Cover Story - July 2009
Tex Med. 2009;105(7):21-26.
By John T. Carlo, MD, MSE, and Wendy Chung, MD, MSPH
Dr. Carlo is the medical director/health authority and Dr. Chung is the chief epidemiologist for Dallas County Health and Human Services.
Pandemics* of influenza disease have occurred throughout human history. Most notable is the 1918 Spanish influenza pandemic in which more than 50 million people died (including more than 500,000 Americans). Estimates show that a third of the population became ill during the 1918-19 pandemic, and the case fatality rate was 2.4%. 1 While the attack rate and virus infectivity were similar to those of other influenza virus strains, the 1918 pandemic virus was unique in that an exceptionally high case fatality ratio was observed in young adults. 2 Federal, state, and local pandemic response planning since 2006 has been directed toward responding to a hypothetical epidemic similar in scope to that observed in 1918. 3
One of the most important considerations for local and state health officials is to determine when to close schools as a control measure during a pandemic of influenza. Most federal, state, and local response plans describe the use of school closures or "snow days" as a control measure, but lack a consensus as to when such measures should be enacted. Better understanding of an effective "trigger point" for school closures during outbreaks would help communities better prepare and coordinate implementation of these measures.
In February 2007, the Centers for Disease Control and Prevention (CDC) published pre-pandemic mitigation guidelines that included school closures as an important social-distancing strategy. In the proposed pandemic mitigation framework, school closures should be initiated early, before the explosive growth of an epidemic with high case fatality ratios. 4 The strength of recommendations for closing schools is presented in the context of assessments of pandemic severity according to a pandemic severity index scale. Without quantitative trigger points such as student case counts and absentee or illness rates, local health officials will likely interpret differently the appropriateness of school closures. Most pandemic plans do not establish a quantitative threshold prompting school closures. 5
This article highlights issues surrounding school closures as a community mitigation measure during a pandemic of influenza. We review the available literature, discuss the rationale for school closure in the context of a pandemic, present the indicators that prompted school closures in Dallas County during the recent 2008-09 influenza seasons, and propose a framework for making decisions about school closures during future influenza epidemics.
Effect of School Closures During Past Pandemics and Influenza Outbreaks
During the1918 pandemic, various cities closed schools in the United States as control measures. However, a survey of cities by the U.S. Public Health Service (USPHS) during 1919-21 failed to demonstrate any differences in illness rates between cities that closed schools and those whose schools remained open. Some studies, particularly reviews of case rates in urban areas such as Chicago, found more cases developed among students after a holiday than when schools were in session. 6 Supportive data for most population-based control measures are lacking; available data consists primarily of historical and contemporary observations, rather than controlled scientific studies. 7
Markel and others 8 recently conducted an extensive archival review of mitigation strategies used by 43 cities in the United States during 1918-19. Their findings demonstrate a strong association between early, sustained, and layered application of control measures and a reduced mortality. The findings identified significant variations in the magnitude of excess mortality, ranging from 15 to 249 per 100,000 persons by city. Cities that enacted isolation or quarantine, school closure, and/or bans on mass gatherings demonstrated statistically lower mortality rates. Cities that enacted the control measures early reported the lowest mortality rates. However, the timing of enacting control measures was uniquely associated with a reduced mortality. The combination and choice of intervention appeared to be as critical as the timing of mitigation. 8
As mentioned, in contrast to Markel's findings, other historical studies failed to demonstrate a significant impact using school closures in 1918. 9 In summary, a number of retrospective reviews on the effect of school closure and other community mitigation measures have been published; however, the data remain inconclusive as to whether benefits in the reduction of disease transmission were seen with such measures during the 1918-19 pandemic.
Two influenza pandemics have occurred since 1918. The 1957 pandemic originated in Asia and was designated as an H2N2 virus. This virus was first identified in the United States on both coasts in June 1957. The virus became a full epidemic in the fall after schools convened. The first peak of excess deaths occurred in late October 1957, which was followed by a second peak in February 1958. The overall mortality rate of the 1957 pandemic was one-tenth of that of the 1918 pandemic, with an estimated 115,700 excess deaths observed in the United States. 10
Vynnycky and Edmunds 11 analyzed through a simulation model the impact of school closures during the 1957 pandemic. Using a relatively small R 0 (~1.8), the authors found that contact patterns among individuals outside of the school setting heavily influenced the reduction in epidemic size when schools were closed. They estimated a 12.5% to 14% reduction in epidemic size when schools were closed in the United Kingdom in 1957.
