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1.  Situational Awareness of Influenza Activity Based on Multiple Streams of Surveillance Data Using Multivariate Dynamic Linear Model 
PLoS ONE  2012;7(5):e38346.
Background
Multiple sources of influenza surveillance data are becoming more available; however integration of these data streams for situational awareness of influenza activity is less explored.
Methods and Results
We applied multivariate time-series methods to sentinel outpatient and school absenteeism surveillance data in Hong Kong during 2004–2009. School absenteeism data and outpatient surveillance data experienced interruptions due to school holidays and changes in public health guidelines during the pandemic, including school closures and the establishment of special designated flu clinics, which in turn provided ‘drop-in’ fever counts surveillance data. A multivariate dynamic linear model was used to monitor influenza activity throughout epidemics based on all available data. The inferred level followed influenza activity closely at different times, while the inferred trend was less competent with low influenza activity. Correlations between inferred level and trend from the multivariate model and reference influenza activity, measured by the product of weekly laboratory influenza detection rates and weekly general practitioner influenza-like illness consultation rates, were calculated and compared with those from univariate models. Over the whole study period, there was a significantly higher correlation (ρ = 0.82, p≤0.02) for the inferred trend based on the multivariate model compared to other univariate models, while the inferred trend from the multivariate model performed as well as the best univariate model in the pre-pandemic and the pandemic period. The inferred trend and level from the multivariate model was able to match, if not outperform, the best univariate model albeit with missing data plus drop-in and drop-out of different surveillance data streams. An overall influenza index combining level and trend was constructed to demonstrate another potential use of the method.
Conclusions
Our results demonstrate the potential use of multiple streams of influenza surveillance data to promote situational awareness about the level and trend of seasonal and pandemic influenza activity.
doi:10.1371/journal.pone.0038346
PMCID: PMC3364986  PMID: 22675456
2.  The New School Absentees Reporting System for Pandemic Influenza A/H1N1 2009 Infection in Japan 
PLoS ONE  2012;7(2):e30639.
Objective
To evaluate the new Japanese School Absentees Reporting System for Infectious Disease (SARSID) for pandemic influenza A/H1N1 2009 infection in comparison with the National epidemiological Surveillance of Infectious Disease (NESID).
Methods
We used data of 53,223 students (97.7%) in Takamatsu city Japan. Data regarding school absentees in SARSID was compared with that in NESID from Oct 13, 2009 to Jan 12, 2010.
Results
Similar trends were observed both in SARSID and NESID. However, the epidemic trend for influenza in SARSID was thought to be more sensitive than that in NESID.
Conclusion
The epidemic trend for influenza among school-aged children could be easily and rapidly assessed by SARSID compared to NESID. SARSID might be useful for detecting the epidemic trend of influenza.
doi:10.1371/journal.pone.0030639
PMCID: PMC3281859  PMID: 22363458
3.  Statistical estimates of absenteeism attributable to seasonal and pandemic influenza from the Canadian Labour Force Survey 
Background
As many respiratory viruses are responsible for influenza like symptoms, accurate measures of the disease burden are not available and estimates are generally based on statistical methods. The objective of this study was to estimate absenteeism rates and hours lost due to seasonal influenza and compare these estimates with estimates of absenteeism attributable to the two H1N1 pandemic waves that occurred in 2009.
Methods
Key absenteeism variables were extracted from Statistics Canada's monthly labour force survey (LFS). Absenteeism and the proportion of hours lost due to own illness or disability were modelled as a function of trend, seasonality and proxy variables for influenza activity from 1998 to 2009.
Results
Hours lost due to the H1N1/09 pandemic strain were elevated compared to seasonal influenza, accounting for a loss of 0.2% of potential hours worked annually. In comparison, an estimated 0.08% of hours worked annually were lost due to seasonal influenza illnesses. Absenteeism rates due to influenza were estimated at 12% per year for seasonal influenza over the 1997/98 to 2008/09 seasons, and 13% for the two H1N1/09 pandemic waves. Employees who took time off due to a seasonal influenza infection took an average of 14 hours off. For the pandemic strain, the average absence was 25 hours.
Conclusions
This study confirms that absenteeism due to seasonal influenza has typically ranged from 5% to 20%, with higher rates associated with multiple circulating strains. Absenteeism rates for the 2009 pandemic were similar to those occurring for seasonal influenza. Employees took more time off due to the pandemic strain than was typical for seasonal influenza.
doi:10.1186/1471-2334-11-90
PMCID: PMC3103439  PMID: 21486453
4.  School Absenteeism As an Adjunct Surveillance Indicator: Experience during the Second Wave of the 2009 H1N1 Pandemic in Quebec, Canada 
PLoS ONE  2012;7(3):e34084.
Background
A school absenteeism surveillance system was implemented in the province of Quebec, Canada during the second wave of the 2009 H1N1pandemic. This paper compares this surveillance approach with other available indicators.
Method
All (3432) elementary and high schools from Quebec were included. Each school was required to report through a web-based system any day where the proportion of students absent for influenza-like illness (ILI) exceeded 10% of current school enrolment.
Results
Between October 18 and December 12 2009, 35.6% of all schools met the 10% absenteeism threshold. This proportion was greater in elementary compared to high schools (40% vs 19%) and in smaller compared to larger schools (44% vs 22%). The maximum absenteeism rate was reached the first day of reporting or within the next two days in 55% and 31% of schools respectively. The first reports and subsequent peak in school absenteeism provincially preceded the peak in paediatric hospitalization by two and one weeks, respectively. Trends in school surveillance otherwise mirrored other indicators.
Conclusion
During a pandemic, school outbreak surveillance based on a 10% threshold appears insufficient to trigger timely intervention within a given affected school. However, school surveillance appears well-correlated and slightly anticipatory compared to other population indicators. As such, school absenteeism warrants further evaluation as an adjunct surveillance indicator whose overall utility will depend upon specified objectives, and other existing capacity for monitoring and response.
doi:10.1371/journal.pone.0034084
PMCID: PMC3316605  PMID: 22479531
5.  Evaluation of school absenteeism data for early outbreak detection, New York City 
BMC Public Health  2005;5:105.
Background
School absenteeism data may have utility as an early indicator of disease outbreaks, however their value should be critically examined. This paper describes an evaluation of the utility of school absenteeism data for early outbreak detection in New York City (NYC).
Methods
To assess citywide temporal trends in absenteeism, we downloaded three years (2001–02, 2002–03, 2003–04) of daily school attendance data from the NYC Department of Education (DOE) website. We applied the CuSum method to identify aberrations in the adjusted daily percent absent. A spatial scan statistic was used to assess geographic clustering in absenteeism for the 2001–02 academic year.
Results
Moderate increases in absenteeism were observed among children during peak influenza season. Spatial analysis detected 790 significant clusters of absenteeism among elementary school children (p < 0.01), two of which occurred during a previously reported outbreak.
