Background Despite high annual rates of influenza in children,influenza vaccines are given to children infrequently. We measuredthe disease burden of influenza in a large cohort of healthychildren in the Tennessee Medicaid program who were youngerthan 15 years of age.
Methods We determined the rates of hospitalization for acutecardiopulmonary conditions, outpatient visits, and courses ofantibiotics over a period of 19 consecutive years. Using thedifferences in the rates of these events when influenzaviruswas circulating and the rates from November through April whenthere was no influenza in the community, we calculated morbidityattributable to influenza. There was a total of 2,035,143 person-yearsof observation.
Results During periods when influenzavirus was circulating,the average number of hospitalizations for cardiopulmonary conditionsin excess of the expected number was 104 per 10,000 childrenper year for children younger than 6 months of age, 50 per 10,000per year for those 6 months to less than 12 months, 19 per 10,000per year for those 1 year to less than 3 years, 9 per 10,000per year for those 3 years to less than 5 years, and 4 per 10,000per year for those 5 years to less than 15 years. For every100 children, an annual average of 6 to 15 outpatient visitsand 3 to 9 courses of antibiotics were attributable to influenza.In winter, 10 to 30 percent of the excess number of coursesof antibiotics occurred during periods when influenzavirus wascirculating.
Conclusions Healthy children younger than one year of age arehospitalized for illness attributable to influenza at ratessimilar to those for adults at high risk for influenza. Therate of hospitalization decreases markedly with age. Influenzaaccounts for a substantial number of outpatient visits and coursesof antibiotics in children of all ages. (N Engl J Med 2000;342:225-31.)
Acute respiratory disease is the most common reason for outpatientvisits and hospitalizations among children in the United States.1The majority of these illnesses are precipitated by viral infection.Influenza is a common disease of childhood; during epidemics,the rates of attack may exceed 40 percent in preschool childrenand 30 percent in school-age children.2,3,4,5,6,7,8 Furthermore,children have an important role in the spread of influenza,because school-age children are the main channel through whichinfluenza is introduced into households.3,6,7
Influenza vaccines are given infrequently to healthy childrendespite the high rates of attack in children and despite theimportant role of children in the transmission of viruses. Oneobstacle to the use of vaccines is the perception that influenzais a benign disease in children. Data on mortality, commonlyused to estimate the effect of influenza in adults, are insensitiveindicators of the effect of influenza in children.9,10,11 Furthermore,the contribution of other respiratory viruses, such as respiratorysyncytial virus, to morbidity from acute cardiopulmonary conditionsis greater in children than adults.12,13 Despite these difficulties,population-based studies of influenza epidemics have reportedhigher than expected, or excess, numbers of hospitalizationsfor acute respiratory disease12,14 and outpatient visits amongchildren.15
The evidence that an investigational, intranasal, live attenuatedinfluenzavirus vaccine is safe, well tolerated, and effectivein healthy children increases the attractiveness of expandingthe coverage of influenza vaccines to include all children.16,17Whether such a change in policy is made depends on the degreeto which the vaccine is expected to reduce the severe and costlyoutcomes of the disease and to be cost effective. We undertooka study to evaluate the effect of influenza on children by assessinga wide spectrum of illnesses in a large cohort of healthy childrenover several influenza seasons.
Methods
Study Design
We performed a retrospective cohort study of healthy childrenyounger than 15 years of age to determine the rates of hospitalizationfor acute cardiopulmonary conditions, outpatient visits, andcourses of antibiotics over a period of 19 consecutive years.To calculate morbidity attributable to influenza, we used annualdifferences between the rates of these events when influenzaviruswas circulating and the rates of these events during wintermonths when there was no influenza in the community.
Sources of Data and Definitions of Seasons
Tennessee Medicaid files for 1973 through 1993 included datesof enrollment in Medicaid, demographic characteristics, andmedical services reimbursed by Medicaid, including dates ofmedical service received in the hospital or on an outpatientbasis, associated diagnoses and procedures, and detailed informationon prescriptions filled. We linked Medicaid files to birth certificates,from which we determined the date of birth and maternal characteristics,and to death certificates, which included the date of deathand coded underlying cause of death.18,19
We defined the influenza season as the period in each year ofthe study from November 1 through April 30 that included thedates of the first and last isolation of influenzavirus in middleTennessee as determined by surveillance in a Vanderbilt University–basedpediatric population.13 These seasons showed reasonable concordancewith the timing of excess numbers of deaths from pneumonia andinfluenza that were estimated for 11 cities in Tennessee andsurrounding states that participate in the Centers for DiseaseControl and Prevention 121 City Surveillance System.20 We definedthe peri-influenza season as the period each year from November1 through April 30 in which there was no influenza activity;the rates from this period served as the base-line values forthe analyses. Two of the 19 years studied (1978–1979 and1979–1980) were determined to have had no influenza season,because of low influenza activity (fewer than five viral isolates),so that all winter months constituted the peri-influenza season.
