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Effectiveness of Previous Mumps Vaccination During a Summer Camp Outbreak

^a Epidemic Intelligence Service, Office of Career Workforce and Development
^d Epidemiology Branch, Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
^b New York State Department of Health, Albany, New York
^c Sullivan County Health Department, Monticello, New York
^e School of Public Health, State University of New York, Albany, New York

	ABSTRACT

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OBJECTIVES. Mumps is a vaccine-preventable disease that may cause outbreaks. In July 2005, an outbreak of mumps occurred during a children's summer camp in upstate New York. An investigation was initiated to describe the cases and evaluate vaccine effectiveness.

METHODS. A retrospective cohort study was conducted among 541 children from the United States and abroad who attended a 1- or 2-month overnight summer camp. Patients with mumps were interviewed; serologic analysis was conducted for 6 case patients. Vaccine effectiveness was calculated by retrospective review of immunization records for 507 attendees who were eligible for vaccination and had verified immunization history.

RESULTS. Thirty-one camp attendees were identified as having mumps (attack rate: 5.7%); 5 (83%) of 6 patients tested had positivity for mumps immunoglobulin M. Of the 507 participants (including 29 patients) with available immunization history, 440 (including 16 [87%] patients) were 2-dose recipients of mumps vaccine (attack rate: 3.6%); 46 participants (including 4 [9%] patients) were 1-dose recipients (attack rate: 8.7%); and 21 (including 9 [4%] patients) were unvaccinated (attack rate: 42.9%). Vaccine effectiveness was 92% for 2 doses and 80% for 1 dose.

CONCLUSIONS. Outbreaks of mumps in settings such as summer camps can occur despite high vaccination rates. Vaccine effectiveness for 2 mumps vaccinations was greater than vaccine effectiveness for 1 mumps vaccination. Therefore, recommendation of 2 mumps vaccinations for summer camp participants continues to be appropriate. Control of mumps disease relies on broad vaccination coupled with correct clinical diagnosis and strict control measures.

Key Words: mumps • measles-mumps-rubella vaccine • immunizations • disease outbreaks

Abbreviations: ACIP—Advisory Committee for Immunization Practices • VE—vaccine effectiveness • CDC—Centers for Disease Control and Prevention • Ig—immunoglobulin • RT-PCR—reverse transcription–polymerase chain reaction • AR—attack rate • CI—confidence interval

Since mumps vaccine licensure in the United States in 1967 and the recommendation of 1 dose of measles-mumps-rubella vaccine in 1977,^1,2 mumps incidence has declined steadily. In the mid-1980s, multiple outbreaks of mumps were reported in the United States.^3–7 This resurgence of mumps disease was thought to be related predominantly to lack of vaccine coverage.⁸ In 1989, the Advisory Committee on Immunization Practices (ACIP) recommended 2 doses of measles-mumps-rubella vaccine for school-aged children and college students.⁹ This recommendation was made for measles control but also had an effect on mumps incidence.¹⁰ Nonetheless, >200 annual sporadic cases of mumps occurred in the United States during 2001–2005,^11–15 as have outbreaks among well-vaccinated populations.^16–19 Most recently, a national outbreak of mumps occurred in the United States in 2006.²⁰ The highest incidence was reported in Iowa, where most patients had received at least 1 dose of mumps vaccine.^21,22

Vaccine effectiveness (VE) in postlicensure studies was 95%,^23,24 and the overall VE of mumps vaccine in field studies remained >80%.^3–7,16,18 Theories proposed for mumps vaccine failure have been primary^16,17 and secondary.^17,18 Although 2 doses of mumps vaccine seem to confer better protection than 1,^16,19,25 few studies have been able to calculate VE of 2 doses of mumps vaccine. In the recent US outbreak, VE of 2 doses of mumps vaccine could not be measured directly because of broad vaccine coverage; however, low attack rates (ARs) among vaccine recipients were indicative of high VE.²¹

In July 2005, the New York State Department of Health was notified of a mumps outbreak during a summer overnight camp. The camp had >500 participants composed of US residents and international visitors. The latter included 40 counselors and staff from the United Kingdom, where a massive mumps outbreak was ongoing.²⁶ State and local health officials were dispatched to investigate the outbreak to confirm diagnoses and to control spread among the camp population. The epidemiologic investigation determined that the index case of the outbreak was a staff member, who was a United Kingdom resident, was unvaccinated against mumps, and had been exposed to mumps before his arrival in the United States.²⁷ This outbreak was not promptly recognized and reported and caused considerable morbidity and expense. Because certain cases occurred among people who previously had been vaccinated against mumps, the outbreak raised questions regarding mumps VE. We describe an evaluation of clinical disease among people with and without a history of vaccination and calculation of VE in this outbreak setting.