Conclusion
Monitoring school absenteeism may be moderately useful for detecting large citywide epidemics, however, school-level data were noisy and we were unable to demonstrate any practical value in using cluster analysis to detect localized outbreaks. Based on these results, we will not implement prospective monitoring of school absenteeism data, but are evaluating the utility of more specific school-based data for outbreak detection.
doi:10.1186/1471-2458-5-105
PMCID: PMC1260024  PMID: 16212669
6.  Effective Detection of the 2009 H1N1 Influenza Pandemic in U.S. Veterans Affairs Medical Centers Using a National Electronic Biosurveillance System 
PLoS ONE  2010;5(3):e9533.
Background
The 2008–09 influenza season was the time in which the Department of Veterans Affairs (VA) utilized an electronic biosurveillance system for tracking and monitoring of influenza trends. The system, known as ESSENCE or Electronic Surveillance System for the Early Notification of Community-based Epidemics, was monitored for the influenza season as well as for a rise in influenza cases at the start of the H1N1 2009 influenza pandemic. We also describe trends noted in influenza-like illness (ILI) outpatient encounter data in VA medical centers during the 2008–09 influenza season, before and after the recognition of pandemic H1N1 2009 influenza virus.
Methodology/Principal Findings
We determined prevalence of ILI coded visits using VA's ESSENCE for 2008–09 seasonal influenza (Sept. 28, 2008–April 25, 2009 corresponding to CDC 2008–2009 flu season weeks 40–16) and the early period of pandemic H1N1 2009 (April 26, 2009–July 31, 2009 corresponding to CDC 2008–2009 flu season weeks 17–30). Differences in diagnostic ICD-9-CM code frequencies were analyzed using Chi-square and odds ratios. There were 649,574 ILI encounters captured representing 633,893 patients. The prevalence of VA ILI visits mirrored the CDC's Outpatient ILI Surveillance Network (ILINet) data with peaks in late December, early February, and late April/early May, mirroring the ILINet data; however, the peaks seen in the VA were smaller. Of 31 ILI codes, 6 decreased and 11 increased significantly during the early period of pandemic H1N1 2009. The ILI codes that significantly increased were more likely to be symptom codes. Although influenza with respiratory manifestation (487.1) was the most common code used among 150 confirmed pandemic H1N1 2009 cases, overall it significantly decreased since the start of the pandemic.
Conclusions/Significance
VA ESSENCE effectively detected and tracked changing ILI trends during pandemic H1N1 2009 and represents an important temporal alerting system for monitoring health events in VA facilities.
doi:10.1371/journal.pone.0009533
PMCID: PMC2832014  PMID: 20209055
7.  Estimating the costs of school closure for mitigating an influenza pandemic 
BMC Public Health  2008;8:135.
Background
School closure is a key component of many countries' plans to mitigate the effect of an influenza pandemic. Although a number of studies have suggested that such a policy might reduce the incidence, there are no published studies of the cost of such policies. This study attempts to fill this knowledge gap
Methods
School closure is expected to lead to significant work absenteeism of working parents who are likely to be the main care givers to their dependent children at home. The cost of absenteeism due to school closure is calculated as the paid productivity loss of parental absenteeism during the period of school closure. The cost is estimated from societal perspective using a nationally representative survey.
Results
The results show that overall about 16% of the workforce is likely to be the main caregiver for dependent children and therefore likely to take absenteeism. This rises to 30% in the health and social care sector, as a large proportion of the workforce are women. The estimated costs of school closure are significant, at £0.2 bn – £1.2 bn per week. School closure is likely to significantly exacerbate the pressures on the health system through staff absenteeism.
Conclusion
The estimates of school closure associated absenteeism and the projected cost would be useful for pandemic planning for business continuity, and for cost effectiveness evaluation of different pandemic influenza mitigation strategies.
doi:10.1186/1471-2458-8-135
PMCID: PMC2377259  PMID: 18435855
8.  Computerized general practice based networks yield comparable performance with sentinel data in monitoring epidemiological time-course of influenza-like illness and acute respiratory illness 
BMC Family Practice  2010;11:24.
Background
Computerized morbidity registration networks might serve as early warning systems in a time where natural epidemics such as the H1N1 flu can easily spread from one region to another.
Methods
In this contribution we examine whether general practice based broad-spectrum computerized morbidity registration networks have the potential to act as a valid surveillance instrument of frequently occurring diseases. We compare general practice based computerized data assessing the frequency of influenza-like illness (ILI) and acute respiratory infections (ARI) with data from a well established case-specific sentinel network, the European Influenza Surveillance Scheme (EISS). The overall frequency and trends of weekly ILI and ARI data are compared using both networks.
Results
Detection of influenza-like illness and acute respiratory illness occurs equally fast in EISS and the computerized network. The overall frequency data for ARI are the same for both networks, the overall trends are similar, but the increases and decreases in frequency do not occur in exactly the same weeks. For ILI, the overall rate was slightly higher for the computerized network population, especially before the increase of ILI, the overall trend was almost identical and the increases and decreases occur in the same weeks for both networks.
Conclusions
Computerized morbidity registration networks are a valid tool for monitoring frequent occurring respiratory diseases and the detection of sudden outbreaks.
doi:10.1186/1471-2296-11-24
PMCID: PMC2856540  PMID: 20307266
9.  Teacher led school-based surveillance can allow accurate tracking of emerging infectious diseases - evidence from serial cross-sectional surveys of febrile respiratory illness during the H1N1 2009 influenza pandemic in Singapore 
BMC Infectious Diseases  2012;12:336.
Background
Schools are important foci of influenza transmission and potential targets for surveillance and interventions. We compared several school-based influenza monitoring systems with clinic-based influenza-like illness (ILI) surveillance, and assessed the variation in illness rates between and within schools.
Methods
During the initial wave of pandemic H1N1 (pdmH1N1) infections from June to Sept 2009 in Singapore, we collected data on nation-wide laboratory confirmed cases (Sch-LCC) and daily temperature monitoring (Sch-DTM), and teacher-led febrile respiratory illness reporting in 6 sentinel schools (Sch-FRI). Comparisons were made against age-stratified clinic-based influenza-like illness (ILI) data from 23 primary care clinics (GP-ILI) and proportions of ILI testing positive for pdmH1N1 (Lab-ILI) by computing the fraction of cumulative incidence occurring by epidemiological week 30 (when GP-ILI incidence peaked); and cumulative incidence rates between school-based indicators and sero-epidemiological pdmH1N1 incidence (estimated from changes in prevalence of A/California/7/2009 H1N1 hemagglutination inhibition titers ≥ 40 between pre-epidemic and post-epidemic sera). Variation in Sch-FRI rates in the 6 schools was also investigated through a Bayesian hierarchical model.
