Respiratory Syncytial Virus
–
Associated Hospitalizations
Among Children Less Than 24 Months of Age
WHAT’S KNOWN ON THIS SUBJECT: Respiratory syncytial virus (RSV) infection is a leading cause of hospitalization among infants. Most estimates of RSV hospitalization rates are imprecise, having been calculated by using retrospective discharge diagnosis data and stratified age groups no narrower than 6 to 12 months.
WHAT THIS STUDY ADDS: Prospective, population-based surveillance data for infants hospitalized with laboratory-confirmed RSV infection were combined with birth certificate information to yield more precise age-specific hospitalization rates. These data should help determine priorities for the use of existing and future RSV prophylaxis strategies.
abstract
BACKGROUND:Respiratory syncytial virus (RSV) infection is a leading cause of hospitalization among infants. However, estimates of the RSV hospitalization burden have varied, and precision has been limited by the use of age strata grouped in blocks of 6 to$12 months.
METHODS:We analyzed data from a 5-year, prospective, population-based surveillance for young children who were hospitalized with laboratory-confirmed (reverse-transcriptase polymerase chain reaction) RSV acute respiratory illness (ARI) during October through March 2000– 2005. The total population at risk was stratified by month of age by birth certificate information to yield hospitalization rates.
RESULTS:There were 559 (26%) RSV-infected children among the 2149 enrolled children hospitalized with ARI (85% of all eligible children with ARI). The average RSV hospitalization rate was 5.2 per 1000 children,24 months old. The highest age-specific rate was in infants 1 month old (25.9 per 1000 children). Infants#2 months of age, who comprised 44% of RSV-hospitalized children, had a hospitalization rate of 17.9 per 1000 children. Most children (79%) were previously healthy. Very preterm infants (,30 weeks’ gestation) accounted for only 3% of RSV cases but had RSV hospitalization rates 3 times that of term infants.
CONCLUSIONS:Young infants, especially those who were 1 month old, were at greatest risk of RSV hospitalization. Four-fifths of RSV-hospitalized infants were previously healthy. To substantially reduce the burden of RSV hospitalizations, effective general preventive strategies will be required for all young infants, not just those with risk factors.Pediatrics2013;132:e341–e348
AUTHORS:Caroline Breese Hall, MD,a,bGeoffrey A.
Weinberg, MD,aAaron K. Blumkin, MS,aKathryn M.
Edwards, MD,cMary A. Staat, MD, MPH,dAndrew F. Schultz,
MS,bKatherine A. Poehling, MD,e,fPeter G. Szilagyi, MD,a
Marie R. Griffin, MD, MPH,g,hJohn V. Williams, MD,c,iYuwei
Zhu, MD, MS,jCarlos G. Grijalva, MD, MPH,hMila M. Prill,
MSPH,kand Marika K. Iwane, PhD, MPHk
Departments ofaPediatrics andbMedicine, University of
Rochester School of Medicine and Dentistry, Rochester, New York; Departments ofcPediatrics,gMedicine,hPreventive Medicine, iPathology, Microbiology, and Immunology, andjBiostatistics,
Vanderbilt University Medical Center, Nashville, Tennessee;
dDepartment of Pediatrics, University of Cincinnati College of
Medicine, Cincinnati, Ohio; Departments ofePediatrics and
fEpidemiology and Prevention, Wake Forest School of Medicine,
Winston-Salem, North Carolina; andkNational Center for
Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
KEY WORDS
respiratory syncytial virus, acute respiratory illness
ABBREVIATIONS
ARI—acute respiratory illness CI—confidence interval
ICD-9-CM—International Classification of Diseases, Ninth Revi-sion, Clinical Modification
IRR—incidence rate ratio RSV—respiratory syncytial virus
(Continued on last page)
of hospitalization among infants.1–6
Accurate assessment of the burden of RSV hospitalizations, therefore, is es-sential in determining priorities for the use of existing RSV prophylaxis and future vaccines. However, estimates of the burden of RSV hospitalizations in the United States have varied.