The 1968 pandemic was thought to have originated near Hong Kong. This was an H3N2 virus - a "hybrid" virus thought to have occurred as a result of a new hemagglutinin (H3) surface protein mixing with the currently circulating influenza virus neuraminidase (N2) protein. Excess mortality peaked in December 1968. The estimated mortality (50,000 to 55,000 deaths in the United States) was half of that observed during the 1957 pandemic. 12
Little published data exist on school closures during the 1968 pandemic, though the Dallas Morning News reported that the Everman School District (Fort Worth) was closed in December 1967 because of excessive absences from influenza infections. 13
Since 1967, individual schools have closed because of excessive absences during peak seasonal influenza epidemics. Such school closures may have been completed upon consultation with local health officials. School dismissals typically are completed when peak absences range from 10% to 30%. 5 In such instances, the reasons for closure are centered around the difficulties with classroom staffing, organization, and the volume of make-up assignments required, which primarily prompt temporary school dismissals.
Few recent studies have addressed the effect of school closure on a reduced incidence of influenza illness. Heymann and others 14 completed a retrospective review in Israel during an organized teachers strike. Because Israel has a universal health care system, Heymann and the coauthors were able to review the records of more than 180,000 health care visits of children. Dividing the visits into periods before, during, and after the school strike (which lasted 13 days in January), they observed a significant reduction in the rate of diagnoses of respiratory illness during the school closure period (RR= 0.76; 95% CI, 0.75-0.77). They also noted a reduction in emergency department visits during the closure period (28% reduction; 95% CI, 11%-46%). However, this study was not able to collect information on laboratory diagnosis and was not able to allow for temporal changes in case frequencies normally observed during influenza epidemics. 14
Cauchemez and others 15 found in France that during school holidays, a 10% to 20% reduction was seen in the rate of influenza transmission in children, with no detectable effect on adults. Through a model, the authors predicted that school closure during a pandemic could reduce the cumulative number of cases by 13% to 17% in children, but the impact may be difficult to maintain if contact among children occurs to a high degree in other environments when the schools are closed.
Cowling and others 16 evaluated influenza surveillance data before, during, and after the closing of all kindergarten and primary schools in Hong Kong. The two-week closure began after reports of three pediatric deaths in March 2008. Surveillance data indicated that the intervention did not substantially influence the disease transmission rate, as the influenza season had already peaked by March 2008.
Population models have been used to help guide decisions regarding school closures. These models' assumptions often heavily influenced the resulting outcomes. Important primary assumptions include the attack rates (age specific), the degree of transmissibility including asymptomatic transmission, and the degree of social mixing outside of the school setting (once schools are closed). Modeling conclusions are mixed, with effects of school closures ranging from no effect to a 55% reduction in epidemic severity. Most models find a modest benefit in terms of case rate reduction in the range of 17% to 20%, especially if contact rates among children are limited during school closure. 11,15,17-21
Influenza Transmission by School-Age Children
Increased attack rates for school-age children were observed during the 1918 pandemic. The USPHS city surveys demonstrated that from 1900 to 1917, the group aged 5 to 15 years accounted for 11% of total influenza cases, while in 1918 the attack rate in that age group increased to 25% of the cases. 22 Other historical reports have shown some cities to have attack rates for school-age children as high as 33% to 70%. 23 Attack rates were similarly disproportionately higher in school-age children in 1957. 10
A recent study estimated that during the influenza season, nearly 75% of childhood influenza cases were infected by other children while in school, and 35% of all adult illnesses were thought to have been transmitted to them by school-age children. 24 Typically, school-age children have higher attack rates of seasonal influenza than the general population and are thought to be more susceptible due to lower preexisting immunity. Children are also less likely to be skilled in handling their respiratory secretions. Adults in households with school-age children exhibit attack rates two to three times higher than adults who do not live in houses where school-age children reside. 25 Studies have also shown that children often introduce influenza illness to members of their households. 19
Children are infectious for longer periods when compared with adults, with a duration of viral shedding of 7 to 10 days. 26 Younger children tend to shed greater quantities of influenza virus than do older children. 27 They have also been shown through household attack models to transmit influenza more frequently than adults. 28 Asymptomatic spread of influenza also is more common in children, with some studies demonstrating viral transmission several days before the onset of symptoms, particularly in younger children. 29
Biological, social, and maturational factors make children important transmitters of influenza. In addition, classroom settings are the highest social density settings in our communities, with densities ranging from 35 to 64 square feet per person. 4 Office settings, hospitals, and homes have much less dense environments.