Results
By week 30, for primary and secondary school children respectively, 63% and 79% of incidence for Sch-LCC had occurred, compared with 50% and 52% for GP-ILI data, and 48% and 53% for Sch-FRI. There were 1,187 notified cases and 7,588 episodes in the Sch-LCC and Sch-DTM systems; given school enrollment of 485,723 children, this represented 0.24 cases and 1.6 episodes per 100 children respectively. Mean Sch-FRI rate was 28.8 per 100 children (95% CI: 27.7 to 29.9) in the 6 schools. We estimate from serology that 41.8% (95% CI: 30.2% to 55.9%) of primary and 43.2% (95% CI: 28.2% to 60.8%) of secondary school-aged children were infected. Sch-FRI rates were similar across the 6 schools (23 to 34 episodes per 100 children), but there was widespread variation by classrooms; in the hierarchical model, omitting age and school effects was inconsequential but neglecting classroom level effects led to highly significant reductions in goodness of fit.
Conclusions
Epidemic curves from Sch-FRI were comparable to GP-ILI data, and Sch-FRI detected substantially more infections than Sch-LCC and Sch-DTM. Variability in classroom attack rates suggests localized class-room transmission.
doi:10.1186/1471-2334-12-336
PMCID: PMC3544582  PMID: 23206689
Respiratory tract infections; Vaccination; Serology
10.  Biosurveillance applying scan statistics with multiple, disparate data sources 
Researchers working on the Department of Defense Global Emerging Infections System (DoD-GEIS) pilot system, the Electronic Surveillance System for the Early Notification of Community-Based Epidemics (ESSENCE), have applied scan statistics for early outbreak detection using hoth traditional and nontraditional data sources. These sources include medical data indexed byInternational Classification of Disease, 9th Revision (ICD-9) diagnosis codes, as well as less-specific, but potentially timelier, indicators such as records of over-the-counter remedy sales and of school absenteeism. Early efforts employed the Kulldorff scan statistic as implemented in the SaTScan software of the National Cancer Institute. A key obstacle to this application is that the input data streams are typically based on time-varying factors, such as consumer behavior, rather than simply on the populations of the component subregions. We have used both modeling and recent historical data distributions to obtain background spatial distributions. Data analyses have provided guidance on how to condition and model input data to avoid excessive clustering. We have used this methodology in combining data sources for both retrospective studies of known outbreaks and surveillance of high-profile events of concern to local public health authorities. We have integrated the scan statistic capability into a Microsoft Access-based system in which we may include or exclude data sources, vary time windows separately for different data sources, censor data from subsets of individual providers or subregions, adjust the background computation method, and run retrospective or simulated studies.
doi:10.1007/PL00022316
PMCID: PMC3456540  PMID: 12791780
Biosurveillance; Clustering; Kulldorff; Scan statistics
11.  Predicting the Epidemic Sizes of Influenza A/H1N1, A/H3N2, and B: A Statistical Method 
PLoS Medicine  2011;8(7):e1001051.
Using weekly influenza surveillance data from the US CDC, Edward Goldstein and colleagues develop a statistical method to predict the sizes of epidemics caused by seasonal influenza strains. This method could inform decisions about the most appropriate vaccines or drugs needed early in the influenza season.
Background
The epidemic sizes of influenza A/H3N2, A/H1N1, and B infections vary from year to year in the United States. We use publicly available US Centers for Disease Control (CDC) influenza surveillance data between 1997 and 2009 to study the temporal dynamics of influenza over this period.
Methods and Findings
Regional outpatient surveillance data on influenza-like illness (ILI) and virologic surveillance data were combined to define a weekly proxy for the incidence of each strain in the United States. All strains exhibited a negative association between their cumulative incidence proxy (CIP) for the whole season (from calendar week 40 of each year to calendar week 20 of the next year) and the CIP of the other two strains (the complementary CIP) from the start of the season up to calendar week 2 (or 3, 4, or 5) of the next year. We introduce a method to predict a particular strain's CIP for the whole season by following the incidence of each strain from the start of the season until either the CIP of the chosen strain or its complementary CIP exceed certain thresholds. The method yielded accurate predictions, which generally occurred within a few weeks of the peak of incidence of the chosen strain, sometimes after that peak. For the largest seasons in the data, which were dominated by A/H3N2, prediction of A/H3N2 incidence always occurred at least several weeks in advance of the peak.
Conclusion
Early circulation of one influenza strain is associated with a reduced total incidence of the other strains, consistent with the presence of interference between subtypes. Routine ILI and virologic surveillance data can be combined using this new method to predict the relative size of each influenza strain's epidemic by following the change in incidence of a given strain in the context of the incidence of cocirculating strains.
Please see later in the article for the Editors' Summary
Editors' Summary
Background
Every winter in temperate countries, millions of people catch influenza, a viral infection of the nose, throat, and airways. Most infected individuals recover quickly but seasonal influenza outbreaks (epidemics) kill about half a million people annually. Epidemics of influenza occur because small but frequent changes in the viral proteins (antigens) to which the immune system responds mean that an immune response produced one year provides only partial protection against influenza the next year. Annual immunization with a vaccine that contains killed influenza viruses of the major circulating strains boosts this natural immunity and greatly reduces a person's chances of catching influenza. Influenza epidemics in temperate latitudes are usually caused by an influenza B virus or one of two influenza A subtypes called A/H3N2 and A/H1N1. The names of the influenza A viruses indicate the types of two major influenza antigens—hemagglutinin (H3 or H1) and neuraminidase (N2 or N1)—present in the viruses.
Why Was This Study Done?
At present, there is no way to predict whether influenza B or an influenza A subtype will be dominant (responsible for the majority of infections) in any given influenza season. There is also no way to predict the size of the epidemic that will be caused by each viral strain. Public health officials would like to be able to make predictions of this sort early in the winter to help them determine which measures to recommend to minimize the illness and death caused by influenza. In this study, the researchers use weekly influenza surveillance data collected by the US Centers for Disease Control and Prevention (CDC) to study the temporal dynamics of seasonal influenza in the United States between 1997 and 2009 and to develop a statistical method to predict the sizes of epidemics caused by influenza A/H1N1, A/H3N2, and B.
What Did the Researchers Do and Find?
The CDC influenza surveillance system collects information on the proportion of patients attending US outpatient facilities who have an influenza-like illness (fever and a cough and/or a sore throat in the absence of any known cause other than influenza) and on the proportion of respiratory viral isolates testing positive for specific influenza strains at US viral surveillance laboratories. The researchers combined these data to define a weekly “proxy” incidence of each influenza strain across the United States (an estimate of the number of new cases per week in the US population) and a cumulative incidence proxy (CIP) for each influenza season. For each strain, there was a negative association between its whole-season CIP and the early-season CIP of the other two strains (the complementary CIP). That is, high infection rates with one strain appeared to interfere with the transmission of other strains. Given this relationship, the researchers then developed a statistical algorithm (a step-by-step problem solving method) that accurately predicted the whole-season CIP for a particular strain by following the incidence of each strain from the start of the season until either its CIP or the complementary CIP had exceeded a specific threshold. So, for example, for influenza B, the algorithm provided an accurate prediction of the whole-season CIP before the peak of influenza B incidence for each season included in the study. Similarly, prediction of whole-season A/H3N2 incidence always occurred several weeks in advance of its weekly incidence peak.