	METHODS

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Case Definition
We defined a case of mumps as parotitis that lasted 2 days with no other apparent cause in a camp participant with onset during June 30 to September 4, 2005 (1 maximum incubation period: 26 days after identification of the final case).^28–30 A confirmed case was defined as a patient with a positive mumps immunoglobulin M (IgM) antibody test on an acute serum sample or a patient who was linked epidemiologically to an IgM-positive patient.^28,29 Because there was extensive mixing among campers and staff, we assumed all camp participants to be epidemiologically linked.

Laboratory Methods
Serum samples for laboratory confirmation were obtained from all patients who were older than 18 years, gave informed consent, and were symptomatic at the time of investigation. This equaled 6 patients at 4 to 8 days from disease onset. Serum was tested at the Centers for Disease Control and Prevention (CDC). Mumps IgM was detected using a capture enzyme immunoassay developed at the CDC, and mumps IgG was detected using Wampole Laboratories Mumps IgG ELISA II assay kit (Princeton, NJ). We collected urine from the same 6 and nasopharyngeal swabs from 5 of the 6 patients for standard viral culture and reverse transcriptase–polymerase chain reaction (RT-PCR) testing. The standard RT-PCR assay used mumps short-hydrophobic gene primers as described.³¹

Case Ascertainment
The camp proprietors instructed campers and staff to report to the camp infirmary if they became ill. We actively sought to identify patients by interview of all infirmary staff and review of camp infirmary medical charts for all participants. We recorded mumps clinical manifestations including parotitis, jaw pain, sore throat, fever, headache, malaise, abdominal pain, orchitis, vomiting, meningitis, onset date, and illness duration for each patient from medical charts or through infirmary staff and patient interviews. We obtained information on mumps immunity and vaccination status from forms that were completed by a medical provider in a precamp evaluation. When the health form was incomplete, camp participants contacted their provider to review their records and verify vaccine, disease history, or serologic history. We considered a person to be immune to mumps when he or she was born before 1957, had a history of physician-diagnosed mumps before arriving at camp, had laboratory evidence of mumps immunity (positive mumps IgG before camp), or had received at least 1 mumps-containing vaccination as documented by a medical provider.³² To be valid, the first vaccination had to have occurred on or after the first birthday and the second at least 30 days after the first.³² A camp participant who did not meet any of the criteria was considered susceptible to mumps. Parental or patient recollection was not accepted as evidence of immunity. As a public health response to an outbreak, this investigation was determined not to be human-subjects research.

Statistical Analysis
Camp participants with undetermined vaccination status (eg, those unable to obtain physician records during the investigation) were excluded from analysis. Participants who were mumps-immune but had no vaccine-related immunity to mumps (ie, those who had a history of physician-diagnosed mumps disease, were born before 1957, or had positive serology before camp) were excluded as well.

VE was calculated by using the equation VE = (ARU – ARV)/ARU = (1 – RR), where ARU is the AR among the unvaccinated, ARV is the AR among the vaccinated, and RR is the relative rate.³³

Rate ratios and 95% confidence intervals (CIs) were calculated by use of exact procedures. For secondary vaccine failure calculations, individual patients were grouped according to number of years since last vaccination, and ARs were calculated for each group. Linear regression analysis was used to assess waning immunity. The outcome measure was presence of mumps disease, with years since vaccination as the independent variable. P < .05 was considered statistically significant. Statistical analyses were performed by using Epi Info 2002 software, including StatCalc 6 (CDC, Atlanta, GA).

	RESULTS

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The outbreak occurred during a 4- or 7-week overnight camp in upstate New York. This camp had 541 participants, including 368 campers and 173 staff. Median age for campers was 12 years (range: 7–15 years) and for staff was 21 years (range: 14–65 years). Campers were 47% male; staff were 43% male. The campers were assigned to 1 of 34 cabins according to age but spent substantial time in activities with children and staff members of different age groups. In addition, staff and groups of campers traveled outside the camp and were visited by groups from other camps for selected events (eg, sports competitions).

Case Descriptions
We identified 31 patients among the 541 camp participants (AR: 5.7%) who had onset of symptoms during June 30 to August 9. All patients met the confirmed case definition by either epidemiologic link to an IgM-positive patient (26 of 31 [84%]) or positive serum IgM antibody testing (5 of 31 [16%]). Serum samples from 6 (19%) patients were tested for mumps IgM and IgG. One of the 6 patients tested had received 2 doses of mumps vaccine; the remainder had received none. Five of the 6 patients, including the 2-dose recipient, were mumps IgM-positive, and all were mumps IgG-positive. None of the nasopharyngeal swabs or urine samples collected was positive by viral culture or mumps virus RT-PCR.