The peak season for the respiratory syncytial virus was definedas the period from the identification on or after November 1of the first of two consecutive isolates of respiratory syncytialvirus (identified within 30 days of each other) until the identificationbefore or on April 30 of the last of two consecutive isolates.We defined the summer season as the period each year from May1 through October 31.
Study Population
The study included children younger than 15 years of age whowere enrolled in Tennessee Medicaid at birth or for at leastone year. Since the number of children who were not white orblack was small, we excluded these children. Children enteredthe study on the first day after June 30, 1974, on which theymet criteria for enrollment and were followed until the developmentof a high-risk condition, loss of coverage by Medicaid, 15 yearsof age, death, or June 30, 1993.
Because our study was designed to evaluate healthy children,we used information from computerized Medicaid files and birth-certificaterecords to identify and exclude children at high risk for influenza-relatedcomplications. Children were determined to be at high risk ifthey were institutionalized or disabled, weighed less than 2500g at birth and were younger than one year (these children couldbe included after one year of age if they had no other high-riskcondition), or had been given a diagnosis or prescription medicationthat indicated a high-risk condition in the year before entryinto the study. High-risk conditions were considered to be congenitalheart disease and other selected cardiac conditions, bronchopulmonarydysplasia, hospitalization for respiratory conditions, asthma,cystic fibrosis, sickle cell disease, diabetes mellitus, infectionwith the human immunodeficiency virus, cancer, chronic use oforal corticosteroids, and chronic renal disease. The remainingchildren were considered to be at low risk for influenza-relatedcomplications and were the focus of our analysis.
We ascertained the following characteristics of the childrenin our study: age group (younger than 6 months, 6 months toless than 12 months, 1 year to less than 3 years, 3 years toless than 5 years, and 5 years to less than 15 years), sex,residence (urban [four largest cities in Tennessee], other standardmetropolitan statistical area, or rural), and race (black orwhite). The number of living siblings was obtained from thebirth certificates of children younger than three years of age.This variable was not included for older children.
Study Outcomes
Study outcomes were hospitalization for or death from pneumonia,influenza, acute respiratory conditions other than pneumoniaor influenza, nonacute respiratory conditions other than pneumoniaor influenza, and heart failure or myocarditis. Secondary outcomeswere the total number of outpatient visits and the number ofantibiotic prescriptions filled.
Statistical Analysis
Crude rates of hospitalization were calculated by dividing thenumber of hospitalizations for acute cardiopulmonary conditionsduring influenza seasons by the age-specific person-years duringinfluenza seasons; these rates were expressed per 10,000 person-years.Rates were similarly calculated for the peri-influenza season,the summer season, and all seasons combined. Differences betweenthese crude rates during influenza and peri-influenza seasonswere calculated as measures of risk attributable to influenza.
Standardized versions of these differences between rates, whichaccount for variation in hospitalization rates between yearsand between other strata, were calculated with the use of stratabased on age group, study year, race, and residence as wellas strata-specific differences in rates. The standardized rateof hospitalizations attributable to influenza was defined asthe weighted average of the strata-specific differences in rate,with use of the corresponding strata-specific person-years inall seasons combined as the weights.
The excess number of hospitalizations per 10,000 persons peryear was estimated separately in all strata by multiplying thestrata-specific differences in rate by the proportion of daysof the corresponding study years accounted for by the respectiveinfluenza season. Standardized estimates were calculated witha weighted average of strata-specific values, as was done forthe standardized differences in rate. The two years in whichthere was no influenza season were included in all calculations.We elected to include as stratifying variables study year, race,residence, and age group. The inclusion of the other variablesresulted in no change of more than 0.5 in any age-specific estimateof annual excess numbers of hospitalizations, and they weretherefore excluded. Confidence intervals were calculated aspreviously described.21
To estimate the overall excess rate of hospitalizations in winteras compared with summer, the excess rate of hospitalizationsin winter that were not associated with influenza was addedto the excess rate of hospitalizations attributable to influenzaand then standardized as described above, with use of a zeroweight when no excess rate of hospitalizations in winter wasobserved. Excess rates of hospitalizations in winter that wereattributable to factors other than influenza (e.g., other respiratoryviruses) were estimated with use of strata-specific differencesin rate between peri-influenza seasons and summer seasons. Theproportion of the overall rate of excess hospitalizations inwinter attributable to influenza was calculated for each agegroup. Rates, differences in rate, excess rates of events, andproportions of excess rates of hospitalizations in winter attributableto influenza were calculated similarly for outpatient visitsand courses of antibiotics.
We performed another analysis to assess the effect of respiratorysyncytial virus seasons on our results. We calculated crudeand standardized differences in rates by subtracting rates ofhospitalizations, outpatient visits, and courses of antibioticsduring peri-influenza seasons from rates during influenza seasons,exclud-ing all person-time and events during respiratory syncytialvirus seasons.