What Do These Findings Mean?
These findings suggest that early circulation of one influenza strain is associated with a reduced total incidence of other strains, possibly because of cross-subtype immunity. Importantly, they also suggest that routine early-season surveillance data can be used to predict the relative size of the epidemics caused by each influenza strain in the United States and in other countries where sufficient surveillance data are available. Because the algorithm makes many assumptions and simplifies the behavior of influenza epidemics, its predictions may not always be accurate. Moreover, it needs to be tested with data collected over more influenza seasons. Nevertheless, the algorithm's ability to predict the relative epidemic size of A/H3N2, the influenza strain with the highest death rates, several weeks before its peak in seasons in which it was the dominant strain suggests that this predictive method could help public-health officials introduce relevant preventative and/or treatment measures early in each influenza season.
Additional Information
Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1001051.
The US Centers for Disease Control and Prevention provides information for patients and health professionals on all aspects of seasonal influenza, including information about the US influenza surveillance system
The UK National Health Service Choices Web site also provides information for patients about seasonal influenza; the UK Health Protection Agency provides information on influenza surveillance in the UK
MedlinePlus has links to further information about influenza l (in English and Spanish)
doi:10.1371/journal.pmed.1001051
PMCID: PMC3130020  PMID: 21750666
12.  Timeliness of Data Sources Used for Influenza Surveillance 
Objective
In recent years, influenza surveillance data has expanded to include alternative sources such as emergency department data, absenteeism reports, pharmaceutical sales, website access and health advice calls. This study presents a review of alternative data sources for influenza surveillance, summarizes the time advantage or timeliness of each source relative to traditional reporting and discusses the strengths and weaknesses of competing approaches.
Methods
A literature search was conducted on Medline to identify relevant articles published after 1990. A total of 15 articles were obtained that reported the timeliness of an influenza surveillance system. Timeliness was described by peak comparison, aberration detection comparison and correlation.
Results
Overall, the data sources were highly correlated with traditional sources and had variable timeliness. Over-the-counter pharmaceutical sales, emergency visits, absenteeism and health calls appear to be more timely than physician diagnoses, sentinel influenza-like-illness surveillance and virological confirmation.
Conclusions
The methods used to describe timeliness vary greatly between studies and hence no strong conclusions regarding the most timely source/s of data can be reached. Future studies should apply the aberration detection method to determine data source timeliness in preference to the peak comparison method and correlation.
doi:10.1197/jamia.M2328
PMCID: PMC1975801  PMID: 17600101
13.  Effects of Hand Hygiene Campaigns on Incidence of Laboratory-confirmed Influenza and Absenteeism in Schoolchildren, Cairo, Egypt 
Emerging Infectious Diseases  2011;17(4):619-625.
To evaluate the effectiveness of an intensive hand hygiene campaign on reducing absenteeism caused by influenza-like illness (ILI), diarrhea, conjunctivitis, and laboratory-confirmed influenza, we conducted a randomized control trial in 60 elementary schools in Cairo, Egypt. Children in the intervention schools were required to wash hands twice each day, and health messages were provided through entertainment activities. Data were collected on student absenteeism and reasons for illness. School nurses collected nasal swabs from students with ILI, which were tested by using a qualitative diagnostic test for influenza A and B. Compared with results for the control group, in the intervention group, overall absences caused by ILI, diarrhea, conjunctivitis, and laboratory-confirmed influenza were reduced by 40%, 30%, 67%, and 50%, respectively (p<0.0001 for each illness). An intensive hand hygiene campaign was effective in reducing absenteeism caused by these illnesses.
doi:10.3201/eid1704.101353
PMCID: PMC3377412  PMID: 21470450
Hand hygiene; campaigns; influenza; viruses; schoolchildren; Egypt; absenteeism; expedited; research
14.  Absenteeism among hospital staff during an influenza epidemic: implications for immunoprophylaxis. 
The 1980-81 epidemic of influenza A/Bangkok 79 was responsible for increased absenteeism (1.7 times the rate for the corresponding period of the subsequent nonepidemic year) among selected hospital staff in Winnipeg's Health Sciences Centre. Retrospective study of employment records for 25 of the centre's largest departments showed excess sick-leave costs of about $24 500 during the 2-week period of peak absenteeism that included the epidemic. Although the centre was sampling prospectively for the virus the first positive results became available too late for chemoprophylactic measures to have been effective. The greater increase in absenteeism among nursing staff caring for patients with chronic respiratory disease and nurses working on general medical or pediatric acute infection/isolation wards suggested that these groups be targeted for influenza vaccination in hospitals.
PMCID: PMC1483462  PMID: 6467117
15.  Rapid detection of pandemic influenza in the presence of seasonal influenza 
BMC Public Health  2010;10:726.
Background
Key to the control of pandemic influenza are surveillance systems that raise alarms rapidly and sensitively. In addition, they must minimise false alarms during a normal influenza season. We develop a method that uses historical syndromic influenza data from the existing surveillance system 'SERVIS' (Scottish Enhanced Respiratory Virus Infection Surveillance) for influenza-like illness (ILI) in Scotland.
Methods
We develop an algorithm based on the weekly case ratio (WCR) of reported ILI cases to generate an alarm for pandemic influenza. From the seasonal influenza data from 13 Scottish health boards, we estimate the joint probability distribution of the country-level WCR and the number of health boards showing synchronous increases in reported influenza cases over the previous week. Pandemic cases are sampled with various case reporting rates from simulated pandemic influenza infections and overlaid with seasonal SERVIS data from 2001 to 2007. Using this combined time series we test our method for speed of detection, sensitivity and specificity. Also, the 2008-09 SERVIS ILI cases are used for testing detection performances of the three methods with a real pandemic data.
Results
We compare our method, based on our simulation study, to the moving-average Cumulative Sums (Mov-Avg Cusum) and ILI rate threshold methods and find it to be more sensitive and rapid. For 1% case reporting and detection specificity of 95%, our method is 100% sensitive and has median detection time (MDT) of 4 weeks while the Mov-Avg Cusum and ILI rate threshold methods are, respectively, 97% and 100% sensitive with MDT of 5 weeks. At 99% specificity, our method remains 100% sensitive with MDT of 5 weeks. Although the threshold method maintains its sensitivity of 100% with MDT of 5 weeks, sensitivity of Mov-Avg Cusum declines to 92% with increased MDT of 6 weeks. For a two-fold decrease in the case reporting rate (0.5%) and 99% specificity, the WCR and threshold methods, respectively, have MDT of 5 and 6 weeks with both having sensitivity close to 100% while the Mov-Avg Cusum method can only manage sensitivity of 77% with MDT of 6 weeks. However, the WCR and Mov-Avg Cusum methods outperform the ILI threshold method by 1 week in retrospective detection of the 2009 pandemic in Scotland.