Retrospective analyses using national databases and International Classifi -cation of Diseases, Ninth Revision, Clinical Modification(ICD-9-CM)–coded discharge diagnoses to determine RSV hospitalizations have estimated annual hospitalization rates of 30 to 50 per 1000 infants,6 months old, 11 to 15 per 1000 infants 6 to,12 months old, and 15 to 26 per 1000 infants ,12 months old.1–6 However, substantially
lower rates, approximately one-half lower, are reported by the few avail-able prospective, population-based studies of laboratory-confirmed cases.7,8
Our goal, therefore, was to more ac-curately define and characterize RSV hospitalizations among children ,24 months old, the group at greatest risk of severe RSV illness. We used pro-spective, population-based surveillance data for laboratory-confirmed RSV hos-pitalizations over a 5-year period and verified the denominator-based data by reviewing birth certificates to provide monthly age strata.
METHODS
Study Design
We previously described the clinical burden of inpatient and outpatient RSV infections among children,5 years old during the 4 respiratory seasons of 2000–2001 through 2003–2004 using census data for the denominators of the at-risk population.7 The current 5-year
study includes the subset of inpatients ,24 months old from the respiratory seasons (October through March each year) reported in that study but includes
–
season. Importantly, the denomi-nators of the at-risk population in this report were defined more precisely (by each month of age) by reviewing birth certificate data for the studied cohorts. Children with RSV infection were pro-spectively identified by surveillance for laboratory-confirmed RSV infections through the New Vaccine Surveillance Network, as previously described.7–10
Viral surveillance was conducted from October through March during the years 2000 through 2005 in counties sur-rounding Nashville, Tennessee (Davidson County), and Rochester, New York (Monroe County), and during 2003–2005 in Cincin-nati, Ohio (Hamilton County). During the respiratory seasons, children with acute respiratory illness (ARI) were enrolled 4 to 7 days per week, as previously described.7–10 Surveillance
hospitals admitted .95% of each county’s children.
Eligible children were county residents ,24 months old with an ARI defined as acute illness onset with$1 of the fol-lowing: fever or respiratory tract signs, including cough, earache, nasal con-gestion, rhinorrhea, wheezing, or rapid or labored respirations.8
Institutional review board approvals were obtained from the Centers for Disease Control and Prevention and from each study site’s institution; informed consent for enrollment of all children was ob-tained from a parent or legal guardian.
Patient and Laboratory Data
The child’s gender, race, gestational age at birth, presence of other children in the home, and palivizumab administra-tion were obtained from parental or guardian interviews. Comorbid con-ditions (chronic pulmonary, cardiac, kidney, or neurologic diseases or im-munodeficiency, cancer, or sickle cell anemia) and insurance information were determined by medical record
performed in duplicate by reverse-transcriptase polymerase chain re-action was RSV-positive.7–10
Birth Certificate Data
The monthly denominator of live births for chronologic and gestational ages, maternal race, and gender was calcu-lated from each county’s birth certifi -cates, and age cohorts were determined. Children with gestational ages of ,30 weeks were defined as very preterm, 30 to 33 weeks as early preterm, 34 to 36 weeks as late preterm, and$37 weeks as term.11
Data Analysis x2
Tests compared the frequencies of characteristics of inpatients with RSV-positive and RSV-negative ARIs.
Monthly incidence rates of RSV hospi-talizations were calculated by dividing the weighted number of RSV cases, accounting for both the number of eli-gible children enrolled and surveillance days, by the total number of children within each birth cohort. Seasonal av-erage monthly incidences were calcu-lated by combining the birth cohorts using direct standardization. The cu-mulative seasonal incidence rate was the summed monthly rates.
Population-based hospitalization rates were calculated for subgroups as
de-fined by birth certificate information, as well as rates by county, age, and month of admission. Subgroups were com-pared by using incidence rate ratios (IRRs). To describe the variability around the rates and rate ratios, bias-corrected bootstrap 95% confidence intervals (CIs) were calculated from 10 000 replications, and bootstrapped SEs were used to determinePvalues.