Results
Children at low risk for influenza-related complications accountedfor 91 percent of all children younger than 15 years of agewho were enrolled in the Tennessee Medicaid program, and theycontributed 2,035,143 person-years during the 19 years of thestudy. By definition, 50 percent of person-time occurred duringsummer seasons; 19 percent occurred during influenza seasons,and 31 percent during peri-influenza seasons. The mean durationof the influenza season was 63 days (range, 0 to 119), and themean duration of the peak season for respiratory syncytial viruswas 68 days (range, 6 to 125). The peak season for respiratorysyncytial virus overlapped the influenza season an average of27 days per year (range, 0 to 83) and occurred with a similarfrequency during the influenza and peri-influenza seasons.
The demographic characteristics of the children in the studyreflected those of children in the Medicaid population; 51 percentwere male, and 60 percent were black. The age distribution wasas follows: 6 percent were younger than 6 months, 4 percentwere 6 months to less than 12 months, 16 percent were 1 yearto less than 3 years, 15 percent were 3 years to less than 5years, and 59 percent were 5 years to less than 15 years. Therewere changes in the demographics of the study population overthe 19 years of study due to changes in Medicaid eligibilityrequirements. The total enrollment for children younger than15 years decreased slightly over the first nine years of thestudy and then increased steadily, with a more marked increasein younger children. The last seven years of the study constituted50 percent of the total person-years, ranging from 46 percentof total person-years in those 5 years to less than 15 yearsof age to 64 percent of total person-years in those youngerthan 6 months of age. In addition, the percentage of the populationmade up of blacks decreased from 69 percent in the first yearto 47 percent in the last.
We identified 46,690 hospitalizations for acute cardiopulmonaryconditions during the entire study period, 28 percent of whichoccurred during an influenza season. For all age groups, therates of hospitalization were higher during the influenza seasonthan during the peri-influenza season (Table 1). In all seasons,the rates of hospitalization were highest for children youngerthan six months of age, and rates decreased with increasingage. Using the rate of hospitalization during the peri-influenzaseason as the base-line rate of hospitalization in winter, wecalculated the rate of hospitalization attributable to influenzaby subtracting the hospitalization rate during the peri-influenzaseason from the hospitalization rate during the influenza season.After adjustment for the duration of each influenza season,these rates translated into average excess numbers of hospitalizationsfor acute cardiopulmonary conditions that ranged from 4 to 104per 10,000 children annually. Another analysis, in which allperson-time and events during respiratory syncytial virus seasonswere excluded, yielded similar results (Table 2).
Table 2. Rates of Hospitalization for Acute Cardiopulmonary Conditions Attributable to Influenza, with Person-Time and Events during Respiratory Syncytial Virus Seasons Excluded.
We identified 154 deaths from selected acute cardiopulmonaryconditions during the 19 years of the study; 87 deaths (56 percent)occurred among children younger than one year of age. For allages combined and for all years, the excess number of deathsfrom cardiopulmonary conditions was 0.077 per 10,000 children(95 percent confidence interval, 0.001 to 0.154).
Trends for secondary outcomes were similar to those for hospitalizationsfor acute cardiopulmonary conditions (Figure 1). The frequenciesof both outpatient visits and courses of antibiotics were higherduring the influenza season than the peri-influenza season forall age groups. The number of outpatient visits attributableto influenza-associated illness was highest in children 6 monthsto less than 12 months of age and ranged from 6 to 15 per 100children. The number of courses of antibiotics attributableto influenza-associated illness ranged from 3 to 9 per 100 children.An analysis in which respiratory syncytial virus seasons wereexcluded yielded similar results (data not shown).
Figure 1. Rates of Outpatient Visits and Courses of Antibiotics Attributable to the Treatment of Influenza, According to Age, during the Influenza and Peri-Influenza Seasons.
Panel A shows the average total age-specific numbers of outpatient visits per 100 person-years. Panel B shows the average total age-specific numbers of courses of antibiotics prescribed per 100 person-years. Panel C shows the average excess age-specific numbers of outpatient visits and courses of antibiotics per 100 children per year.
For children younger than three years of age, the rates of alloutcomes were consistently higher in winter than in summer.Among children younger than 6 months, 6 months to less than12 months of age, and 1 year to less than 3 years of age, influenzaaccounted for 19 percent, 18 percent, and 20 percent of theexcess number of hospitalizations in winter, respectively; 24percent, 23 percent, and 35 percent of the excess number ofoutpatient visits in winter; and 10 percent, 14 percent, and20 percent of the excess number of courses of antibiotics inwinter. Among older children, there was more variation in therates of hospitalization and outpatient visits, with no consistentexcess in winter. However, the number of antibiotic prescriptionsfilled for older children was consistently higher in winterthan in summer. The courses of antibiotics attributable to influenza-associatedillness accounted for 26 percent and 30 percent of the excessnumber of courses of antibiotics prescribed for children 3 yearsto less than 5 years of age and 5 years to less than 15 yearsof age, respectively, in winter.