Authority to Close Schoolsin Texas
The responsibility for opening and closing schools in Texas remains with the schools and independent school districts themselves. In Texas, the Texas Department of State Health Services (DSHS) or local health authority has the legal authority under the Texas Health and Safety Code Chapter 81.084 to apply control measures of quarantine to property. 30 The statute specifies that if there is reasonable cause to believe that property in the jurisdiction is or may be infected or contaminated with a communicable disease, then the property may be quarantined. The section also specifies additional language broadening the ability to impose control measures during a public health disaster. Such action requires a formal delivery of a written medical order to the property owner in question. However, this control measure is rarely used and likely could be subject to an appeal process through the court system. Locally, most court systems in Texas are generally unfamiliar with this portion of the statute, and there likely would be considerable variation in interpretation of this law if officials attempted to use it to mandate school closure.
Ultimate authority for school dismissal in Texas rests with the senior elected official of an affected jurisdiction if a disaster is declared. During times of disasters, the governor has broad powers to ensure the safety of citizens. The Texas Government Code, Section 418.018, Movement of People, establishes the authority of evacuations and egress orders under the governor with a formal order or declaration. This authority appears to be transmitted to the county judge or mayor of a municipality under Section 418.108, Declaration of Local Disaster. 31
Impact of School Closures on the Community
Closing large numbers of public schools even briefly would likely substantially impact the entire community. A recent review found that an estimated 16% of the workers in the United Kingdom would need to miss work because they are the primary caregivers of a dependent child. The estimated costs of productivity loss ranged from £222 million to £254 million per week in the United Kingdom. 32
Many children, particularly in urban settings, receive important services through their schools, such as those of federally assisted school breakfast and lunch programs. In 2007, the National School Lunch Program provided low-cost or free lunches to more than 30.5 million children. 33 In the largest three school districts in Dallas County, 62% to 84% of the more than 205,000 students enrolled are considered economically disadvantaged and receive low-cost or free lunches in schools. 34 Without such services, lower-income families could suffer a significant burden when schools are closed.
Although closing an individual school could slow the spread of illness within a student population, the closure would not protect students from exposure to influenza in other settings. A recent survey of parents in North Carolina found that during a countywide school closure due to influenza, almost all children visited public places despite public health recommendations not to do so. 35 School closures alone likely would not be effective in mitigating disease transmission on a community level, unless closures are accompanied by concomitant restrictions of public gatherings and congregations. Public venues such as malls, movie theaters, and retail stores would therefore also need to be closed during the same time. Closure and cancellation of such venues, as well as the loss of caretakers from the workforce, could overwhelmingly impact the economy.
As student safety remains a primary consideration, we must recognize that in some situations, a child's school may be a safer environment than his or her home. Students in larger households may have similar risk of illness compared with that of a classroom setting. Additionally, school-based surveillance of illness activity in school-age children cannot be conducted during school closures, reducing the surveillance capability for estimating illness rates in the community. Finally, school health services often are an important provider of initial health care assessments to children in many communities; school closure would remove access to this service.