RESULTS
Patient Population
Of 132 085 children born in the sur-veillance area during the study period, 2539 had an ARI hospitalization before reaching 24 months of age during the surveillance period and were eligible for inclusion. Of these, 2149 (85%) were enrolled, and 559 (26%) enrolled chil-dren had laboratory-confirmed RSV infection. The major reasons for non-enrollment were parental refusal (46%) or unavailability (30%) or dis-charge before enrollment (15%). Less than 1% of the children’s physicians declined participation.
The characteristics of children hospi-talized with RSV-positive ARIs were similar to those with ARIs from other causes, except a higher proportions of RSV-infected children were ,12 months old and were white (Table 1).
The mean overall RSV season duration from thefirst to the last RSV-positive sample for all years and sites was 28 weeks. For Davidson, Monroe, and Hamilton Counties, it was 30, 26, and 28 weeks, respectively. However, nearly 80% of RSV infections occurred over 14 weeks beginning in early December.
Average Seasonal RSV Hospitalization Rates Among Subsets of Young Children
The average rate of RSV admissions over the 6-month respiratory season was 5.2 per 1000 (95% CI: 4.8–5.7) children,24 months old, with signifi -cant seasonal variation from 2.5 to 9.9 per 1000 children (P , .01; data not shown). One-month-old infants had the highest average hospitalization rate, 25.9 per 1000 (95% CI: 21.3–30.8) infants (Table 2), with rates ranging by season from 8.6 to 37.0 per 1000 infants. Infants who were 2 months old and infants,1 month old had the next highest average hospitalization rates, with wide seasonal ranges: 14.3 (95%
CI: 11.1–17.8) and 13.5 (95% CI: 10.3– 17.1) per 1000 infants, respectively (Table 2). Overall, infants #2 months old were the most likely to be hospi-talized, with an average rate of 17.9 (95% CI: 15.7–20.1) per 1000 infants.
Over the next 3 months of life the average seasonal rates of RSV hospitalization consistently declined from 10.3 per 1000 infants who were 3 months old to 4.8 per 1000 infants who were 5 months old (Table 2). The average hospitalization rate for all 3- to 5-month-old infants was 8.0 (95% CI: 6.6–9.5), and for all 6- to 11-month-old infants was 3.9 (95% CI: 3.2– 4.7), which was not significantly different than any of the individual rates for each month of age between 6 and 11 months of age.
Infants who were#2 months old were hospitalized more than twice as often as infants who were 3 to 5 months old
(IRR: 2.2; 95% CI: 1.8–2.8) and 4.5 times more often than infants who were 6 to 11 months old (IRR: 4.5; 95% CI: 3.6–5.8). Of all children hospitalized with RSV, 44% were#2 months old, 64% were ,6 months old, and 83% were ,12 months old.
County and Calendar Month
The average seasonal hospitalization rates per 1000 children ,24 months old varied among the 3 counties. The rates of Monroe County (6.5; 95% CI: 5.8–7.3) and Hamilton County (6.2; 95% CI: 5.2–7.2) were significantly higher than Davidson County’s rate (4.0; 95% CI: 3.4–4.6) (IRR: 1.6; 95% CI: 1.2–2.0) (Supplemental Fig 2)
The calendar month also significantly influenced RSV hospitalizations. Av-erage monthly hospitalization rates per 1000 children ,24 months old TABLE 1 Characteristics of Children,24 Months of Age Hospitalized With Acute Respiratory
Infection, 2000–2005
Characteristic Hospitalized Patients Pa
RSV-Positive (n= 559) RSV-Negative (n= 1590)
Gender .82
Male 315 (56) 905 (57) Female 244 (44) 685 (43)
Age ,.001
0–2 months 245 (44) 755 (47) 3–5 months 111 (20) 200 (13) 6–11 months 106 (19) 269 (17) 12–23 months 97 (17) 366 (23)
Race ,.001
White 326 (58) 747 (47) Black 151 (27) 593 (37) Other 44 (8) 127 (8) Unknown 38 (7) 123 (8)
Health insurance .33
Public 300 (54) 884 (56) Private 216 (39) 555 (35) None 39 (7) 139 (9) Unknown 4 (1) 12 (1)
Palivizumab 19 (3) 93 (6) .03 Prematurity (,37 wk) 56 (10)b
177 (12)b
.44 Received palivizumab 13 (23) 49 (27) .51 Comorbid conditions 116 (21) 359 (23) .37 Other children in home .32
,18 and$5 years old 108 (19) 353 (22)
,5 years old 316 (57) 852 (54) No other children 135 (24) 385 (24)
Data are presented asn(%).
