCV was 98.6% (95% CI: 92.0%–99.4%). VE was 99.1% (95% CI: 95.5%–99.8%) among the students who had received both doses of MCV in the United States. However, vaccine effectiveness was 94.0% (95% CI: 69.6%–98.3%) among the students who had received both doses outside the United States (Table 2). Students who had received both doses of MCV outside the United States were more likely to contract measles than those who had received both doses of MCV in the United States (rate ratio: 6.8; 95% CI: 1.4–33.0).

	DISCUSSION

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This outbreak illustrates the current epidemiology of measles in the United States. There is no endemic measles transmission,^{7, 13} most measles cases are linked to importations,⁷ and outbreaks are short in size and duration.⁶ It also serves as a reminder that measles disease may result in serious illness and highlights the risk that vaccine exemptors face when exposed to vaccine-preventable diseases.¹⁴ The limited spread outside the school seen in this outbreak also serves as a reminder that reducing the risk for measles in the school-aged population increases the protection from measles for the whole community.

Our source case was infected in Lebanon. Although circulating measles genotypes in Lebanon have not been described, the viral genotype D4 that was isolated from 2 cases in this outbreak is known to circulate in Pakistan and India.¹⁵ Until measles is eradicated globally, there will be an ongoing risk for imported measles cases in the United States. Despite impressive achievements in measles control throughout the world, in 2001, there were still an estimated 30 to 40 million measles cases and 745000 deaths from measles globally.¹⁶ Thus, importations into the United States are likely to continue for the foreseeable future and challenge the level of population immunity. Continued high vaccination coverage is required.

The United States was 1 of the first countries in the world to implement a 2-dose MMR vaccination policy in school-aged children.⁴ During the past decade, with progressive implementation of this policy, measles outbreaks in schools have decreased in size from a median size of 8 cases (range: 4–233) during 1993–1995 to a median size of 4 cases (range: 3–15) during 1999–2001.⁶ The larger outbreaks occurred in states without a 2-dose MMR vaccination requirement,¹⁷ in grades that were not covered by a 2-dose requirement,¹⁸ or in groups that were opposed to vaccination.¹⁹ The largest measles school outbreak in the past 6 years occurred in Anchorage, Alaska, in 1998 with 33 cases; 30 of the case patients had received 1 dose of MCV,¹⁷ as required in Alaska at that time. As states continue to implement and evaluate the 2-dose MMR vaccination requirements to cover all children from kindergarten to 12th grade, the incidence of measles should remain low in this age group. The majority of outbreaks should be limited in size and duration and should require only limited control efforts, as was seen in this outbreak.

Evaluating and enforcing school requirements ensures high 2-dose MMR vaccine coverage in US school-aged children. A 2000 survey of the states; the District of Columbia; and US territories, commonwealths, and protectorates indicated that by 2009, 52 of 54 responding programs will require a second dose for all grades.⁵ The PADOH estimates that 2-dose MMR vaccine coverage among children from kindergarten to 12th grade has been >90% since 2001 (PADOH, unpublished data). However, in addition to medical exemption, which is allowed in all states, religious and/or philosophical exemptions are permitted in Pennsylvania as in most states.²⁰ People who are exempt from vaccination place not only themselves at increased risk for contracting disease but also people around them.^{14, 21}

In this outbreak, individuals who were vaccinated with 2 doses of MCV outside the United States had a greater risk for developing measles. Reasons for this may include failure to maintain the cold chain,^{22, 23} mishandling of vaccine with respect to reconstitution, less accurate vaccination histories, or greater intensity of exposure during this outbreak. Schools with international students might consider revaccination of these individuals in an outbreak setting.

This outbreak highlights that health care providers may not readily recognize measles, a disease that is now rare in the United States. Vaccine-modified measles, which may be milder and less classical in presentation, poses more diagnostic challenges and is likely to be missed except in an outbreak setting. Measles should be considered in the differential diagnosis of patients with rash; fever; and cough, coryza, or conjunctivitis even if the patient gives a history of receiving measles vaccination. A history of travel outside the United States or contact with a traveler should raise the suspicion for measles in a patient with a clinically consistent illness. Health care providers should test suspected measles cases for measles IgM and obtain viral specimens for viral confirmation and genotyping.

Our study has several limitations. First, misclassification of vaccination status as a result of inaccuracy in the student vaccination records may have either over- or underestimated vaccine effectiveness. Second, we did not ascertain history of measles illness as a source of measles immunity, which can confound the VE calculation. Given that measles is rare in the United States, this confounding may have been more important in students who had received vaccination outside the United States. Third, even with active surveillance in place at the school, we may have missed asymptomatic and very mild cases that did not meet our suspected case definition. This could lead to misclassification of the case status and to overestimating the VE. However, these cases are not clinically significant and are unlikely to be epidemiologically relevant, as asymptomatic cases do not seem to shed measles virus in quantities required for transmission.²⁴

The small size and limited spread of this outbreak highlight the success of the measles vaccination program. However, continued efforts are needed to maintain a high level of population immunity in the United States as well as vigilance to recognize, report, and initiate public health action for measles cases. Until measles is eradicated globally, there will be an ongoing risk for imported measles cases in the United States. States and schools should continue to enforce strictly the 2-dose MMR vaccination requirement and, in an outbreak setting, consider revaccinating students who received measles vaccine outside the United States. Continued vigilance by health care providers is needed to recognize measles cases.

	ACKNOWLEDGMENTS

 
We thank the students, parents, and staff of this boarding school for participation and collaboration in this study, especially Carolyn Stahl, RNC, BSN, and Ian M. Ballard, MD. We thank the staff of the Philadelphia Department of Health and Jean Bowen, RN, Norine Mountcastle, RN, Heather Stafford, RN, BSN, and Phuoc Tran, RN, BSN, MEd, from the Pennsylvania Department of Health for assistance with outbreak control measures; Robert Levy, MD, CDC elective student, for assistance with data collection; Ynolde A. Andrews Gillan, MS, DrPH, from the New York City Department of Health for sharing information regarding New York City cases; William Bellini, PhD, Paul Rota, PhD, and Jennifer Rota from CDC for laboratory assistance; C.J. Alverson, MS, from CDC for statistical assistance; R.J. Berry, MD, MPHTM, from CDC for valuable comments regarding early drafts of the manuscript; and Mary McCauley, MTSC, from CDC for editorial assistance.

	FOOTNOTES

 
Accepted Mar 1, 2005.

Reprint requests to (L.F.Y.) National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention, 1600 Clifton Rd, MS E-86, Atlanta, GA 30333. E-mail: LYeung{at}cdc.gov

PEDIATRICS (ISSN 0031 4005). Published in the public domain by the American Academy of Pediatrics.

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This Article Abstract Full Text (PDF) P3Rs: Submit a response Alert me when this article is cited Alert me when P3Rs are posted Alert me if a correction is posted Citation Map Services E-mail this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My File Cabinet Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (7) Citing Articles via Google Scholar Google Scholar Articles by Yeung, L. F. Articles by Seward, J. F. Search for Related Content PubMed PubMed Citation Articles by Yeung, L. F. Articles by Seward, J. F. Related Collections Musculoskeletal System Related AAP Red Book topics: Measles

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