Conclusions
While computationally and statistically simple to implement, the WCR algorithm is capable of raising alarms, rapidly and sensitively, for influenza pandemics against a background of seasonal influenza. Although the algorithm was developed using the SERVIS data, it has the capacity to be used at other geographic scales and for different disease systems where buying some early extra time is critical.
doi:10.1186/1471-2458-10-726
PMCID: PMC3001734  PMID: 21106071
16.  Estimates of Pandemic Influenza Vaccine Effectiveness in Europe, 2009–2010: Results of Influenza Monitoring Vaccine Effectiveness in Europe (I-MOVE) Multicentre Case-Control Study 
PLoS Medicine  2011;8(1):e1000388.
Results from a European multicentre case-control study reported by Marta Valenciano and colleagues suggest good protection by the pandemic monovalent H1N1 vaccine against pH1N1 and no effect of the 2009–2010 seasonal influenza vaccine on H1N1.
Background
A multicentre case-control study based on sentinel practitioner surveillance networks from seven European countries was undertaken to estimate the effectiveness of 2009–2010 pandemic and seasonal influenza vaccines against medically attended influenza-like illness (ILI) laboratory-confirmed as pandemic influenza A (H1N1) (pH1N1).
Methods and Findings
Sentinel practitioners swabbed ILI patients using systematic sampling. We included in the study patients meeting the European ILI case definition with onset of symptoms >14 days after the start of national pandemic vaccination campaigns. We compared pH1N1 cases to influenza laboratory-negative controls. A valid vaccination corresponded to >14 days between receiving a dose of vaccine and symptom onset. We estimated pooled vaccine effectiveness (VE) as 1 minus the odds ratio with the study site as a fixed effect. Using logistic regression, we adjusted VE for potential confounding factors (age group, sex, month of onset, chronic diseases and related hospitalizations, smoking history, seasonal influenza vaccinations, practitioner visits in previous year). We conducted a complete case analysis excluding individuals with missing values and a multiple multivariate imputation to estimate missing values. The multivariate imputation (n = 2902) adjusted pandemic VE (PIVE) estimates were 71.9% (95% confidence interval [CI] 45.6–85.5) overall; 78.4% (95% CI 54.4–89.8) in patients <65 years; and 72.9% (95% CI 39.8–87.8) in individuals without chronic disease. The complete case (n = 1,502) adjusted PIVE were 66.0% (95% CI 23.9–84.8), 71.3% (95% CI 29.1–88.4), and 70.2% (95% CI 19.4–89.0), respectively. The adjusted PIVE was 66.0% (95% CI −69.9 to 93.2) if vaccinated 8–14 days before ILI onset. The adjusted 2009–2010 seasonal influenza VE was 9.9% (95% CI −65.2 to 50.9).
Conclusions
Our results suggest good protection of the pandemic monovalent vaccine against medically attended pH1N1 and no effect of the 2009–2010 seasonal influenza vaccine. However, the late availability of the pandemic vaccine and subsequent limited coverage with this vaccine hampered our ability to study vaccine benefits during the outbreak period. Future studies should include estimation of the effectiveness of the new trivalent vaccine in the upcoming 2010–2011 season, when vaccination will occur before the influenza season starts.
Please see later in the article for the Editors' Summary
Editors' Summary
Background
Following the World Health Organization's declaration of pandemic phase six in June 2009, manufacturers developed vaccines against pandemic influenza A 2009 (pH1N1). On the basis of the scientific opinion of the European Medicines Agency, the European Commission initially granted marketing authorization to three pandemic vaccines for use in European countries. During the autumn of 2009, most European countries included the 2009–2010 seasonal influenza vaccine and the pandemic vaccine in their influenza vaccination programs.
The Influenza Monitoring Vaccine Effectiveness in Europe network (established to monitor seasonal and pandemic influenza vaccine effectiveness) conducted seven case-control and three cohort studies in seven European countries in 2009–2010 to estimate the effectiveness of the pandemic and seasonal vaccines. Data from the seven pilot case-control studies were pooled to provide overall adjusted estimates of vaccine effectiveness.
Why Was This Study Done?
After seasonal and pandemic vaccines are made available to populations, it is necessary to estimate the effectiveness of the vaccines at the population level during every influenza season. Therefore, this study was conducted in European countries to estimate the pandemic influenza vaccine effectiveness and seasonal influenza vaccine effectiveness against people presenting to their doctor with influenza-like illness who were confirmed (by laboratory tests) to be infected with pH1N1.
What Did the Researchers Do and Find?
The researchers conducted a multicenter case-control study on the basis of practitioner surveillance networks from seven countries—France, Hungary, Ireland, Italy, Romania, Portugal, and Spain. Patients consulting a participating practitioner for influenza-like illness had a nasal or throat swab taken within 8 days of symptom onset. Cases were swabbed patients who tested positive for pH1N1. Patients presenting with influenza-like illness whose swab tested negative for any influenza virus were controls.
Individuals were considered vaccinated if they had received a dose of the vaccine more than 14 days before the date of onset of influenza-like illness and unvaccinated if they were not vaccinated at all, or if the vaccine was given less than 15 days before the onset of symptoms. The researchers analyzed pandemic influenza vaccination effectiveness in those vaccinated less than 8 days, those vaccinated between and including 8 and 14 days, and those vaccinated more than 14 days before onset of symptoms compared to those who had never been vaccinated.
The researchers used modeling (taking account of all potential confounding factors) to estimate adjusted vaccine effectiveness and stratified the adjusted pandemic influenza vaccine effectiveness and the adjusted seasonal influenza vaccine effectiveness in three age groups (<15, 15–64, and ≥65 years of age).
The adjusted results suggest that the 2009–2010 seasonal influenza vaccine did not protect against pH1N1 illness. However, one dose of the pandemic vaccines used in the participating countries conferred good protection (65.5%–100% according to various stratifications performed) against pH1N1 in people who attended their practitioner with influenza-like illness, especially in people aged <65 years and in those without any chronic disease. Furthermore, good pandemic influenza vaccine effectiveness was observed as early as 8 days after vaccination.
What Do These Findings Mean?
The results of this study provide early estimates of the pandemic influenza vaccine effectiveness suggesting that the monovalent pandemic vaccines have been effective. The findings also give an indication of the vaccine effectiveness for the Influenza A (H1N1) 2009 strain included in the 2010–2011 seasonal vaccines, although specific vaccine effectiveness studies will have to be conducted to verify if similar good effectiveness are observed with 2010–2011 trivalent vaccines. However, the results of this study should be interpreted with caution because of limitations in the pandemic context (late timing of the studies, low incidence, low vaccine coverage leading to imprecise estimates) and potential biases due the study design, confounding factors, and missing values. The researchers recommend that in future season studies, the sample size per country should be enlarged in order to allow for precise pooled and stratified analyses.
Additional Information
Please access these websites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1000388.
