Clinical and Health Affairs
The 2009 H1N1 Influenza Pandemic and Minnesota’s K-12 Schools
Public Health Lessons Learned
By Kathryn Como-Sabetti, M.P.H., Franci Livingston, J.D., M.P.H., Pamala Gahr, M.P.H., Kayla Nagle, Karen Martin, M.P.H., Craig Morin, M.P.H., and Elizabeth Parilla, M.P.H.
Abstract
Prior to 2009, influenza pandemic planners had primarily planned for a virus that would originate in a location other than North America, giving public health officials in the United States time to determine its severity before widespread disease occurred here. Thus, response plans for schools focused on closure in the case of a severe pandemic and potential closure in the event of a moderate one. The 2009 H1N1 pandemic, however, presented a different scenario. The severity of 2009 H1N1 was initially unknown and later was determined to be mild to moderate. Thus, as the pandemic unfolded, state and national public health entities found themselves adapting their recommendations for school closure. This article reviews Minnesota’s experience with 2009 H1N1, focusing on the pandemic among school-aged children during the spring (April to August 2009) and fall (September 2009 to April 2010), and it chronicles how outbreak surveillance policies and recommendations for K-12 schools changed over the course of the pandemic.
Both nationally and in Minnesota, K-12 schools received significant attention during the 2009 H1N1 pandemic, as the 2009 H1N1 influenza virus was first confirmed in the United States in school-aged children. On April 21, 2009, the Centers for Disease Control and Prevention (CDC) reported that two cases of febrile respiratory illness—one in a 9-year-old and the other in a 10-year-old in neighboring counties in California—were caused by infection with 2009 H1N1.1 On April 23, the New York City Department of Health and Mental Hygiene was notified of approximately 100 cases of respiratory illness in students at a New York City high school, and by April 24, 222 students had left the school because of illness. Students tested were confirmed to be infected with 2009 H1N1, and the school closed for five days.2,3
Prior to the 2009 H1N1 pandemic, the CDC and state health departments including the Minnesota Department of Health had planned primarily for a pandemic virus that would originate in a location other than North America and that its level of severity would be known before widespread disease occurred in the United States. Plans for schools focused on closure in the case of a severe pandemic and potential closure in the event of a moderate one.4
When 2009 H1N1 emerged in the United States, knowledge about the severity of the strain was limited. News reports from Mexico suggested that illness caused by 2009 H1N1 was moderate to severe. However, the CDC had not yet verified the level of severity. Cases in the United States appeared to be mild, but there were too few from which to draw firm conclusions. Thus, initially across the United States, when a case of 2009 H1N1 was associated with a K-12 school, the school closed.
As more data were collected and it appeared that 2009 H1N1 was similar to seasonal influenza in terms of severity and transmissibility, the Minnesota Department of Health and the CDC changed their recommendation, shifting from school closures to exclusion of students and staff with influenza-like illness coupled with basic infection-prevention measures. This approach was similar to what had been recommended for K-12 schools during a typical influenza season. However, because a 2009 H1N1 vaccine was not available to protect staff and students at high risk for complications from 2009 H1N1, increased school surveillance was emphasized.
Minnesota was one of the first states to adopt the new policy of keeping schools open when cases of 2009 H1N1 were identified among students or staff. After careful review of epidemiologic data, health department officials concluded that the disruption that goes along with closing schools was not warranted, given the mild severity of the influenza strain. Further, officials reasoned that if schools were closed, it was likely that students would congregate in other settings that did not have infection-prevention practices in place.
This article reviews Minnesota’s experience with 2009 H1N1, focusing on surveillance data for school-aged children, the outbreak surveillance system in K-12 schools, and the recommendations for K-12 schools during the spring and fall waves of the pandemic. It also discusses how outbreak surveillance and recommendations for K-12 schools changed over the course of the pandemic.
The Spring Wave (April to August 2009)
■ Surveillance of Hospitalized Cases
Seasonal influenza virus usually affects the very young and the elderly; 2009 H1N1, however, disproportionally affected school-aged children. During the spring pandemic wave, there were 260 laboratory-confirmed 2009 H1N1 hospitalizations in Minnesota (all hospitalized patients with suspected influenza were tested for 2009 H1N1 by the Minnesota Department of Health’s Public Health Laboratory). Eighty-two (32%) of the 260 hospitalizations involved school-aged children. Of these, 58 were elementary school-aged children (5 to 12 years of age) and 24 were high-school-aged children (13 to 17 years). Among all school-aged children, the rate was 9.2 hospitalizations per 100,000 population. The rate among elementary school-aged children was 10.8 per 100,000 population; among high-school-aged children it was 6.7 per 100,000 (Table).