Discussion
In this large, retrospective cohort study, we found that amonghealthy children younger than 15 years of age, there were excessnumbers of hospitalizations for acute cardiopulmonary conditions,excess numbers of outpatient visits, and excess numbers of antibioticprescriptions filled during the periods when influenzaviruswas circulating in the community between 1974 and 1993. Theseoutcomes were observed among children of all ages. Deaths wererare in these healthy children, and most deaths occurred inthose younger than one year of age. The estimate of the excessnumber of deaths due to influenza was 8 per million childrenyounger than 15 years of age (95 percent confidence interval,0.1 to 15 per million).
Excess rates of hospitalization for acute cardiopulmonary conditionsduring influenza season were most frequent in children youngerthan one year of age and were less frequent with increasingage. Although these results, from a group of children enrolledin Medicaid, may not be generalizable to other populations,two prior studies of excess rates of hospitalization in differentpopulations yielded similar estimates. In Houston, estimatedrates of hospitalization attributable to influenza ranged from51 to 160 per 10,000 children younger than 1 year of age, 26to 45 per 10,000 children 1 to 4 years of age, and 3 to 7 per10,000 children 5 to 19 years of age.12 In a large prepaid grouppractice, the excess rates of hospitalization of low-risk childrenduring two influenza seasons were 10 per 10,000 children youngerthan 4 years of age and 2 per 10,000 children 5 to 14 yearsof age.14
These findings argue for the designation of children youngerthan one year of age as being at high risk for influenza. Theexcess rate of hospitalization in this age group is similarto rates in adults for whom an influenzavirus vaccine is recommended.12,22,23,24An inactivated influenzavirus vaccine is poorly immunogenicin children younger than six months of age and is not approvedfor children in this age group. Likewise, investigational, monovalentlive attenuated influenzavirus vaccines were well toleratedbut not consistently immunogenic in small numbers of childrenyounger than six months of age.25,26 Until better vaccines areavailable, stronger recommendations should be considered forimmunizing family members of children younger than one yearof age. Further research is needed to determine whether broadeningthe coverage of the influenzavirus vaccine to include pregnantwomen will provide protection to the infant through the transferof maternal antibody.27,28
Our results indicate that the effect of influenza on childrenmay be underestimated when only inpatient morbidity is assessed.Children of all ages were more likely to receive outpatientmedical care and receive antibiotic prescriptions during aninfluenza season than at other times during the winter wheninfluenzavirus was not circulating in the community. Excessnumbers of outpatient visits ranged from 6 to 15 per 100 children.We evaluated excess numbers of antibiotic prescriptions as amore specific indicator of outpatient infections; these rangedfrom 3 to 9 per 100 children. Our data suggest that influenzaaccounts for up to 35 percent of the excess number of outpatientvisits in winter in children younger than 3 years of age and10 to 30 percent of the excess use of antibiotics in winterin children younger than 15 years of age.
Increased use of an influenzavirus vaccine in healthy childrencould reduce the number of outpatient visits and the use ofantibiotics during winter months. Randomized, controlled trialshave demonstrated that both inactivated and cold-adapted influenzavirusvaccines prevent influenza-like illness in children.16,17 Intwo randomized, placebo-controlled studies, children youngerthan three years of age who received inactivated influenzavirusvaccine had a 31 to 36 percent lower incidence of acute otitismedia during subsequent influenza A epidemics than childrenwho were not vaccinated.29,30 A cold-adapted, trivalent intranasalinfluenzavirus vaccine reduced the incidence of febrile otitismedia by 30 percent and the incidence of any febrile illnesswith concomitant use of antibiotics by 29 percent in children15 to 71 months old.17
The main strengths of our study were the large number of childrenin a well-defined population, the use of more than one outcome,and the length of the study period. Previously published prospectivestudies, which used active virologic surveillance to defineinfluenza-associated outcomes, involved small numbers of childrenover a limited number of influenza seasons or were hospital-based.Morbidity from influenza varies markedly from season to season,9,12,22,31and the severity of any given season cannot be predicted inadvance. Thus, recommendations regarding influenza immunizationshould consider morbidity over a period of several years.
A potential confounding factor in this observational study isthe contribution of other respiratory viruses, particularlyrespiratory syncytial virus, to the morbidity among the childrenin our cohort. The effect of respiratory syncytial virus ismost problematic in younger children, in whom it is thoughtto cause the greatest morbidity.13,32,33,34,35
Three lines of evidence suggest that respiratory syncytial viruswas not a serious confounder. First, the analysis in which respiratorysyncytial virus seasons were excluded yielded similar results.Second, influenza accounted for 20 percent of the excess numberof hospitalizations in winter in the children less than threeyears old, which is consistent with the finding that respiratorysyncytial virus, not influenza, is the most frequent cause oflower respiratory tract disease that leads to hospitalizationin infants and young children.13,32,33,34,35 Third, our estimatesare corroborated by the findings of a 20-year hospital-basedstudy in which 10 to 36 percent of children younger than sixyears of age who were hospitalized with respiratory illnessduring the peak month of influenza season had laboratory-confirmedinfluenzavirus infection.31 Other respiratory viruses that causemorbidity in young children, such as parainfluenza viruses,may be less likely to occur when influenzavirus is circulatingin the community.32,36 If these viruses contribute to morbidityduring the peri-influenza season, our analysis may have underestimatedthe effect of influenza.
