DRO, RTH, and FM conceived of the study. DRO, RTH, DW, and FM designed the study. DRO, KK, and FM analyzed the data. All authors contributed to writing the paper. DRO, RTH, MP, and KK collected data or performed experiments for this study. DRO, RTH, MP, and KK participated in the rotation of analysts who clean, analyze, and report data daily. RTH oversaw the syndromic surveillance unit that collected the data.
The authors have declared that no competing interests exist.
The importance of understanding age when estimating the impact of influenza on hospitalizations and deaths has been well described, yet existing surveillance systems have not made adequate use of age-specific data. Monitoring influenza-related morbidity using electronic health data may provide timely and detailed insight into the age-specific course, impact and epidemiology of seasonal drift and reassortment epidemic viruses. The purpose of this study was to evaluate the use of emergency department (ED) chief complaint data for measuring influenza-attributable morbidity by age and by predominant circulating virus.
We analyzed electronically reported ED fever and respiratory chief complaint and viral surveillance data in New York City (NYC) during the 2001–2002 through 2005–2006 influenza seasons, and inferred dominant circulating viruses from national surveillance reports. We estimated influenza-attributable impact as observed visits in excess of a model-predicted baseline during influenza periods, and epidemic timing by threshold and cross correlation. We found excess fever and respiratory ED visits occurred predominantly among school-aged children (8.5 excess ED visits per 1,000 children aged 5–17 y) with little or no impact on adults during the early-2002 B/Victoria-lineage epidemic; increased fever and respiratory ED visits among children younger than 5 y during respiratory syncytial virus-predominant periods preceding epidemic influenza; and excess ED visits across all ages during the 2003–2004 (9.2 excess visits per 1,000 population) and 2004–2005 (5.2 excess visits per 1,000 population) A/H3N2 Fujian-lineage epidemics, with the relative impact shifted within and between seasons from younger to older ages. During each influenza epidemic period in the study, ED visits were increased among school-aged children, and each epidemic peaked among school-aged children before other impacted age groups.
Influenza-related morbidity in NYC was highly age- and strain-specific. The impact of reemerging B/Victoria-lineage influenza was focused primarily on school-aged children born since the virus was last widespread in the US, while epidemic A/Fujian-lineage influenza affected all age groups, consistent with a novel antigenic variant. The correspondence between predominant circulating viruses and excess ED visits, hospitalizations, and deaths shows that excess fever and respiratory ED visits provide a reliable surrogate measure of incident influenza-attributable morbidity. The highly age-specific impact of influenza by subtype and strain suggests that greater age detail be incorporated into ongoing surveillance. Influenza morbidity surveillance using electronic data currently available in many jurisdictions can provide timely and representative information about the age-specific epidemiology of circulating influenza viruses.
Don Olson and colleagues report that influenza-related morbidity in NYC from 2001 to 2006 was highly age- and strain-specific and conclude that surveillance using electronic data can provide timely and representative information about the epidemiology of circulating influenza viruses.
Seasonal outbreaks (epidemics) of influenza (a viral infection of the nose, throat, and airways) send millions of people to their beds every winter. Most recover quickly, but flu epidemics often disrupt daily life and can cause many deaths. Seasonal epidemics occur because influenza viruses continually make small changes to the viral proteins (antigens) that the human immune system recognizes. Consequently, an immune response that combats influenza one year may provide partial or no protection the following year. Occasionally, an influenza virus with large antigenic changes emerges that triggers an influenza pandemic, or global epidemic. To help prepare for both seasonal epidemics and pandemics, public-health officials monitor influenza-related illness and death, investigate unusual outbreaks of respiratory diseases, and characterize circulating strains of the influenza virus. While traditional influenza-related illness surveillance systems rely on relatively slow voluntary clinician reporting of cases with influenza-like illness symptoms, some jurisdictions have also started to use “syndromic” surveillance systems. These use electronic health-related data rather than clinical impression to track illness in the community. For example, increased visits to emergency departments for fever or respiratory (breathing) problems can provide an early warning of an influenza outbreak.