The spring wave primarily affected school-aged children in the metropolitan area, with 68 (83%) of 82 hospitalized school-aged children residing in the seven-county Minneapolis-St. Paul metropolitan area. Fifty-seven (70%) of the 82 school-aged children hospitalized with 2009 H1N1 had at least one underlying medical condition that put them at increased risk for complications from influenza; the most common underlying medical condition was asthma. Eleven (13%) required admission to an intensive care unit. Of those, three also required mechanical ventilation. One school-aged child died before discharge from the hospital.
■ Surveillance in Schools
The Minnesota Department of Health has conducted influenza surveillance in schools since 1988. Prior to the emergence of 2009 H1N1, outbreaks of influenza-like illness were reported by schools when they experienced a doubling of their usual absence rate for any reason between October and April of each year. Schools were then asked to report the primary symptoms of ill children. Schools reported once a season, which was deemed appropriate, given the single peak of seasonal influenza during the school year. Between 1988 and 2009, the number of schools reporting suspected influenza outbreaks ranged from a low of 38 schools in 20 counties in 1996-1997 to a high of 441 schools in 71 counties in 1991-1992.
At the onset of the 2009 H1N1 pandemic, health officials decided that its existing school surveillance plan was not sensitive enough to collect the relevant data on influenza-like illness in schools. In mid-May, daily reporting of the number of students with influenza-like illness from all Minnesota K-12 schools was initiated; this intensive reporting took place through the end of the school year. However, it was quickly realized that this method, although sensitive, was too labor intensive for school health professionals, and the data were difficult to interpret. The Department of Health made plans to re-evaluate influenza-like illness surveillance in schools for the fall.
■ Prevention and Control Recommendations
The CDC published guidelines for schools with probable or confirmed cases when 2009 H1N1 was first identified in the United States. These guidelines recommended school closure for a minimum of seven days. In Minnesota, the first case of 2009 H1N1 was identified on April 28 in an individual associated with Rocori Middle School in Cold Spring. As recommended by the Minnesota Department of Health, administrators from the Rocori district dismissed classes and activities for middle school students for seven school days. A parochial school, St. Boniface School, opted to dismiss classes as well because students shared hallways and a cafeteria with Rocori Middle School.
Additional cases of 2009 H1N1 were quickly identified in people associated with Southwest High School, Kenwood Middle School, and Emerson Elementary School in Minneapolis; Osseo High School; and Hugo Early Childhood Family Education. Initially, these schools dismissed classes as well. On May 4, the Department of Health released new guidelines for schools, recommending that they remain open, screen students and staff for influenza-like illness symptoms, and exclude ill individuals for seven days after the onset of symptoms and 24 hours after acute symptoms resolved (without fever-reducing medication), whichever was longer (unless they were diagnosed with an alternate infection such as streptococcal pharyngitis). As a result, some schools that had initially dismissed students resumed classes.
On May 22, the CDC changed its recommendations as well, calling for exclusion of ill students and staff rather than school closures. The move was similar to the recommendations already in place in Minnesota. The seven-day exclusion period was intended to decrease the risk of disease transmission, which was especially important for individuals at high risk for complications from 2009 H1N1 because vaccine was unavailable at the time. Confirmatory testing for 2009 H1N1 was limited, which meant that exclusion was based on symptoms. In certain circumstances, this created confusion when students had a negative rapid influenza test but met the symptom criteria. Rapid influenza tests were eventually found to have limited diagnostic value.5
The Minnesota Department of Health developed a screening tool that parents and caregivers could use each morning to assess the health status of their children. It prompted parents to look for symptoms of 2009 H1N1 including fever (100.0 degrees F or higher), cough, or sore throat, and then assisted with the decision to keep their child home and notify the school. The screening tool was available in Spanish, Hmong, and Somali as well as English. In addition to excluding symptomatic students, schools were encouraged to promote good hand hygiene and cough etiquette.
Summer Planning
After the spring wave of the pandemic subsided, officials from the CDC, the Minnesota Department of Health, local public health departments, the Minnesota Department of Education, and K-12 schools evaluated the actions taken during the spring pandemic wave. All anticipated that a second wave was likely to occur with the return of students to school in the fall. Planning for a second wave encompassed all areas including vaccine distribution, antiviral distribution, and ways health care facilities could handle a surge of cases. Given the burden of the first pandemic wave on schools, both the CDC and the Minnesota Department of Health also continued to focus on K-12 school planning.
During the summer, a work group made up of school health professionals from around the state as well as state and local public health officials convened to address three goals in preparation for the likelihood of a fall pandemic wave of 2009 H1N1. Those goals were to develop a more sensitive and logistically feasible system for reporting influenza-like illness in schools, to improve communication between public health departments and schools, and to determine recommendations for infection prevention.
They developed a new surveillance protocol by which school health professionals were to report to the Department of Health when the number of students absent or sent home with influenza-like illness reached 5% of total school enrollment or when three or more students from the same classroom were absent or sent home with influenza-like illness on a given day. Schools were also to report each new outbreak that met the reporting criteria.