The World Health Organization has information on H1N1 vaccination
The US Centers for Disease Control and Prevention provides a fact sheet on the 2009 H1N1 influenza virus
The US Department of Health and Human services has a comprehensive website on flu
The European Centre for Disease Prevention and Control provides information on 2009 H1N1 pandemic
The European Centre for Disease Prevention and Control presents a summary of the 2009 H1N1 pandemic in Europe and elsewhere
doi:10.1371/journal.pmed.1000388
PMCID: PMC3019108  PMID: 21379316
17.  Increased emergency department chief complaints of fever identified the influenza (H1N1) pandemic before outpatient symptom surveillance 
Objective
To determine whether a sentinel clinic network or an emergency department (ED) was more timely in identifying the 2009 influenza A (H1N1) pandemic.
Methods
All reasons for presenting to the adult regional medical ED were coded online by admission secretaries, without the aid of medical personnel. Increased influenza activity defined by weekly chief complaints of fever was compared with activity defined by the Israel Center for Disease Control (viral surveillance as well as a large sentinel clinic network).
Results
Influenza activity during the pandemic increased in the ED 2 weeks before outpatient sentinel clinics. During the pandemic, maximal ED activity was much higher than in previous seasons. Maximal activity during the past 5 years correlated with the timeliness of the chief complaint of fever in identifying the onset of epidemics.
Conclusion
Chief complaint of fever in the ED can be a sensitive marker of increased influenza activity and might replace the use of sentinel clinics.
doi:10.1007/s12199-011-0213-2
PMCID: PMC3258318  PMID: 21448581
Emergency department; Fever; Clusters; Influenza; Epidemics
18.  Using surveillance data to estimate pandemic vaccine effectiveness against laboratory confirmed influenza A(H1N1)2009 infection: two case-control studies, Spain, season 2009-2010 
BMC Public Health  2011;11:899.
Background
Physicians of the Spanish Influenza Sentinel Surveillance System report and systematically swab patients attended to their practices for influenza-like illness (ILI). Within the surveillance system, some Spanish regions also participated in an observational study aiming at estimating influenza vaccine effectiveness (cycEVA study). During the season 2009-2010, we estimated pandemic influenza vaccine effectiveness using both the influenza surveillance data and the cycEVA study.
Methods
We conducted two case-control studies using the test-negative design, between weeks 48/2009 and 8/2010 of the pandemic season. The surveillance-based study included all swabbed patients in the sentinel surveillance system. The cycEVA study included swabbed patients from seven Spanish regions. Cases were laboratory-confirmed pandemic influenza A(H1N1)2009. Controls were ILI patients testing negative for any type of influenza. Variables collected in both studies included demographic data, vaccination status, laboratory results, chronic conditions, and pregnancy. Additionally, cycEVA questionnaire collected data on previous influenza vaccination, smoking, functional status, hospitalisations, visits to the general practitioners, and obesity. We used logistic regression to calculate adjusted odds ratios (OR), computing pandemic influenza vaccine effectiveness as (1-OR)*100.
Results
We included 331 cases and 995 controls in the surveillance-based study and 85 cases and 351 controls in the cycEVA study. We detected nine (2.7%) and two (2.4%) vaccine failures in the surveillance-based and cycEVA studies, respectively. Adjusting for variables collected in surveillance database and swabbing month, pandemic influenza vaccine effectiveness was 62% (95% confidence interval (CI): -5; 87). The cycEVA vaccine effectiveness was 64% (95%CI: -225; 96) when adjusting for common variables with the surveillance system and 75% (95%CI: -293; 98) adjusting for all variables collected.
Conclusion
Point estimates of the pandemic influenza vaccine effectiveness suggested a protective effect of the pandemic vaccine against laboratory-confirmed influenza A(H1N1)2009 in the season 2009-2010. Both studies were limited by the low vaccine coverage and the late start of the vaccination campaign. Routine influenza surveillance provides reliable estimates and could be used for influenza vaccine effectiveness studies in future seasons taken into account the surveillance system limitations.
doi:10.1186/1471-2458-11-899
PMCID: PMC3262832  PMID: 22129083
19.  Assessing Google Flu Trends Performance in the United States during the 2009 Influenza Virus A (H1N1) Pandemic 
PLoS ONE  2011;6(8):e23610.
Background
Google Flu Trends (GFT) uses anonymized, aggregated internet search activity to provide near-real time estimates of influenza activity. GFT estimates have shown a strong correlation with official influenza surveillance data. The 2009 influenza virus A (H1N1) pandemic [pH1N1] provided the first opportunity to evaluate GFT during a non-seasonal influenza outbreak. In September 2009, an updated United States GFT model was developed using data from the beginning of pH1N1.
Methodology/Principal Findings
We evaluated the accuracy of each U.S. GFT model by comparing weekly estimates of ILI (influenza-like illness) activity with the U.S. Outpatient Influenza-like Illness Surveillance Network (ILINet). For each GFT model we calculated the correlation and RMSE (root mean square error) between model estimates and ILINet for four time periods: pre-H1N1, Summer H1N1, Winter H1N1, and H1N1 overall (Mar 2009–Dec 2009). We also compared the number of queries, query volume, and types of queries (e.g., influenza symptoms, influenza complications) in each model. Both models' estimates were highly correlated with ILINet pre-H1N1 and over the entire surveillance period, although the original model underestimated the magnitude of ILI activity during pH1N1. The updated model was more correlated with ILINet than the original model during Summer H1N1 (r = 0.95 and 0.29, respectively). The updated model included more search query terms than the original model, with more queries directly related to influenza infection, whereas the original model contained more queries related to influenza complications.
Conclusions
Internet search behavior changed during pH1N1, particularly in the categories “influenza complications” and “term for influenza.” The complications associated with pH1N1, the fact that pH1N1 began in the summer rather than winter, and changes in health-seeking behavior each may have played a part. Both GFT models performed well prior to and during pH1N1, although the updated model performed better during pH1N1, especially during the summer months.
doi:10.1371/journal.pone.0023610
PMCID: PMC3158788  PMID: 21886802
20.  Hand hygiene instruction decreases illness-related absenteeism in elementary schools: a prospective cohort study 
BMC Pediatrics  2012;12:52.
Background
Illness-related absences have been shown to lead to negative educational and economic outcomes. Both hand washing and hand sanitizer interventions have been shown to be effective in reducing illness-related absences. However, while the importance of hand hygiene in schools is clear, the role of instruction in use is less obvious. The purpose of this study was to compare absenteeism rates among elementary students given access to hand hygiene facilities versus students given both access and short repetitive instruction in use, particularly during influenza season when illness-related absences are at a peak.
Methods
A hand hygiene intervention was implemented from October to May during the 2009/2010 academic year, including peak flu season, in two Chicago Public Elementary Schools among students grades pre-kindergarten to eighth grade (ages 4–14). Classrooms were systematically assigned to an intervention or control group by grade (cluster design). Hand hygiene facilities (sanitizer and soap) were made available to all students. Students in the intervention group also received short repetitive instruction in hand hygiene every 2 months. Only absences as a result of respiratory or gastrointestinal illness were used to establish illness-related absenteeism rates. Percent absent days were calculated and bivariate analyses were performed to compare percent absent days among students given access to hand hygiene facilities versus students given both access and instruction. Prior to the intervention, teachers’ perceptions of students’ hand hygiene were also evaluated. Teacher perceptions were analysed to describe attitudes and beliefs.