Rapid illness surveillance systems have been shown to detect flu outbreaks earlier than is possible through monitoring deaths from pneumonia or influenza. Increases in visits to emergency departments by children for fever or respiratory problems can provide an even earlier indicator. Researchers have not previously examined in detail how fever and respiratory problems by age group correlate with the predominant circulating respiratory viruses. Knowing details like this would help public-health officials detect and respond to influenza epidemics and pandemics. In this study, the researchers have used data collected between 2001 and 2006 in New York City emergency departments to investigate these aspects of syndromic surveillance for influenza.
The researchers analyzed emergency department visits categorized broadly into a fever and respiratory syndrome (which provides an estimate of the total visits attributable to influenza) or more narrowly into an influenza-like illness syndrome (which specifically indicates fever with cough and/or sore throat) with laboratory-confirmed influenza surveillance data. They found that emergency department visits were highest during peak influenza periods, and that the affect on different age groups varied depending on the predominant circulating viruses. In early 2002, an epidemic reemergence of B/Victoria-lineage influenza viruses caused increased visits among school-aged children, while adult visits did not increase. By contrast, during the 2003–2004 season, when the predominant virus was an A/H3N2 Fujian-lineage influenza virus, excess visits occurred in all age groups, though the relative increase was greatest and earliest among school-aged children. During periods of documented respiratory syncytial virus (RSV) circulation, increases in fever and respiratory emergency department visits occurred in children under five years of age regardless of influenza circulation. Finally, the researchers found that excess visits to emergency departments for fever and respiratory symptoms preceded deaths from pneumonia or influenza by about two weeks.
These findings indicate that excess emergency department visits for fever and respiratory symptoms can provide a reliable and timely surrogate measure of illness due to influenza. They also provide new insights into how different influenza viruses affect people of different ages and how the timing and progression of each influenza season differs. These results, based on data collected over only five years in one city, might not be generalizable to other settings or years, warn the researchers. However, the present results strongly suggest that the routine monitoring of influenza might be improved by using electronic health-related data, such as emergency department visit data, and by examining it specifically by age group. Furthermore, by showing that school-aged children can be the first people to be affected by seasonal influenza, these results highlight the important role this age group plays in community-wide transmission of influenza, an observation that could influence the implementation of public-health strategies such as vaccination that aim to protect communities during influenza epidemics and pandemics.
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Throughout the twentieth century, epidemic and pandemic influenza was responsible for causing widespread illness, economic disruption, and considerable loss of life worldwide [
Influenza surveillance currently conducted in the United States encompasses systems for monitoring influenza-related illness and death, investigating unusual respiratory disease outbreaks, and identifying and characterizing viral influenza strains [
In recent years, New York City (NYC) and other jurisdictions have tracked influenza using syndromic surveillance systems such as those based on electronically reported emergency department (ED) patient chief complaints [
Epidemiologic community and family studies [
The purpose of this study was to evaluate the use of ED visit data for monitoring the age-specific timing and impact of epidemic influenza by predominant circulating viral type, subtype, and antigenic strain. Using a broad definition of ED visits classified as fever or respiratory syndrome chief complaints, we applied a statistical method, routinely used for monitoring clinical ILI [
Electronic reporting of ED chief complaint data from NYC hospitals occurred daily during the study period from mid-November 2001 through June 2006. Data received each morning were typically >90% complete for the preceding day, and data received Monday mornings >95% complete for the preceding week. During the 2001–2002 season participating hospital EDs captured an estimated 65% of all ED visits citywide. Coverage gradually increased through the study period, reaching 79% of all ED visits citywide during 2002–2003, 88% during 2003–2004 and 90% during 2004–2005 and 2005–2006. Individual ED visit data were aggregated by age group, chief complaint syndrome group, and week ending Saturday.