The cost, inconvenience, and safety of yearly immunization mustbe considered before expanded strategies for immunization canbe recommended. Our study of excess numbers of hospitalizations,outpatient visits, and courses of antibiotics quantifies aneffect of influenza on healthy children and suggests that theincreased use of influenza vaccines in this population couldhave substantial benefits. Strategies designed to control epidemicsof influenza must also focus on healthy schoolchildren and childrenin day care because of their role in the transmission of disease.3,6
Supported in part by a cooperative agreement with the Centersfor Disease Control and Prevention (U50/CCU41398-01).
We are indebted to Juliette Thompson and Sharon Tollefson fortheir role in influenzavirus surveillance; to Drs. Edgar K.Marcuse and Thomas G. Boyce for helpful suggestions on the manuscript;and to Cindy Naron for editorial assistance.
Source Information
From the Department of Medicine, University of Washington School of Medicine, and the Department of Veterans Affairs, Puget Sound Health Care System — both in Seattle (K.M.N.); and the Departments of Preventive Medicine (B.G.M., E.F.M., M.R.G.), Pediatrics (P.F.W.), and Medicine (M.R.G.), Vanderbilt University School of Medicine, Nashville.
Address reprint requests to Dr. Neuzil at the Department of Veterans Affairs, Puget Sound Health Care System, Division of Infectious Diseases 111, 1660 S. Columbian Way, Seattle, WA 98108-1595, or at kneuzil{at}u.washington.edu.
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Shinall, M. C. Jr, Plosa, E. J., Poehling, K. A.
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Lambert, S. B., Allen, K. M., Druce, J. D., Birch, C. J., Mackay, I. M., Carlin, J. B., Carapetis, J. R., Sloots, T. P., Nissen, M. D., Nolan, T. M.
(2007). Community Epidemiology of Human Metapneumovirus, Human Coronavirus NL63, and Other Respiratory Viruses in Healthy Preschool-Aged Children Using Parent-Collected Specimens. Pediatrics
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Lewis, E. N., Griffin, M. R., Szilagyi, P. G., Zhu, Y., Edwards, K. M., Poehling, K. A.
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(2007). Trivalent Live Attenuated Intranasal Influenza Vaccine Administered During the 2003 2004 Influenza Type A (H3N2) Outbreak Provided Immediate, Direct, and Indirect Protection in Children. Pediatrics
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(2007). Misperceptions About Influenza Vaccination Among Parents of Healthy Young Children. CLIN PEDIATR
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Chiu, S. S., Peiris, J.S. M., Chan, K. H., Wong, W. H. S., Lau, Y. L.
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(2007). Prevention of Influenza Episodes With Colostrum Compared With Vaccination in Healthy and High-Risk Cardiovascular Subjects: The Epidemiologic Study in San Valentino. CLIN APPL THROMB HEMOST
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Coffin, S. E., Zaoutis, T. E., Rosenquist, A. B. W., Heydon, K., Herrera, G., Bridges, C. B., Watson, B., Localio, R., Hodinka, R. L., Keren, R.
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Committee on Infectious Diseases,
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Verani, J. R., Irigoyen, M., Chen, S., Chimkin, F.
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Shuler, C. M., Iwamoto, M., Bridges, C. B., Marin, M., Neeman, R., Gargiullo, P., Yoder, T. A., Keyserling, H. L., Terebuh, P. D.
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Dodds, L., McNeil, S. A., Fell, D. B., Allen, V. M., Coombs, A., Scott, J., MacDonald, N.
(2007). Impact of influenza exposure on rates of hospital admissions and physician visits because of respiratory illness among pregnant women. CMAJ
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Grijalva, C. G., Poehling, K. A., Edwards, K. M., Weinberg, G. A., Staat, M. A., Iwane, M. K., Schaffner, W., Griffin, M. R.
(2007). Accuracy and Interpretation of Rapid Influenza Tests in Children. Pediatrics
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France, E. K., Smith-Ray, R., McClure, D., Hambidge, S., Xu, S., Yamasaki, K., Shay, D., Weintraub, E., Fry, A. M., Black, S. B., Shinefield, H. R., Mullooly, J. P., Jackson, L. A., for the Vaccine Safety Datalink Team,
(2006). Impact of Maternal Influenza Vaccination During Pregnancy on the Incidence of Acute Respiratory Illness Visits Among Infants. Arch Pediatr Adolesc Med
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Vesikari, T., Fleming, D. M., Aristegui, J. F., Vertruyen, A., Ashkenazi, S., Rappaport, R., Skinner, J., Saville, M. K., Gruber, W. C., Forrest, B. D., for the CAIV-T Pediatric Day Care Clinical Trial N,
(2006). Safety, Efficacy, and Effectiveness of Cold-Adapted Influenza Vaccine-Trivalent Against Community-Acquired, Culture-Confirmed Influenza in Young Children Attending Day Care. Pediatrics
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Ampofo, K., Gesteland, P. H., Bender, J., Mills, M., Daly, J., Samore, M., Byington, C., Pavia, A. T., Srivastava, R.