Case patients were distributed in 20 of the 34 cabins, and no cabin had >3 patients. Twelve (39%) patients were campers, all aged 10 to 15 years (median: 12 years), 3 (25%) of whom were male. Nineteen (61%) patients were staff, all aged 19 to 41 years (median: 21 years), 12 (63%) of whom were male. Vaccination status was unknown for 2 patients, both staff. Of the 29 patients with available immunization history, 16 (55%; 12 campers and 4 staff) had received 2 doses of mumps vaccine, 4 (14%; all staff) had received 1 dose, and 9 (31%; all staff) had received none.

Parotitis was bilateral among 8 (26%) patients. Four males, 3 unvaccinated and 1 who had received 2 mumps vaccinations, had unilateral orchitis (Table 1); all recovered spontaneously. No patients experienced meningitis or hearing loss. Clinical manifestations and illness duration did not differ significantly between vaccinated and unvaccinated patients (Table 1).

View larger version (22K): [in this window] [in a new window]   FIGURE 1 VE analysis cohort determination. Highlighted boxes denote groups that were included in VE calculations.

	DISCUSSION

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
This outbreak occurred among a highly vaccinated population. After introduction, mumps was able to persist among both susceptible and vaccinated individuals. Nonetheless, a history of 1 or 2 mumps vaccinations was effective in preventing disease. VE was higher among 2-dose recipients compared with 1-dose recipients. ARs were higher among recipients who had been vaccinated for longer a period before camp, but no statistically significant trend of waning immunity was identified.

Mumps was determined to be the causative agent responsible for this outbreak using published guidance documents.^28–30 Mumps infection was confirmed in 5 individuals by positive mumps IgM serology. By definition, a symptomatic person linked epidemiologically to a confirmed patient is also a confirmed case. Because we assumed that all camp attendees were linked epidemiologically to each other, all cases were confirmed. Six of the 19 patients among staff were selected for viral testing by culture or RT-PCR because they were symptomatic at the time of our site visit. However, specimens obtained were nasopharyngeal specimens and not buccal mucosa swabs as is recommended. In addition, nasopharyngeal specimens were obtained 4 to 8 days after onset, not immediately as is recommended.²⁹ Had we tested patients who were no longer symptomatic, we would expect serum IgM to be present in a portion, as mumps IgM is known to persist at times for months.³⁴ However, we tested only symptomatic camp staff who were 18 years of age or older at the request of the camp proprietors.

During this outbreak, signs and symptoms of mumps disease were indistinguishable between people with and without history of vaccination. This was true for mild symptoms (eg, jaw pain, sore throat), as well as a more severe manifestation of mumps, such as orchitis. Symptom similarity was described in a previous report of a mumps outbreak.⁷ No evidence of other serious sequelae existed (eg, pancreatitis, meningitis, deafness) in either group. However, such conditions might not have been observed during this outbreak because they occur at a relatively low rate.³⁵

During this outbreak, we determined VE for 1 or more dose of mumps vaccine to be comparable to previous studies. One dose of mumps VE measured in outbreak-based studies where the Jeryl-Lynn strain of mumps vaccine has been used ranged from 64% to 91%.^3–7,25 Combined VE measurements of 1- and 2-dose recipients in outbreak settings ranged from 81% to 95%.^16–19 Previous studies of mumps outbreaks have also identified higher protection of 2 mumps vaccinations compared with 1.^16,25 The more than twofold difference between ARs among 1- and 2-dose recipients found in our study indicates that 2 vaccinations were more beneficial than 1 in protecting people from mumps; however, this difference was not statistically significant (data not shown).

A majority (69%) of cases in this outbreak were attributed to vaccine failure. Previous studies have classified vaccine failure as primary or secondary and have proposed mechanisms for each. Primary vaccine failure, the failure to respond appropriately to a vaccination, would be expected to occur primarily among singly vaccinated individuals and would be expected to be reduced by a second vaccine dose, as is the case for measles.³⁶ Disease that occurs among vaccinated people because of failure to maintain effective immunity despite an initial immune response is termed secondary vaccine failure. Two predominant explanations for secondary mumps vaccine failure have been proposed: low antibody avidity to wild-type virus^37,38 and waning immunity.¹⁷ Production of mumps antibodies that were unable to prevent disease because of low avidity was not tested during this outbreak. We did identify an increase in AR among people who were vaccinated within 15 years when grouped in 5-year stretches, demonstrating a trend toward diminishing immunity over time. However, this trend disappeared after 15 years and did not demonstrate linearity when subjected to regression analysis. No cases might have been detected among those who were vaccinated >15 years before because a limited number of people were included in the group or because they had been exposed to wild-type virus before camp. However, waning immunity does not seem to be the primary explanation for mumps vaccine failure.