Of the 13.3 million ED visits reported by participating NYC facilities during the study period, 2.3 million were categorized into a broad “fever and respiratory” syndrome composed of the hierarchical and mutually exclusive syndromes “respiratory,” “fever/flu,” “common cold,” and “sepsis,” as previously described [
The broad “fever and respiratory” syndrome category described above was used to provide the most sensitive measure of ED visits potentially attributable to influenza. We also created a specific “ILI” syndrome following the commonly used clinical surveillance definition of fever with cough and/or sore throat: Of the 2.3 million visits categorized into the broad fever and respiratory syndrome, 260,000 visits were categorized as ILI, defined as a chief complaint composed of an influenza keyword or of a fever-related key word with a mention of “cough” and/or “sore throat.” The broad fever and respiratory and the narrow ILI syndrome data are shown in
Dates are CDC year and week ending Saturday. Top graph, isolates by influenza type are from WHO collaborating laboratories, with subtype and strain designation based on predominant regional and national antigenic lineage: A/H3-SY, predominant circulating A(H3N2) Sydney-lineage viruses; B/VI, predominant circulating B/Victoria-lineage; A/H1, either A(H1N1) New Caledonia- or A(H1N2) Wisconsin-lineage; A/H3-FU, A(H3N2) Fujian-lineage; B/YA, B/Yamagata-lineage; and A/H3-CA, A(H3N2) California-lineage. Middle and bottom graphs, observed fever and respiratory syndrome (middle) and ILI syndrome (bottom) ED visits are shown as black lines, and seasonally expected Serfling baseline visits as red lines. Dashed lines represent epidemic thresholds as model estimates plus two standard deviations. Shaded areas represent estimated influenza-attributable excess ED visits: blue areas correspond to periods of increasing and dominant influenza A circulation and red areas to influenza B. Vertical lines indicate the first week of continuous influenza isolate reporting each season.
Observed fever and respiratory ED visits by age group are shown as black lines, and seasonally expected Serfling baseline visits are as red lines. Dashed lines represent model estimates plus two standard deviations. Shaded areas represent influenza-attributable excess ED visits by type A (blue) or B (red). Vertical lines indicate the first week of continuous influenza isolate reporting. Codes in top graph: A/H3-SY, influenza A(H3N2) Sydney; B/VI, influenza B/Victoria; A/H1, either A(H1N1) New Caledonia or A(H1N2) Wisconsin; A/H3-FU, influenza A(H3N2) Fujian; B/YA, influenza B/Yamagata; and A/H3-CA, influenza A(H3N2) California.
Weekly counts of influenza A and Bvirus isolates were reported duringthe study by three World HealthOrganization (WHO) collaboratinglaboratories located in NYC(
Summary of Excess Emergency Department Visits, Hospitalizations, and Deaths per 1,000 Population in New York City during the 2001–2002 to 2005–2006 Influenza Seasons
Confirmed hospitalizations by admission date in NYC from 1997–1998 to 2004–2005 were analyzed by multiple cause ICD-9 code reports for influenza (487), P&I (480–487), and respiratory syncytial virus (RSV) (079.6, 466.11) [
Observed P&I hospitalizations by age group from 1998–1999 to 2004–2005, and deaths for all ages from 1998–1999 to 2003–2004, are shown as black lines. Seasonally expected Serfling baseline levels are shown as red lines, and two-standard-deviation thresholds are shown as dashed lines. Catastrophic event deaths were removed from the data, and heat-wave period deaths were censored from the Serfling analysis. Observed P&I deaths during the 1999–2000 season were low due to a changeover from ICD-9 to ICD-10 coding. Codes in top graph: A/H3-SY, influenza A(H3N2) Sydney; B/VI, influenza B/Victoria; A/H1, either A(H1N1) New Caledonia or A(H1N2) Wisconsin; A/H3-FU, influenza A(H3N2) Fujian; B/YA, influenza B/Yamagata; and A/H3-CA, influenza A(H3N2) California.