(2006). Epidemiology, Complications, and Cost of Hospitalization in Children With Laboratory-Confirmed Influenza Infection. Pediatrics
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Pelletier, A. J., Mansbach, J. M., Camargo, C. A. Jr
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Zimmerman, R. K., Hoberman, A., Nowalk, M. P., Lin, C. J., Greenberg, D. P., Weinberg, S. T., Ko, F. S., Fox, D. E.
(2006). Improving Influenza Vaccination Rates of High-Risk Inner-City Children Over 2 Intervention Years. Ann Fam Med
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Jackson, L. A., Neuzil, K. M., Baggs, J., Davis, R. L., Black, S., Yamasaki, K. M., Belongia, E., Zangwill, K. M., Mullooly, J., Nordin, J., Marcy, S. M., DeStefano, F.
(2006). Compliance With the Recommendations for 2 Doses of Trivalent Inactivated Influenza Vaccine in Children Less Than 9 Years of Age Receiving Influenza Vaccine for the First Time: A Vaccine Safety Datalink Study. Pediatrics
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Keren, R., Zaoutis, T. E., Saddlemire, S., Luan, X. Q., Coffin, S. E.
(2006). Direct Medical Cost of Influenza-Related Hospitalizations in Children. Pediatrics
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Hambidge, S. J., Glanz, J. M., France, E. K., McClure, D., Xu, S., Yamasaki, K., Jackson, L., Mullooly, J. P., Zangwill, K. M., Marcy, S. M., Black, S. B., Lewis, E. M., Shinefield, H. R., Belongia, E., Nordin, J., Chen, R. T., Shay, D. K., Davis, R. L., DeStefano, F., for the Vaccine Safety Datalink Team,
(2006). Safety of Trivalent Inactivated Influenza Vaccine in Children 6 to 23 Months Old. JAMA
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Santibanez, T. A., Santoli, J. M., Bridges, C. B., Euler, G. L.
(2006). Influenza Vaccination Coverage of Children Aged 6 to 23 Months: The 2002-2003 and 2003-2004 Influenza Seasons. Pediatrics
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Walter, E. B., Neuzil, K. M., Zhu, Y., Fairchok, M. P., Gagliano, M. E., Monto, A. S., Englund, J. A.
(2006). Influenza Vaccine Immunogenicity in 6- to 23-Month-Old Children: Are Identical Antigens Necessary for Priming?. Pediatrics
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Englund, J. A., Walter, E. B., Gbadebo, A., Monto, A. S., Zhu, Y., Neuzil, K. M.
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Moore, D. L., Vaudry, W., Scheifele, D. W., Halperin, S. A., Dery, P., Ford-Jones, E., Arishi, H. M., Law, B. J., Lebel, M., Le Saux, N., Grimsrud, K., Tam, T.
(2006). Surveillance for Influenza Admissions Among Children Hospitalized in Canadian Immunization Monitoring Program Active Centers, 2003-2004. Pediatrics
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Naleway, A. L., Smith, W. J., Mullooly, J. P.
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Poehling, K. A., Edwards, K. M., Weinberg, G. A., Szilagyi, P., Staat, M. A., Iwane, M. K., Bridges, C. B., Grijalva, C. G., Zhu, Y., Bernstein, D. I., Herrera, G., Erdman, D., Hall, C. B., Seither, R., Griffin, M. R., the New Vaccine Surveillance Network,
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Poehling, K. A., Zhu, Y., Tang, Y.-W., Edwards, K.
(2006). Accuracy and Impact of a Point-of-Care Rapid Influenza Test in Young Children With Respiratory Illnesses. Arch Pediatr Adolesc Med
160: 713-718
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Bourgeois, F. T., Valim, C., Wei, J. C., McAdam, A. J., Mandl, K. D.
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Stephenson, I., Democratis, J.
(2006). Influenza: current threat from avian influenza. Br Med Bull
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Louie, J. K., Schechter, R., Honarmand, S., Guevara, H. F., Shoemaker, T. R., Madrigal, N. Y., Woodfill, C. J.I., Backer, H. D., Glaser, C. A.
(2006). Severe Pediatric Influenza in California, 2003-2005: Implications for Immunization Recommendations. Pediatrics
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Ma, K.K., Schaffner, W., Colmenares, C., Howser, J., Jones, J., Poehling, K.A.
(2006). Influenza Vaccinations of Young Children Increased With Media Coverage in 2003. Pediatrics
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Daley, M. F., Crane, L. A., Chandramouli, V., Beaty, B. L., Barrow, J., Allred, N., Berman, S., Kempe, A.