Communication between public health departments and schools was improved in a number of ways. The most significant new communication vehicle was a website on which Department of Health experts posted information for school health professionals. A listserv was launched to let school officials know when the website had been updated. Department of Health officials had heard from school health professionals that it was important for all school officials to be informed at the same time, so both administrators and school health professionals received the update notifications.
On August 7, the CDC released its recommendations for K-12 schools for the fall. These recommendations included excluding ill students and staff for 24 hours after resolution of fever, if disease characteristics of the second pandemic wave were similar to those of the spring wave. The CDC also recommended that schools have an isolation or sick room for students who became ill at school, that school dismissals take place only if indicated by local conditions, and that schools reinforce the importance of good hand hygiene and respiratory etiquette.
The Minnesota work group strategized about how to implement the national recommendations at the local level. As in the spring, the objective was for schools to close only if they could not continue to function because of excessive absenteeism among students or staff. The work group recommended that schools notify parents/guardians when the influenza-like illness reporting threshold was met in a classroom or school, eliminate the doctor’s note requirement for ill students and athletes to avoid overwhelming health care providers, and promptly identify and exclude ill students and staff. During the 24-hour exclusion period, it was agreed that students and staff should stay home except to seek medical care and not participate in extracurricular activities. Those receiving antiviral treatment were also to abide by the full exclusion period because they could shed 2009 H1N1 during the course of treatment.
The CDC had specified that a different exclusion period might be warranted for students who were medically fragile or pregnant. The Minnesota work group discussed the needs of these special populations and decided that recommendations for schools specifically for medically fragile or pregnant students be developed. A stricter exclusion criteria of seven days after onset of symptoms or 24 hours after resolution of acute symptoms, whichever was longer, was recommended for both staff and students. Also, the families of these students were encouraged to speak to their health care provider to determine a plan in case of illness or exposure.
The Fall Wave (September 2009 to April 2010)
■ Surveillance of Hospitalized Cases
The epidemiologic characteristics of the fall pandemic wave were similar to those of the spring wave. Again, when compared with seasonal influenza, school-aged children were disproportionately affected. There were 1,564 laboratory-confirmed hospitalized cases during the fall pandemic wave, of which 340 (22%) were among school-aged children. Of those, 148 (45%) were reported among elementary-school-aged children (5 to 12 years of age) and 192 (56%) among high-school-aged children (13 to 17 years of age). Among school-aged children, the rate of hospitalization was 37.9 per 100,000 population. The rate among elementary-school-aged children was 47.4 compared with 23.7 hospitalizations per 100,000 among high-school-aged children.
One notable difference between the fall and spring pandemic waves was that greater Minnesota was more affected during the fall wave. Among school-aged children, 181 (53%) of 340 hospitalized cases occurred in the seven-county Minneapolis-St. Paul metropolitan area compared with 83% during the spring pandemic wave. Two hundred (59%) of 340 school-aged children hospitalized with 2009 H1N1 had at least one underlying medical condition that put them at increased risk for complications from influenza; asthma was the most common underlying condition. Forty-eight (14%) hospitalized children were admitted to the intensive care unit, of which, 20 required mechanical ventilation. Three school-aged children died before discharge from the hospital.
■ Surveillance in Schools
The fall pandemic wave started shortly after the 2009-2010 school year began. It encompassed 1,302 schools in 85 counties. Influenza-like illness outbreaks peaked during the week of October 18 to 24, 2009 (the 42nd week of the year), when 288 schools reported outbreaks (Figure). Hospitalizations also peaked that week. During a typical influenza season, outbreaks of influenza-like illness in schools typically peak sometime between late February and the end of March (the 8th through 12th weeks of the year).
■ The Vaccination Plan
The 2009 H1N1 influenza vaccine arrived in Minnesota during the first week of October. Because only a small quantity of vaccine was available, the Department of Health used the recommendations of the CDC’s Advisory Committee on Immunization Practices to allocate vaccine for populations at highest risk for infection or complications of influenza. During the first eight weeks that the vaccine was available, the groups recommended to receive it included pregnant women, household contacts of children younger than 6 months of age, health care workers with direct exposure to infected patients or the virus, children between 6 months and 4 years of age, and children ages 5 years to 8 years of age with underlying risk factors. In December, the recommendations expanded to include all health care workers, young people between the ages of 5 and 24 years and adults younger than 65 years of age with underlying medical conditions.
Because school-aged children were considered a priority group, public health officials worked with medical providers and school staff to ensure vaccine was available to them in a variety of settings. School-aged children in Minnesota were vaccinated in their home medical clinics, at vaccination clinics held at schools, and at mass vaccination clinics in the community. During this period, 902 clinics were held at schools. Ninety-six percent of local health departments reported holding at least one clinic at schools. The largest clinic at a K-12 school vaccinated 2,400 individuals.