Weekly counts of ED visits coded by chief complaint into the broad fever and respiratory syndrome and the narrow ILI syndrome categories followed annual sinusoidal patterns of winter seasonal increase, punctuated by seven distinct periods of 6–12 wk duration coincident with positive influenza A or B isolate reporting by WHO collaborating laboratories in the city (
Our estimates of expected ED visits by age and syndrome group during week
Estimates of excess seasonal epidemic ED visits were calculated as observed minus expected visits during influenza epidemic periods and consecutive weeks adjacent to those periods when the observed was above expected (shaded areas,
To better understand age-specific visit patterns that occurred during periods of sporadic or no influenza circulation, we evaluated the timing and impact of two additional causes of seasonal respiratory illness: RSV and tree pollen. We identified predominant RSV periods as the upper quartile weeks of RSV hospitalizations from 2001 to mid-December 2005 (data shown in
We defined initial detection of annual influenza epidemics as the first week ED visits, hospitalizations or deaths exceeded the two-standard-deviation threshold above model baseline. We compared the date of initial detection based on ED visits, hospitalizations, and deaths by age group (
Excess fever and respiratory ED visits and P&I hospitalizations and deaths were correlated against influenza isolates during the 33 wk centered on peak isolates. Top, maximum cross-correlation values for ED visits and hospitalizations coincided with influenza isolates (no lag) with ED visits leading hospitalizations, by less than 1 wk. Maximum correlation values for P&I deaths lagged isolates by 2 wk. Middle, maximum correlation values for 2–4 y, 5–12 y, and 13–17 y ED visits led isolates by 1 wk, < 2 y, 18–39 y, and 40–64 y visits had no lag, and ≥ 65 y visits lagged isolates by 1 wk. Bottom, maximum cross-correlation values for < 65 y P&I hospitalizations had no lag, for ≥ 65 y hospitalizations and < 65 y P&I deaths had a 1 wk lag, and for ≥ 65 y P&I deaths had a 3 wk lag.
To visualize the temporal course of age-specific illness trends in NYC, fever and respiratory ED visits were detrended, normalized, and plotted by week and age group. To detrend the data, we fit a least-squares linear regression to the nonepidemic fever and respiratory ED visit data by age group, as above, but with the annual and semiannual seasonal sinusoidal terms removed. We divided the observed data time series by the nonepidemic linear fit to obtain normalized ED visits by week and category. We made a surface plot of normalized weekly time series as a gradient interpolated between adjacent week and age-group data points (
Each season is shown from early September through mid-June by CDC week and year. Weeks of predominant influenza A (blue bar) or B (red bar) isolate surveillance during the study period, retrospectively identified predominant RSV hospitalizations through 2005 (gray bar), and dominant tree pollen periods for 2005 and 2006 (green bar) are shown above each season. Weekly ED visits by age group were detrended and normalized: age-specific intensity is shown as a color gradient interpolated between data points, with observed visits ranging from 2 to >4 times mean noninfluenza levels during peak epidemic weeks, and 0.25 to 1.25 during nonepidemic periods. Visits were increased across all age groups during periods of influenza A/H3N2 predominance, and were most markedly increased during the 2003–2004 and 2004–2005 A/Fujian-lineage epidemics. Visit increases during periods of influenza A/H1 and B predominance impacted preschool (2–4 y) and school-aged (5–17 y) children, and were most dramatically elevated during the B/Victoria-lineage reemergence in early 2002. The autumn and early-winter predominance of RSV preceded influenza in 2001, 2002, and 2005, and coincided with increased visits in the < 2 y and 2–4 y age groups. Visits were notably increased among school-aged children and working-aged adults during the dominant tree pollen period in 2006. RSV hospitalization data were not available for 2006 (*), and viral influenza surveillance reporting was incomplete during weeks 12 to 16, 2006 (*).
From the 2001–2002 to 2005–2006 influenza seasons in NYC, we estimate on average that 40,000 excess ED visits (5.0 visits per 1,000 population) occurred per season during the documented influenza circulation periods. We estimate that 2,800 excess P&I hospitalizations (0.35 per 1,000) on average occurred per season from 2001–2002 to 2004–2005, and 500 excess all-cause (0.065 per 1,000) and 100 excess P&I (0.012 per 1,000) deaths occurred per season from 2001–2002 to 2003–2004. The seasonal impact of excess ED visits, hospitalizations, and deaths, however, varied greatly by age group and circulating virus. We summarize our results by season and predominant viral period.