(2006). Influenza Among Healthy Young Children: Changes in Parental Attitudes and Predictors of Immunization During the 2003 to 2004 Influenza Season. Pediatrics
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Beard, F, McIntyre, P, Gidding, H, Watson, M
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Bhat, N., Wright, J. G., Broder, K. R., Murray, E. L., Greenberg, M. E., Glover, M. J., Likos, A. M., Posey, D. L., Klimov, A., Lindstrom, S. E., Balish, A., Medina, M.-j., Wallis, T. R., Guarner, J., Paddock, C. D., Shieh, W.-J., Zaki, S. R., Sejvar, J. J., Shay, D. K., Harper, S. A., Cox, N. J., Fukuda, K., Uyeki, T. M., the Influenza Special Investigations Team,
(2005). Influenza-Associated Deaths among Children in the United States, 2003-2004. NEJM
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Neuzil, K. M., Griffin, M. R.
(2005). Vaccine Safety--Achieving the Proper Balance. JAMA
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Keren, R., Zaoutis, T. E., Bridges, C. B., Herrera, G., Watson, B. M., Wheeler, A. B., Licht, D. J., Luan, X. Q., Coffin, S. E.
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Rothberg, M. B., Fisher, D., Kelly, B., Rose, D. N.
(2005). Management of Influenza Symptoms in Healthy Children: Cost-effectiveness of Rapid Testing and Antiviral Therapy. Arch Pediatr Adolesc Med
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Brownstein, J. S., Kleinman, K. P., Mandl, K. D.
(2005). Identifying Pediatric Age Groups for Influenza Vaccination Using a Real-Time Regional Surveillance System. Am J Epidemiol
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Piedra, P. A., Gaglani, M. J., Riggs, M., Herschler, G., Fewlass, C., Watts, M., Kozinetz, C., Hessel, C., Glezen, W. P.
(2005). Live Attenuated Influenza Vaccine, Trivalent, Is Safe in Healthy Children 18 Months to 4 Years, 5 to 9 Years, and 10 to 18 Years of Age in a Community-Based, Nonrandomized, Open-Label Trial. Pediatrics
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Ritzwoller, D. P., Bridges, C. B., Shetterly, S., Yamasaki, K., Kolczak, M., France, E. K.
(2005). Effectiveness of the 2003-2004 Influenza Vaccine Among Children 6 Months to 8 Years of Age, With 1 vs 2 Doses. Pediatrics
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Teo, S S S, Nguyen-Van-Tam, J S, Booy, R
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Englund, J. A., Walter, E. B., Fairchok, M. P., Monto, A. S., Neuzil, K. M.
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Humiston, S. G., Lerner, E. B., Hepworth, E., Blythe, T., Goepp, J. G.
(2005). Parent Opinions About Universal Influenza Vaccination for Infants and Toddlers. Arch Pediatr Adolesc Med
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Kempe, A., Daley, M. F., Barrow, J., Allred, N., Hester, N., Beaty, B. L., Crane, L. A., Pearson, K., Berman, S.
(2005). Implementation of Universal Influenza Immunization Recommendations for Healthy Young Children: Results of a Randomized, Controlled Trial With Registry-Based Recall. Pediatrics
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Langley, J. M., Faughnan, M. E., The Canadian Task Force on Preventive Health Care,
(2004). Prevention of influenza in the general population: recommendation statement from the Canadian Task Force on Preventive Health Care. CMAJ
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Langley, J. M., Faughnan, M. E.
(2004). Prevention of influenza in the general population. CMAJ
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France, E. K., Glanz, J. M., Xu, S., Davis, R. L., Black, S. B., Shinefield, H. R., Zangwill, K. M., Marcy, S. M., Mullooly, J. P., Jackson, L. A., Chen, R.
(2004). Safety of the Trivalent Inactivated Influenza Vaccine Among Children: A Population-Based Study. Arch Pediatr Adolesc Med
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Pappano, D., Humiston, S., Goepp, J.
(2004). Efficacy of a Pediatric Emergency Department-Based Influenza Vaccination Program. Arch Pediatr Adolesc Med
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Principi, N, Esposito, S, Gasparini, R, Marchisio, P, Crovari, P, for the Flu-Flu Study Group*,
(2004). Burden of influenza in healthy children and their households. Arch. Dis. Child.
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Hemingway, C. O., Poehling, K. A.
(2004). Change in Recommendation Affects Influenza Vaccinations Among Children 6 to 59 Months of Age. Pediatrics
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Thompson, W. W., Shay, D. K., Weintraub, E., Brammer, L., Bridges, C. B., Cox, N. J., Fukuda, K.
(2004). Influenza-Associated Hospitalizations in the United States. JAMA
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Humiston, S. G., Szilagyi, P. G., Iwane, M. K., Schaffer, S. J., Santoli, J., Shone, L., Barth, R., McInerny, T., Schwartz, B.
(2004). The Feasibility of Universal Influenza Vaccination for Infants and Toddlers. Arch Pediatr Adolesc Med
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Poehling, K. A., Lafleur, B. J., Szilagyi, P. G., Edwards, K. M., Mitchel, E., Barth, R., Schwartz, B., Griffin, M. R.
(2004). Population-Based Impact of Pneumococcal Conjugate Vaccine in Young Children. Pediatrics
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Baydur, A.