Data on 2009 H1N1 vaccination were reported to the Minnesota Immunization Information Connection (MIIC) immunization registry. Twenty-eight percent of children between the ages of 5 and 18 years received at least one dose of 2009 H1N1 vaccine, according to the MIIC. Medical facilities continue to report 2009 H1N1 administration information to the registry, so this percentage may increase slightly.
As of April 2010, Minnesota ranked 14th in the nation regarding the percentage of children 6 months to 17 years of age vaccinated against 2009 H1N1 influenza based on preliminary data from the CDC.6 According to these data, Minnesota vaccinated 44% of children 6 months to 17 years of age, compared with 36% in the region and 37% nationally.6 These data were collected between November 2009 and February 2010 using the Behavioral Risk Factor Surveillance System and the National 2009 H1N1 Flu Survey. For the fall of 2010, the CDC and the Minnesota Department of Health recommend that everyone 6 months of age and older, regardless of disease or vaccine history, receive the seasonal influenza vaccine, which will include the 2009 H1N1 strain in addition to H3N2 influenza A and influenza B.
Conclusion
Because they are densely populated environments, and because children can shed influenza virus for longer periods than adults and tend to be the ones to introduce influenza into their households,7 schools are important sites for reducing the transmission of emerging infections. The 2009 H1N1 pandemic challenged the Minnesota Department of Health planning assumptions for K-12 schools. The plan was to tie K-12 school recommendations to pandemic severity and to recommend school closure in the event of a severe pandemic and potential closure during a moderate one. However, knowledge about the severity of illness caused by 2009 H1N1 was initially very limited and school closures were recommended when severity was unclear. As data showed 2009 H1N1 was similar to that of seasonal influenza, the recommendation for K-12 schools shifted from school closure to a seven-day exclusion of students and staff members after symptom onset to 24 hours of exclusion after resolution of fever.
The 2009 H1N1 pandemic experience led us to recognize that we need to better plan for different scenarios. Planners need to consider what to do during outbreaks of mild, moderate, and severe illness as well as what to do when disease severity is unknown. And planners should consider a scenario in which a novel virus is first identified in the United States. Throughout the 2009 H1N1 pandemic, the Minnesota Department of Health strengthened its working relationships with K-12 schools in the state. These relationships will be valuable in future efforts to protect school-aged children from emerging diseases. MM
Kathryn Como-Sabetti is a senior epidemiologist; Franci Livingston is an assistant section manager; Pamala Gahr is a senior epidemiologist; Kayla Nagle is a project analyst; Karen Martin is a senior epidemiologist; Craig Morin is a senior epidemiologist; and Elizabeth Parilla is an epidemiologist. All are at the Minnesota Department of Health.
We would like to thank all the school health professionals who worked tirelessly during the 2009 H1N1 pandemic and who kept us informed about influenza activity in their schools. We also thank the following local public health and school health professionals who participated in the summer planning work group: Louise Anderson, Mary Carter, Kim Craven, Nancy Haugen, Marie Hauser, Mary Heiman, Deb Hermann, Cindy Hiltz, Carol Hooker, Ann Hoxie, Kathy Hughes, Sharon Lynch, Cheryl Malecha, Gretchen Musicant, Jane Schleisman, Cyndy Silkworth, Carmen Teskey, and Denise Tracy.
References
1. Centers for Disease Control and Prevention. Swine influenza A (H1N1) infection in two children—Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep. 2009;58(15):400-2.
2. Centers for Disease Control and Prevention. Swine-origin influenza A (H1N1) virus infections in a school—New York City, April 2009. MMWR Morb Mortal Wkly Rep. 2009;58(17);470-2.
3. New York City Department of Health and Mental Hygiene. Press Release: Testing Confirms Swine Influenza at St. Francis Preparatory School in Queens. April 26, 2009.
4. Centers for Disease Control and Prevention. Interim Pre-pandemic Planning Guidance: Community Strategy for Pandemic Influenza Mitigation in the United States. February 2007.
5. Centers for Disease Control and Prevention. Evaluation of rapid influenza diagnostic tests for the detection of novel influenza A (H1N1) virus—United States, 2009. MMWR Morbid Mortal Wkly Rep. 2009;58(30):826-9.
6. Centers for Disease Control and Prevention. Interim results: state-specific influenza A (H1N1) 2009 monovalent vaccination coverage—United States, October 2009-January 2010. MMWR Morb Mortal Wkly Rep. 2010;59(12):363-8.
7. Longini IM, Koopman JS, Monto AS, Fox JP. Estimating household and community transmission parameters for influenza. Am J Epidemiol. 1982;115:736-51.