2001–2002 season: An estimated 24,000 excess fever and respiratory ED visits (3.0 visits per 1,000 population), 2,200 excess P&I hospitalizations (0.28 per 1,000), 540 excess all-cause deaths (0.067 per 1,000), and 90 excess P&I deaths (0.011 per 1,000) occurred during the influenza A/H3N2 predominant period in NYC from December 2001 to February 2002 (weeks 50–07) (
2002–2003 season: An estimated 10,000 excess ED visits (1.2 per 1,000 population) occurred during the predominant influenza A/H1 period (
2003–2004 season: An estimated 71,000 excess fever and respiratory ED visits (8.9 per 1,000 population) occurred during the influenza A/H3N2 predominant period from November 2003 to January 2004 (weeks 46–01) (
2004–2005 season: An estimated 42,000 excess fever and respiratory ED visits (5.2 per 1,000 population) and 3,600 excess P&I hospitalizations (0.44 per 1,000) occurred during the influenza A/H3N2 predominant period from November 2004 through January 2005 (weeks 46–04) (
2005–2006 season: An estimated 12,000 excess ED visits (1.5 per 1,000 population) occurred during the influenza A/H3N2 predominant period, with excess ED visits detected in the age groups 2–4 y, 5–12 y, 13–17 y, 18–39 y, and 40–64 y (
Influenza epidemic period increases were seen earlier in ED visits than in hospitalizations or deaths. During the influenza A/H3N2 epidemics in 2001–2002 and 2003–2004, excess all-ages fever and respiratory ED visits exceeded our two-standard-deviation Serfling model threshold 1 wk prior to P&I hospitalizations and, respectively, 1 and 3 wk prior to P&I deaths. During the mild influenza A/H1 epidemic in 2002–2003, all-ages fever and respiratory ED visits exceeded threshold 2 wk prior to deaths, and in the A/H3N2 epidemic in 2004–2005, all-ages ED visits exceeded threshold 3 wk prior to P&I hospitalizations (
Fever and respiratory ED visits among children often exceeded threshold before adults, but there were differences between seasons. During 2001–2002, ED visits exceeded model thresholds in the < 2 y and 2–4 y age groups 1 wk before the 13–17 y and 18–39 y age groups, and 2 wk before the 5–12 y and 40–64 y age groups. During the more severe 2003–2004 A/H3N2 epidemic, age-specific ED visits exceeded threshold in the 13–17 y age group 1 wk before the < 2 y, 2–4 y, 5–12 y, and 18–39 y groups, 3 wk before the 40–64 y group, and 4 wk before the ≥ 65 y group (
In our estimation of inherent epidemic timing, we limited our analysis to the 2003–2004 season, since it was the most severe and the only one with available ED, hospitalization, and death data and significant excess estimates across age groups (
Observed fever and respiratory ED visits peaked annually during influenza epidemic periods as defined by laboratory evidence (
The more specific subset of ILI ED visits, with mention of influenza or co-occurrence of fever with cough and/or sore throat, constituted only 11% of the broader fever and respiratory category (
In our analysis of New York City ED data, we found that predominant increases in fever and respiratory visits corresponded in timing and magnitude with laboratory-confirmed influenza, and we suggest that our estimates of excess ED visits provide a reliable surrogate measure of the incident impact attributable to influenza. By applying standard statistical methods to electronic ED chief complaint data, and interpreting results in the context of available information about circulating viruses, we were able to evaluate and track age-specific influenza morbidity in greater detail than was previously possible in NYC. We found the burden of excess ED visits was greatest during peak influenza periods, disproportionately impacted children, often impacted children earliest, generally coincided in timing with P&I hospitalization admission data, and preceded P&I death data by roughly 1–2 wk. The age-specific pattern of excess ED visits varied depending on the predominant circulating viral type, subtype, and strain. We expand on these findings below.