Our field assessment of VE is subject to certain limitations.^1,33 Mild or asymptomatic disease, expected among 20% of cases,^34,35 might not have been recognized, thereby leading to an overestimation of VE. Every case of symptomatic parotitis was likely detected. Examination of camp infirmary records for instances of parotitis not diagnosed as mumps or febrile illness not identified as mumps identified no additional cases of parotitis and only 3 cases of febrile illness without a diagnosis. The 3 were presumed to have a nonspecific viral illness and were included in the analysis as noncases. Had we chosen to exclude or include the 3 persons as patients, our VE calculations would not have been altered significantly. Only 6 of 31 cases had laboratory confirmation of the diagnosis. However, all cases were epidemiologically linked according to the standard case definition.^28,29 We determined mumps immunity and vaccination status during this investigation by using precamp evaluations that were completed by medical providers and were available for all campers and nearly all staff. Requiring provider documentation to determine vaccination status has been reported to result in more accurate VE estimates.⁶ Therefore, individuals without available history from a medical provider during the outbreak were excluded from our calculations. Equal likelihood of exposure to mumps among campers and staff was assumed. Although close contact among all members of camp that could lead to mumps transmission cannot be demonstrated, site visits to the camp revealed extensive mixing among different age groups at meals and activities. This justified classifying all symptomatic patients as mumps. Therefore, VE calculations might have been overestimated as a result of variable exposure throughout camp. Finally, our VE calculations were limited by a small sample size.

At the time of the outbreak, evidence of mumps immunity through vaccination required history of a single mumps vaccination.³² The results of this study further confirm the need for 2 doses of mumps vaccine to achieve optimal immunity. Recommending 2 doses of mumps vaccine would not be difficult or costly to implement, because most school-aged children receive 2 doses already. On May 17, 2006, in response to the outbreak of mumps ongoing in the United States, the ACIP voted to change the criteria for proof of immunity, requiring 2 doses for children and adults at high risk, and revised their outbreak-control recommendations.³⁹ This change was justified using existing data as well as the results of this outbreak investigation.

	CONCLUSIONS

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Despite low incidence and broad vaccination coverage in the United States,⁴⁰ sporadic cases and outbreaks of mumps may continue to occur. This and other outbreaks demonstrate that mumps disease can be present and is likely communicable, even within a highly vaccinated population. With variable mumps immunization uptake worldwide, a real potential for introduction and spread of mumps virus continues to exist among the US population.^41,42 The revised ACIP recommendations should help to increase overall mumps immunity, which in turn is likely to help reduce the risk for future mumps outbreaks.⁴³ However, to control the disease adequately, prevent outbreaks, and move toward the goal of elimination by 2010,⁴⁴ health care providers should have a high index of suspicion for mumps and report disease in a timely manner. In turn, public health officials should respond to reports of mumps to confirm the diagnosis, implement control measures, and prevent additional spread and outbreaks.

	ACKNOWLEDGMENTS

 
We acknowledge Barbara Bright-Motelson, MPH, Renee Nealy, MD, and other members of the New York State Department of Health Immunization Program for assistance during the outbreak investigation; Danielle Cartuccio, CHN, and Tiffany Kleingardner of the Sullivan County (New York) Health Department for assistance in outbreak control and vaccination; William Bellini, PhD, Paul Gargiullo, PhD, Luis Lowe, MS, Susan Reef, MD, Jennifer Rota, MPH, Paul Rota, PhD, and Nobia Williams of the National Center for Immunization and Respiratory Diseases; and Anindya De, PhD, and Julie Magri, MD, MPH, of the Office of Workforce and Career Development (CDC). We especially thank the camp owners, operators, staff, and campers for cooperation during this investigation.

	FOOTNOTES

 
Accepted Feb 7, 2007.

Address correspondence to Joshua K. Schaffzin, MD, PhD, New York State Department of Health, Bureau of Communicable Disease Control, Empire State Plaza, Corning Tower Room 651, Albany, NY 12237-0627. E-mail: jks05{at}health.state.ny.us

Dr Smith owns stock in Merck & Co, Inc, the manufacturer of the MMR vaccine. All other authors have indicated they have no financial relationships relevant to this article to disclose.

The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention (CDC). The findings and conclusions in this report have not been formally disseminated by the CDC and should not be construed to represent any CDC determination or policy.

	REFERENCES

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