aPvalues derived byx2analyses for characteristics between hospitalized children with or without RSV infection. bGestational age could not be verified for 24 of RSV-positive and 78 of RSV-negative children.
were highest in December (1.0; 95% CI: 0.8–1.2), January (1.7; 95% CI: 1.5– 1.9), and February (1.2; 95% CI: 1.0– 1.4). During these 3 months, 73% of RSV hospitalizations for all children ,24 months old occurred, 19% in December, 31% in January, and 23% in February. Most RSV hospitalizations occurred in December in Hamilton County (27%) and in January in Davidson and Monroe Counties (27% and 37%, respectively).
Prematurity
Of RSV-hospitalized children, 10% were preterm, of whom 38% had an additional comorbid condition beyond prematurity. For all preterm infants (,37 weeks’ gestation), the average seasonal RSV hospitalization rate was 4.6 (95% CI: 3.4– 5.8) per 1000 children, which was not significantly different from that for term
– 1.1). However, the few very preterm infants born at ,30 weeks gestation (3%) had the highest RSV hospitalization
rate (18.7 per 1000 children), which was significantly greater than that for both early-preterm (30–33 weeks’gestation) and late-preterm (34–36 weeks’ gesta-tion) infants, as well as for full-term
infants (IRR for very preterm and early-preterm infants: 2.7; 95% CI: 1.3– 5.8) (Fig 1). Late-preterm infants, how-ever, were hospitalized significantly less
often than term infants (IRR: 0.5; 95% CI: 0.3–0.7).
Among all preterm infants hospitalized with RSV, 23% received palivizumab (Table 1). When analyzed according to
the gestational age groups used for palivizumab recommendations by the American Academy of Pediatrics12
(Supplemental Table 3), the hospitaliza-tion rate of all infants of 32 to 34 weeks’
gestation (regardless of palivizumab us-age) was 6.9 (95% CI: 4.3–10.1) per 1000 compared with that of all infants$35 weeks’gestation, which was 5.1 (95%
CI: 4.7–5.5) per 1000 (IRR: 1.4; 95% CI: 0.8–2.0).
Gender and Race
The overall seasonal rates of RSV hos-pitalization among all children ,24 months old were not significantly af-fected by gender or race (Supplemental Fig 3). Hospitalization rates per 1000
children,24 months old were 5.4 (95% CI: 4.6–6.3) for black children and 4.7 (95% CI: 4.2–5.1) for white children (IRR: 1.2; 95% CI: 1.0–1.4). Among infants,6 months old, the hospitalization rates for
black and white children were not sig-nificantly different, but among children
$6 months old black children were hospitalized significantly more often
(IRR: 1.9; 95% CI: 1.4–2.6).
Overall, 21% of children who were,24 months old hospitalized with RSV infection had a comorbid condition. The most frequent comorbid condition among RSV-positive children was car-diopulmonary disease. The proportion of RSV-hospitalized children with comorbid conditions varied with age. Coexisting medical conditions were present more frequently among older children. Among 12- to 23-month-old RSV-hospitalized children, 53% had a comorbid condition, whereas among infants ages ,6 months and 6 to 11 months, the proportions were only 7% and 39%, respectively. Thus, the pro-portion of the 12- to 23-month-old children with comorbid conditions was .7 times greater than that of infants,6 months old and 1.4 times greater than that of infants 6 to 11 months old. Similarly, 12- to 23-month-old RSV-hospitalized children had 9- and 1.4-fold greater proportions of cardio-pulmonary comorbidities than did infants who were,6 months old and those who were 6 to 11 months old, respectively.