Beginning the week ending February 16, 2002 (week 06–2002), a marked and sustained increase in ED fever and respiratory visits began in NYC that predominated among school-aged children (5–17 y). In the US, influenza B/Victoria-lineage viruses had last been widespread 13 y prior, during 1988–1989 in a mixed influenza B and A/H1N1 season, and had last been the predominant epidemic virus 16 y earlier, during the 1985–1986 season [
Antigenic variant influenza A/H3N2 Fujian-lineage viruses emerged in autumn 2003 and were widespread across the US by the beginning of winter. The 2003–2004 seasonal influenza vaccine was reported to be poorly matched with the circulating A/Fujian viruses [
In autumn 2004, influenza viruses reported to be antigenically A/Fujian-like [
While RSV surveillance data were not available during the study period, coded hospitalizations allowed us to retrospectively identify predominant RSV periods in NYC (
In NYC we have consistently observed increases in ED respiratory and asthma visits outside of influenza season during the spring and early fall. The impact seen each spring is often severe enough to affect any syndrome that includes respiratory chief complaints, but is not associated with an increase in febrile illness. Pollen data obtained for the spring of 2005 and 2006 show that increases apparent in the broad fever and respiratory syndrome group among patients aged 5–64 y were coincident with the predominant annual tree pollen release (
In our analysis, we found that increases in influenza-attributable ED visits preceded hospitalizations, which in turn preceded deaths (corresponding to the logical progression of illness). During the 2003–2004 A/Fujian epidemic season we found fever and respiratory ED visits and P&I hospitalizations and deaths strongly correlated with viral isolate data, with an optimum lag between ED visits and deaths on the order of 2–3 wk (
A study of Boston area ED surveillance data reported that ED respiratory visits increased first among preschool age children (aged 3–4 y), some 5–7 wk before ED visits among older persons [
While the burden of influenza-attributable hospitalizations and deaths occurred predominantly among older adults, the burden of influenza-attributable excess fever and respiratory visits to NYC EDs during our study was predominantly among children (
Our study had several limitations. First, estimating influenza-attributable morbidity and mortality is imperfect due to the nonspecific nature of influenza symptoms and the lack of laboratory confirmation for the vast majority of influenza cases [
The reliance of researchers on hospitalization and death data, and the difficulty of obtaining population-based and age-detailed estimates of morbidity have contributed to the misconception that influenza affects only the very young and the very old. While the burden of severe morbidity and mortality occurs at the extremes of age, our findings support the observation that school-aged children experience early and high attack rates and exhibit significant morbidity, supporting evidence that they play an important role in communitywide transmission [
Twentieth-century influenza can inform twenty-first-century surveillance. The experience with pandemic influenza in the last century in New York City illustrates that early waves, multiple waves, and within- and between-season age shifts in morbidity and mortality can occur [
Observed ILI syndrome ED visits by age group are shown as black lines, and seasonally expected Serfling baseline visits as red lines. Dashed lines represent epidemic thresholds as model estimates plus two-standard deviations. Shaded areas represent estimated influenza attributable excess ED visits: blue areas correspond to periods of increasing and dominant influenza A circulation and red areas to influenza B. Vertical lines indicate the first week of continuous influenza isolate reporting each season.
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Vertical lines indicate the first week of continuous influenza virus isolate reporting, viral isolate surveillance is indicated as in
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Influenza isolate circulation dates are the CDC weeks from the first influenza isolate reported in continuous weeks (vertical lines in
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We thank D. Das, T. Singh, and W. Li for assistance with NYC ED surveillance, hospitalization, and mortality data; and S. Harper, M. Layton, D. Morens, and C. Viboud for helpful comments on earlier drafts. We are indebted to A. Galvani, S. Morse, L. Simonsen, and A-J Valleron for critical comments and generously shared insights.
Centers for Disease Control and Prevention
emergency department
influenza-like illness
New York City
pneumonia and influenza
respiratory syncytial virus