Results
Data were collected and analysed for 773 students reporting 1,886 absences during the study period (1.73% of total school days). Both the percent total absent days and percent illness-related absent days were significantly lower in the group receiving short instruction during flu season (P = 0.002, P < 0.001, respectively). This difference peaked during the influenza season (when intervention began) and declined in the following months. Teachers (n = 23) agreed that hand hygiene is not performed properly among students and reported time constraints as a barrier to frequent hand washing.
Conclusions
Adding hand hygiene instruction to existing hand hygiene practices improved attendance at public elementary schools during the flu season. Standardized and brief repetitive instruction in hand hygiene holds potential to significantly reduce absenteeism.
doi:10.1186/1471-2431-12-52
PMCID: PMC3470997  PMID: 22587432
Hand hygiene; Education; Elementary school; Illness
21.  Evaluation of a school-based influenza surveillance system. 
Public Health Reports  1995;110(3):333-337.
Previous studies have suggested using school-based surveillance to monitor epidemic influenza-like illness in a community. Since the late 1970s, no studies have sought to evaluate this public health measure. The Boulder County Health Department developed, piloted, and implemented a school-based surveillance system beginning with the 1988-89 school year. After five seasons of surveillance, the school-based system was evaluated for sensitivity by comparing the epidemic curves from the school-based system with those of a preexisting communicable disease sentinel surveillance system. Additional attributes evaluated included acceptability, simplicity, timeliness, and overall usefulness. Comparisons of the overall epidemic patterns suggest a close correlation between the two measures for the influenza seasons 1988-89 through 1992-93. The school-based system closely followed the general rise, peak, and fall of epidemic influenza-like illness as measured by the preexisting sentinel system. Three of five epidemic peaks matched on the week of occurrence between the two surveillance systems; for the remaining seasons, 1989-90 and 1991-92, the school-based system peaked 1 week earlier than the sentinel system. The use of school-based surveillance has several positive attributes which suggests schools are an ideal setting for detecting influenza outbreaks, including the epidemiology of influenza which has shown children play an important role in the acquisition and spread of influenza-like illness. Student populations were accessible and easily monitored by absenteeism rates that required no diagnosis or invasive testing. All 44 schools within the school district readily participated in the surveillance of influenza.(ABSTRACT TRUNCATED AT 250 WORDS)
PMCID: PMC1382129  PMID: 7610226
22.  Cost-effectiveness of Sick Leave Policies for Health Care Workers with Influenza-like Illness, Brazil, 2009 
Emerging Infectious Diseases  2011;17(8):1421-1429.
TOC Summary: Seven-day leave was more costly and no more effective than 2 days plus reevaluation.
We describe the effect of influenza-like illness (ILI) during the outbreak of pandemic (H1N1) 2009 on health care worker (HCW) absenteeism and compare the effectiveness and cost of 2 sick leave policies for HCWs with suspected influenza. We assessed initial 2-day sick leaves plus reassessment until the HCW was asymptomatic (2-day + reassessment policy), and initial 7-day sick leaves (7-day policy). Sick leaves peaked in August 2009: 3% of the workforce received leave for ILI. Costs during May–October reached R$798,051.87 (≈US $443,362). The 7-day policy led to a higher monthly rate of sick leave days per 100 HCWs than did the 2-day + reassessment policy (8.72 vs. 3.47 days/100 HCWs; p<0.0001) and resulted in higher costs (US $609 vs. US $1,128 per HCW on leave). ILI affected HCW absenteeism. The 7-day policy was more costly and not more effective in preventing transmission to patients than the 2-day + reassessment policy.
doi:10.3201/eid1708.101546
PMCID: PMC3381579  PMID: 21801619
Influenza A virus; H1N1 subtype; pandemic (H1N1) 2009; sick leave; costs; cost analysis; health care workers; viruses; Brazil; influenza; research
23.  Strategy to Enhance Influenza Surveillance Worldwide1 
Emerging Infectious Diseases  2009;15(8):1271-1278.
Sentinel surveillance for severe acute respiratory infection and influenza-like illness is effective in resource-limited settings.
The emergence of a novel strain of influenza virus A (H1N1) in April 2009 focused attention on influenza surveillance capabilities worldwide. In consultations before the 2009 outbreak of influenza subtype H1N1, the World Health Organization had concluded that the world was unprepared to respond to an influenza pandemic, due in part to inadequate global surveillance and response capacity. We describe a sentinel surveillance system that could enhance the quality of influenza epidemiologic and laboratory data and strengthen a country’s capacity for seasonal, novel, and pandemic influenza detection and prevention. Such a system would 1) provide data for a better understanding of the epidemiology and extent of seasonal influenza, 2) provide a platform for the study of other acute febrile respiratory illnesses, 3) provide virus isolates for the development of vaccines, 4) inform local pandemic planning and vaccine policy, 5) monitor influenza epidemics and pandemics, and 6) provide infrastructure for an early warning system for outbreaks of new virus subtypes.
doi:10.3201/eid1508.081422
PMCID: PMC2815958  PMID: 19751590
influenza; human influenza influenza A virus; avian influenza; H5N1 subtype; sentinel surveillance; epidemiology; viruses; policy review
24.  Overview of the winter wave of 2009 pandemic influenza A(H1N1)v in Vojvodina, Serbia 
Croatian Medical Journal  2011;52(2):141-150.
Aim
To analyze the epidemiological data for pandemic influenza A(H1N1)v in the Autonomous Province of Vojvodina, Serbia, during the season of 2009/2010 and to assess whether including severe acute respiratory illness (SARI) hospitalization data to the surveillance system gives a more complete picture of the impact of influenza during the pandemic.
Methods
From September 2009 to September 2010, the Institute of Public Health of Vojvodina conducted sentinel surveillance of influenza-like illnesses and acute respiratory infections in all hospitalized patients with SARI and virological surveillance of population of Vojvodina according to the European Centers for Disease Control technical document.
Results
The pandemic influenza outbreak in the province started in October 2009 (week 44) in students who had returned from a school-organized trip to Prague, Bratislava, and Vienna. The highest incidence rate was 1090 per 100 000 inhabitants, found in the week 50. The most affected age group were children 5-14 years old. A total of 1591 patients with severe illness were admitted to regional hospitals, with a case fatality rate of 2%, representing a hospitalization rate of 78.3 per 100 000 inhabitants and a mortality rate of 1.6 per 100 000. Most frequently hospitalized were 15-19 years old patients, male patients, and patients with pneumonia (P < 0.001). The highest case fatality rate was found among patients with acute respiratory distress syndrome (P < 0.001). Nasal/throat swabs were obtained for polymerase chain reaction test from 315 hospitalized patients and 20 non-hospitalized patients, and 145 (46%) and 15 (75%) specimens, respectively, tested positive on A(H1N1)v.