Recent Experience With School Closures, Dallas County, 2008-09
A novel H1N1 strain of swine origin emerged from Mexico in March 2009. 36 An early modeling study by Fraser and others indicates that the new H1N1 virus was readily transmissible from person to person early in the virus evoluation. 37 To date, the severity of symptoms in infected persons has appeared to be similar to that seen in typical influenza seasons. 36
On April 27, 2009, after the Secretary of the Department of Homeland Security Janet Napolitano declared a public health emergency, the CDC recommended the consideration of dismissing students from schools with a confirmed or suspected case of novel H1N1 influenza infection. Broader school dismissal recommendations also were to be considered by local health authorities, depending on the extent of influenza-like illness in the community. 38 Schools were recommended to remain closed for 14 days. As of May 18, 2009, the Texas Education Agency listed 858 closed school campuses, with an estimated 504,696 students affected by school dismissals from April 27, 2009, to May 26, 2009. 34
During the novel H1N1 influenza outbreak of 2009, local and state officials tracked several key data elements to determine when to close schools in Texas. In Dallas County, area school districts were asked to change from a weekly absence-reporting surveillance program to tracking absences daily. Weekly absence reporting has been a component of the seasonal influenza surveillance program since 2003. School nurses were asked to verify a student's absence to determine if it was likely due to an influenza-like illness (ILI). Daily absence reports, including ILI reports, were collected from each of the 14 independent school districts in Dallas County with nearly 100% compliance. Reports of confirmed and probable cases were communicated to each school nurse director and superintendent when available.
In addition to school absence-rate-tracking and ILI reporting, Dallas County health officials assessed influenza severity through hospital surveillance reporting. Emergency department visit volume was collected daily by using the Dallas/Fort Worth Syndromic Surveillance System, and hospital admissions were reported by area hospital infection preventionists. Local hospital data, along with reports from DSHS, other local and state health departments, and CDC, helped determine that the early epidemic did not appear to have an increased severity above what was seen during typical influenza seasons. During the epidemic, many local departments in the United States kept up-to-date Web sites with key surveillance information.
From April 28 to May 5,2009, during the H1N1 outbreak in Dallas County, four public elementary schools were closed, and 2,104 public school students were out of school because of the closures. The duration of school closure ranged from four to eight school days. Three of the four schools were closed under advisory of the Dallas County Health Authority, and one school was closed under the recommendation of the City Health Authority.
From April 23 to May 5, 2009, 81 children in 35 different schools were reported to have confirmed or probable novel H1N1 infections in Dallas County.
In addition to the presence of confirmed or probable cases, a careful review of the trends in student illness and absentee rates affected the decisions regarding the four school closures. This assessment provided indicators as to whether the transmission of influenza was increasing, which could be curtailed through a school closure. As observed, rates of absences from influenza-like illnesses were reduced in all four schools following reopening.
Schools remain the single most important communal setting for children aged 5 to 17. Because those in this age group are described as being the sentinel spreaders of seasonal influenza, targeting this population for control measures could potentially have the largest effect in reducing early disease transmission. However, given the observed rate of asymptomatic transmission and the many other social-mixing venues in our communities, school closures alone are not expected to completely extinguish or contain an influenza epidemic in the community. The apparent effectiveness of school closures may be related to levels of adherence to additional recommendations for these students to avoid public gatherings during this time. Given the societal costs of large-scale school closures, it is valuable to study whether similar levels of illness reduction can be achieved through alternate control measures, such as strict reinforcement of illness policies and intensified prevention education of students and families.
In the setting of an influenza epidemic (pandemic or seasonal), school officials should consult with local health officials for guidance and determination of school closures. Local health officials should consider the severity of the epidemic by reviewing local, state, national, and international data from early cases. The simple presence of laboratory-confirmed or probable cases may not accurately reflect the level of influenza activity within a school. Further, laboratory-based case identification likely is heavily influenced by access to medical care for diagnostic testing. Thus, schools with large proportions of economically disadvantaged students may not demonstrate numbers of laboratory-confirmed cases, even if significant levels of influenza activity are present in those schools.
With the available information regarding disease severity, local health officials should establish a threshold for absentee rates that would prompt strong consideration for closure and evaluate both the trends in overall absence rates per school and the absence rates due to influenza-like illness. Comparisons of absence rates should be made among the schools to identify potentially more intense foci of transmission. To establish a uniform school closure policy, local and state health officials should collectively determine an absence threshold to warrant school closings. Having different standards for this threshold of closure, as observed, results in confusion by the public and can result in a lack of coordinated response by local health officials.