(2004). Influenza Vaccination in Vulnerable Populations. Chest
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Iwane, M. K., Edwards, K. M., Szilagyi, P. G., Walker, F. J., Griffin, M. R., Weinberg, G. A., Coulen, C., Poehling, K. A., Shone, L. P., Balter, S., Hall, C. B., Erdman, D. D., Wooten, K., Schwartz, B., for the New Vaccine Surveillance Network,
(2004). Population-Based Surveillance for Hospitalizations Associated With Respiratory Syncytial Virus, Influenza Virus, and Parainfluenza Viruses Among Young Children. Pediatrics
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Meissner, H. C., Rennels, M. B.
(2004). Unpredictable Patterns of Viral Respiratory Disease in Children. Pediatrics
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Committee on Infectious Diseases,
(2004). Recommendations for Influenza Immunization of Children. Pediatrics
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Frisbie, B., Tang, Y.-W., Griffin, M., Poehling, K., Wright, P. F., Holland, K., Edwards, K. M.
(2004). Surveillance of Childhood Influenza Virus Infection: What Is the Best Diagnostic Method To Use for Archival Samples?. J. Clin. Microbiol.
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O'Brien, M. A., Uyeki, T. M., Shay, D. K., Thompson, W. W., Kleinman, K., McAdam, A., Yu, X.-J., Platt, R., Lieu, T. A.
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Gaglani, M. J., Herschler, G. B.
(2004). Every Nose Counts: A New Influenza Vaccine for All Healthy Schoolchildren?. CLIN PEDIATR
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Gaglani, M. J., Piedra, P. A., Herschler, G. B., Griffith, M. E., Kozinetz, C. A., Riggs, M. W., Fewlass, C., Halloran, M. E., Longini, I. M. Jr, Glezen, W. P.
(2004). Direct and Total Effectiveness of the Intranasal, Live-Attenuated, Trivalent Cold-Adapted Influenza Virus Vaccine Against the 2000-2001 Influenza A(H1N1) and B Epidemic in Healthy Children. Arch Pediatr Adolesc Med
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Daley, M. F., Barrow, J., Pearson, K., Crane, L. A., Gao, D., Stevenson, J. M., Berman, S., Kempe, A.
(2004). Identification and Recall of Children With Chronic Medical Conditions for Influenza Vaccination. Pediatrics
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Szilagyi, P. G., Iwane, M. K., Schaffer, S., Humiston, S. G., Barth, R., McInerny, T., Shone, L., Schwartz, B.
(2003). Potential Burden of Universal Influenza Vaccination of Young Children on Visits to Primary Care Practices. Pediatrics
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Hoberman, A., Greenberg, D. P., Paradise, J. L., Rockette, H. E., Lave, J. R., Kearney, D. H., Colborn, D. K., Kurs-Lasky, M., Haralam, M. A., Byers, C. J., Zoffel, L. M., Fabian, I. A., Bernard, B. S., Kerr, J. D.
(2003). Effectiveness of Inactivated Influenza Vaccine in Preventing Acute Otitis Media in Young Children: A Randomized Controlled Trial. JAMA
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Quach, C., Piche-Walker, L., Platt, R., Moore, D.
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van Woensel, J B M, van Aalderen, W M C, Kimpen, J L L
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Harnden, A., Brueggemann, A., Shepperd, S., White, J., Hayward, A. C, Zambon, M., Crook, D., Mant, D.
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Szilagyi, P. G., Iwane, M. K., Humiston, S. E., Schaffer, S., McInerny, T., Shone, L., Jennings, J., Washington, M. L., Schwartz, B.
(2003). Time Spent by Primary Care Practices on Pediatric Influenza Vaccination Visits: Implications for Universal Influenza Vaccination. Arch Pediatr Adolesc Med
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Grant, V. J., Le Saux, N., Plint, A. C., Correll, R., Gaboury, I., Ellis, E., Tam, T. W.S.
(2003). Factors influencing childhood influenza immunization. CMAJ
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Aoki, F. Y., Macleod, M. D., Paggiaro, P., Carewicz, O., El Sawy, A., Wat, C., Griffiths, M., Waalberg, E., Ward, P., on behalf of the IMPACT Study Group,
(2003). Early administration of oral oseltamivir increases the benefits of influenza treatment. J Antimicrob Chemother
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Chiu, S. S., Lau, Y. L., Chan, K. H., Wong, W. H. S., Peiris, J.S. M.
(2002). Influenza-Related Hospitalizations among Children in Hong Kong. NEJM
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Griffin, M. R., Neuzil, K. M.
(2002). The Global Implications of Influenza in Hong Kong. NEJM
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Byington, C. L., Castillo, H., Gerber, K., Daly, J. A., Brimley, L. A., Adams, S., Christenson, J. C., Pavia, A. T.
(2002). The Effect of Rapid Respiratory Viral Diagnostic Testing on Antibiotic Use in a Children's Hospital. Arch Pediatr Adolesc Med
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