Conclusion
Sentinel influenza-like illness and SARI surveillance, both followed with virological surveillance, seem to be the optimal method to monitor the full scope of the influenza pandemic (from mild to severe influenza) in Vojvodina.
doi:10.3325/cmj.2011.52.141
PMCID: PMC3081212  PMID: 21495196
25.  Characterizing the Epidemiology of the 2009 Influenza A/H1N1 Pandemic in Mexico 
PLoS Medicine  2011;8(5):e1000436.
Gerardo Chowell and colleagues address whether school closures and other social distancing strategies were successful in reducing pandemic flu transmission in Mexico by analyzing the age- and state-specific incidence of influenza morbidity and mortality in 32 Mexican states.
Background
Mexico's local and national authorities initiated an intense public health response during the early stages of the 2009 A/H1N1 pandemic. In this study we analyzed the epidemiological patterns of the pandemic during April–December 2009 in Mexico and evaluated the impact of nonmedical interventions, school cycles, and demographic factors on influenza transmission.
Methods and Findings
We used influenza surveillance data compiled by the Mexican Institute for Social Security, representing 40% of the population, to study patterns in influenza-like illness (ILIs) hospitalizations, deaths, and case-fatality rate by pandemic wave and geographical region. We also estimated the reproduction number (R) on the basis of the growth rate of daily cases, and used a transmission model to evaluate the effectiveness of mitigation strategies initiated during the spring pandemic wave. A total of 117,626 ILI cases were identified during April–December 2009, of which 30.6% were tested for influenza, and 23.3% were positive for the influenza A/H1N1 pandemic virus. A three-wave pandemic profile was identified, with an initial wave in April–May (Mexico City area), a second wave in June–July (southeastern states), and a geographically widespread third wave in August–December. The median age of laboratory confirmed ILI cases was ∼18 years overall and increased to ∼31 years during autumn (p<0.0001). The case-fatality ratio among ILI cases was 1.2% overall, and highest (5.5%) among people over 60 years. The regional R estimates were 1.8–2.1, 1.6–1.9, and 1.2–1.3 for the spring, summer, and fall waves, respectively. We estimate that the 18-day period of mandatory school closures and other social distancing measures implemented in the greater Mexico City area was associated with a 29%–37% reduction in influenza transmission in spring 2009. In addition, an increase in R was observed in late May and early June in the southeast states, after mandatory school suspension resumed and before summer vacation started. State-specific fall pandemic waves began 2–5 weeks after school reopened for the fall term, coinciding with an age shift in influenza cases.
Conclusions
We documented three spatially heterogeneous waves of the 2009 A/H1N1 pandemic virus in Mexico, which were characterized by a relatively young age distribution of cases. Our study highlights the importance of school cycles on the transmission dynamics of this pandemic influenza strain and suggests that school closure and other mitigation measures could be useful to mitigate future influenza pandemics.
Please see later in the article for the Editors' Summary
Editors' Summary
Background
From June 2009 to August 2010, the world was officially (according to specific World Health Organization [WHO] criteria—WHO phase 6 pandemic alert) in the grip of an Influenza A pandemic with a new strain of the H1N1 virus. The epidemic in Mexico, which had the second confirmed global case of H1N1 virus was first noted in early April 2009, when reports of respiratory hospitalizations and deaths among 62 young adults in Mexico alerted local health officials to the occurrence of atypical rates of respiratory illness. In line with its inter-institutional National Pandemic Influenza Preparedness and Response Plan, the Ministry of Health cancelled school attendance in the greater Mexico City area on April 24 and expanded these measures to the rest the country three days later. The Ministry of Health then implemented in Mexico City other “social distancing” strategies such as closing cinemas and restaurants and cancelling large public gatherings.
Why Was This Study Done?
School closures and other intense social distancing strategies can be very disruptive to the population, but as yet it is uncertain whether these measures were successful in reducing disease transmission. In addition, there have been no studies concentrating on recurrent pandemic waves in Mexico. So in this study the authors addressed these issues by analyzing the age- and state-specific incidence of influenza morbidity and mortality in 32 Mexican States and quantified the association between local influenza transmission rates, school cycles, and demographic factors.
What Did the Researchers Do and Find?
The researchers used the epidemiological surveillance system of the Mexican Institute for Social Security—a Mexican health system that covers private sector workers and their families, a group representative of the general population, that comprises roughly 40% of the Mexican population (107 million individuals), with a network of 1,099 primary health care units and 259 hospitals nationwide. Then the researchers compiled state- and age-specific time series of incident influenza-like illness and H1N1 influenza cases by day of symptom onset to analyze the geographic dissemination patterns of the pandemic across Mexico and defined three temporally distinct pandemic waves in 2009: spring (April 1–May 20), summer (May 21–August 1), and fall (August 2–December 31). The researchers then applied a mathematical model of influenza transmission to daily case data to assess the effectiveness of mandatory school closures and other social distancing measures implemented during April 24–May 11, in reducing influenza transmission rates.
The Mexican Institute for Social Security reported a total of 117,626 people with influenza-like illness from April 1 to December 31, 2009, of which 36,044 were laboratory tested (30.6%) and 27,440 (23.3%) were confirmed with H1N1 influenza. During this period, 1,370 people with influenza-like illness died of which 585 (1.5 per 100,000) were confirmed to have H1N1 influenza. The median age of people with laboratory confirmed influenza like illness (H1N1) was 18 years overall but increased to 31 years during the autumn wave. The overall case-fatality ratio among people with influenza like illness was 1.2%, but highest (5.5%) among people over 60 years. The researchers found that the 18-day period of mandatory school closures and other social distancing measures implemented in the greater Mexico City area was associated with a substantial (29%–37%) reduction in influenza transmission in spring 2009 but increased in late May and early June in the southeast states, after mandatory school suspension resumed and before summer vacation started. State-specific pandemic waves began 2–5 weeks after school reopened for the fall term, coinciding with an age shift in influenza cases.
What Do These Findings Mean?
These findings show that the age distribution of pandemic influenza morbidity was greater in younger age groups, while the risk of severe disease was skewed towards older age groups, and that there were substantial geographical variation in pandemic patterns across Mexico, in part related to population size. But most importantly, these findings support the effectiveness of early mitigation efforts including mandatory school closures and cancellation of large public gatherings, reinforcing the importance of school cycles in the transmission of pandemic influenza. This analysis increases understanding of the age and transmission patterns of the Mexican 2009 influenza pandemic at various geographic scales, which is crucial for designing more efficient public health interventions against future influenza pandemics.
Additional Information
Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1000436.
The World Health Organization provides information about the global response to the 2009 H1N1 pandemic
doi:10.1371/journal.pmed.1000436
PMCID: PMC3101203  PMID: 21629683

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