Communitywide school dismissals or entire district closures should be completed in conjunction with a ban on other mass gatherings and events in the area, if the goal of this measure is to reduce influenza illness rates in the community. Such actions should be completed only if there is an imminent danger that expected hospitalized patient volume is going to overwhelm area hospitals. Such actions are likely to have a significant impact on local communities, and, as such, should be completed under a public health disaster declaration. Under such a declaration, the senior elected official should at minimum concur publicly with the local health official's decision. Inherent in this decision should be that individuals and businesses existing under such a condition may be eligible for disaster assistance funding through local, state, or federal assistance funding.
Every school's pandemic and seasonal influenza planning and response efforts should include the capability to report daily absence rates, including ILI absence rates, to local health officials. Funding to develop this surveillance capability should be available to independent school districts. Establishing this type of surveillance routinely and broadly in our schools would provide an important and consistent measure for monitoring influenza activity in our school-age populations.
The ability to provide effective interventions and disease control measures in this age group could substantially impact the direction of an epidemic in the community.
*The term pandemic is used to describe a disease that is spread across the entire planet. An influenza pandemic has additional implied meanings that the virus has spread across multiple continents within the same time period, and the severity of illness is a degree higher than seasonal influenza epidemics. This excess mortality was first described as an important hallmark of pandemic influenza by William Farr in 1847.
- Morens DM, Fauci AS. The 1918 influenza pandemic: insights for the 21st century. J Infect Dis . 2007;195(7):1018-1028.
- Mills CE, Robins JM, Lipsitch M. Transmissibility of 1918 pandemic influenza. Nature . 2004;432(7019):904-906.
- The Homeland Security Council. National strategy for pandemic influenza. November 2005. http://www.pandemicflu.gov/plan/federal/pandemic-influenza.pdf .
- The Centers for Disease Control and Prevention. Interim pre-pandemic planning guidance: community strategy for pandemic influenza mitigation in the United States. February 2007. http://www.pandemicflu.gov/plan/community/community_mitigation.pdf .
- Kahn LH. Pandemic influenza school closure policies [comment]. Emerg Infect Dis . 2007;13(2):344-345.
- Bell DM; World Health Organization Writing Group. Non-pharmaceutical interventions for pandemic influenza, national and community measures. Emerg Infect Dis . 2006;12(1):88-94.
- Taubenberger JK. The origin and virulence of the 1918 "Spanish" influenza virus. Proc Am Philos Soc . 2006;150(1):86-112.
- Markel H, Lipman HB, Navarro JA, et al. Nonpharmaceutical interventions implemented by US cities during the 1918-1919 influenza pandemic. JAMA . 2007;298(6):644-654.
- Bootsma MC, Ferguson NM. The effect of public health measures on the 1918 influenza pandemic in US cities. Proc Nat Acad Sci U S A . 2007;104(18):7588-7593.
- Glezen PW. Emerging infections: pandemic influenza. Epidemiol Rev . 1996;18(1):64-76.
- Vynnycky E, Edmunds WJ. Analysis of the 1957 (Asian) influenza pandemic in the United Kingdom and the impact of school closures. Epidemiol Infect . 2008;136(2):166-179.
- Choi K, Thacker SB. Mortality during influenza epidemics in the United States, 1967-1978. Am J Public Health . 1982;72(11):1280-1283.
- Fort Worth Bureau of the News. Wave of flu shuts school at Everman. The Dallas Morning News. December 20, 1967.
- Heymann A, Chodick G, Reichman B, Kokia E, Laufer J. Influence of school closure on the incidence of viral respiratory diseases among children and on health care utilization. Pediatr Infect Dis J . 2004;23(7):675-677.
- Cauchemez S, Valleron AJ, Boëlle PY, Flahault A, Ferguson NM. Estimating the impact of school closure on influenza transmission from sentinel data. Nature . 2008;452(7188):750-754.
- Cowling BJ, Lau EH, Lam CL, et al. Effects of school closures, 2008 winter influenza season, Hong Kong. Emerg Infect Dis . 2008;14(10):1660-1662.
- Ferguson NM, Cummings DA, Fraser C, Cajka JC, Cooley PC, Burke DS. Strategies for mitigating an influenza pandemic. Nature . 2006;442(7101):448-452.
- Germann TC, Kadau K, Longini IM Jr, Macken CA. Mitigation strategies for pandemic influenza in the United States. Proc Natl Acad Sci U S A . 2006;103(15):5935-5940.
- Longini IM Jr, Koopman JS, Monto AS, Fox JP. Estimating household and community transmission parameters for influenza. Am J Epidemiol . 1982;115(5):736-751.
- Milne GJ, Kelso JK, Kelly HA, Huband ST, McVernon J. A small community model for the transmission of infectious diseases: comparison of school closure as an intervention in individual-based models of an influenza pandemic. PLoS ONE . 2008;3(12):e4005.
- Yasuda H, Yoshizawa N, Kimura M, et al. Preparedness for the spread of influenza: prohibition of traffic, school closure, and vaccination of children in the commuter towns of Tokyo. J Urban Health . 2008;85(4):619-635.
- Jordan EO. Epidemic Influenza: A Survey . Chicago, IL: American Medical Association; 1927.
- Neuzil KM, Hohlbein C, Zhu Y. Illness among schoolchildren during influenza season: effect on school absenteeism, parental absenteeism from work, and secondary illness in families. Arch Pediatr Adolesc Med . 2002;156:986-991.
- Local mitigation strategies for pandemic influenza. Albuquerque, NM: National Infrastructure Simulation & Analysis Center, Sandia National Laboratories; December 2005. SAND No. 2005-7955J. http://www.sandia.gov/nisac/docs/NISAC_FluMitigationPaperWithFullSOMTables.doc .
- Woodall J, Rowson KE, McDonald JC. Age and Asian influenza, 1957. Br Med J . 1958;2(5108):1316-1318.
- Long CE, Hall CB, Cunningham CK, et al. Influenza surveillance in community-dwelling elderly compared with children. Arch Fam Med . 1997;6(5):459-465.
- Hall CB, Douglas RG Jr, Geiman JM, Meagher MP. Viral shedding patterns of children with influenza B infection. J Infect Dis . 1979;140(4):610-613.
- Cauchemez S, Carrat F, Viboud C, Valleron AJ, Boëlle PY. A Bayesian MCMC approach to study transmission of influenza: application to household longitudinal data. Stat Med . 2004;23(22):3469-3487.
- Advisory Committee on Immunization Practices, Smith NM, Bresee JS, Shay DK, Uyeki TM, Cox NJ, Strikas RA. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep . 2006;55(RR-10):1-42.
- Vernon's Texas Codes Annotated. Health and Safety Code; Section 81.084: Application of Control Measures to Property. Last amended September 2003. http://tlo2.tlc.state.tx.us/statutes/hs.toc.htm .
- Texas Statutes: Government Code, Chapter 418: Emergency Management. http://tlo2.tlc.state.tx.us/statutes/gv.toc.htm .
- Sadique MZ, Adams EJ, Edmunds WJ. Estimating the costs of school closure for mitigating an influenza pandemic. BMC Public Health . 2008;8:135.
- The National School Lunch Program. US Department of Agriculture, Food and Nutrition Service. http://www.fns.usda.gov/cnd/Lunch/ . Accessed May 18, 2009.
- Texas Education Agency. H1N1 flu related information: known school closings. http://ritter.tea.state.tx.us/swineflu/schclosings.html . Accessed May 18, 2009.
- Johnson AJ, Moore ZS, Edelson PJ, et al. Household responses to school closure resulting from outbreak of influenza B, North Carolina. Emerg Infect Dis . 2008;14(7):1024-1030.
- Novel Swine-Origin Influenza (H1N1) Virus Investigation Team. Emergence of a novel swine-origin influenza A (H1N1) virus in humans [Epub ahead of print]. N Engl J Med. 2009;May 7. NEJMoa0903810.
- Fraser C, Donnelly CA, Cauchemez S, et al. Pandemic potential of a strain of influenza A (H1N1): early findings [Epub ahead of print]. Science . 2009;May 14.
- Centers for Disease Control and Prevention. CDC health update: swine influenza A (H1N1) update: interim CDC guidance for nonpharmaceutical community mitigation in response to human infections with swine influenza (H1N1) virus . http://www.cdc.gov/h1n1flu/HAN/042709.htm . Posted April 27, 2009.
Cover Story: Swing Flu - Rehearsal for Disaster?
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