Other Children in Home
Among all children ,24 months old who were hospitalized with RSV, 76% lived in homes with$1 other children of any age; 57% lived with another child ,5 years old, and 19% lived with an-other child 5 to,18 years old. Among RSV-hospitalized infants who were,12 months old, 58% lived with another child,5 years old, and 20% lived with another child 5 to,18 years old.
DISCUSSION
The average seasonal RSV hospitaliza-tion rate in this study was 5.2 per 1000 children who were ,24 months old, but the rate varied by season as much as fourfold. Nevertheless, 1-month-old infants consistently were most likely to
Among Children,24 Months of
Age, 2000–2005
Age (in months)a
n Rate per 1000 Children
95% CI
,1 62 13.5 10.3–17.1 1 115 25.9 21.3–30.8 2 68 14.3 11.1–17.8 3 47 10.3 7.7–13.5 4 42 8.9 6.3–11.8 5 22 4.8 2.9–7.0 6 20 4.1 2.5–6.2 7 26 5.6 3.6–8.0 8 15 3.4 1.8–5.2 9 16 3.8 2.1–6.0 10 16 3.7 2.0–5.7 11 13 2.9 1.5–4.8 12 13 3.2 1.7–5.3 13 8 1.7 0.7–3.2 14 7 1.6 0.6–3.1 15 11 2.7 1.3–4.6 16 9 2.0 0.8–3.6 17 7 1.7 0.6–3.2 18 11 2.6 1.2–4.4 19 3 0.6 0.2–1.7 20 7 1.7 0.6–3.2 21 6 1.6 0.5–3.2 22 7 1.7 0.7–3.2 23 8 2.0 0.8–3.7
,24 559 5.2 4.8–5.7
aA child was defined as being,1 month old if the child had
be hospitalized, almost twice as often as the next 2 most at-risk groups: infants ,1 month old and infants 2 months old. These youngest infants accounted for an important proportion of all children admitted with RSV in-fection in thefirst 2 years of life: 11% were infants,1 month old, 44% were
#2 months old, and only 36% were.5 months old.
The appreciable, but generally un-recognized, impact of neonatal RSV infection is important in planning strategies to control RSV infection because of both the financial health care burden and the hurdles inherent in developing safe and effective vaccines and therapeutic measures that must be administered within thefirst few weeks of life. Although recent studies, most of which were retrospective assessments, have consistently shown RSV hospital-izations to be the highest in thefirst year of life, very few have dissected the exact age of RSV-specific hospitalizations more precisely.4–6,13–20 For example,
a retrospective, population-based study
from Spain found that among children ,24 months old hospitalized with laboratory-identified RSV, 9% were,1 month of age, similar to our findings; however, their rate of RSV hospital-izations among infants,1 month of age was more than twice ours (31 per 1000 vs 13.5 per 1000, respectively).19
An-other study estimated a notably high annual rate of RSV-associated hospital-izations among infants#3 months old, 48.9 per 1000 children, which is more than twice the rate we found.6The
dif-ferences between studies could result from actual differences in disease bur-den or from the use in database studies of ICD-9-CM–coded discharge diagnoses for RSV-associated syndromes such as bronchiolitis, because they are in-accurate indicators of RSV infection among young infants.
Race has been correlated with more severe viral infections, especially
in-fluenza.21,22 For RSV infection,
in-formation is limited, but the reported severity of disease among black versus white children has been variable and
inconclusive.14,22,23 The rates of RSV
hospitalization among black children ,24 months old or,6 months old were not significantly different from those for white children. However, after 6 months of age, black children were hospitalized nearly twice as often. Thisfinding sug-gests that the decision to hospitalize young infants is strongly affected by their age, and perhaps also by other unidentified factors (eg, socioeconomic factors). We found no differences in RSV hospitalization rates by gender in this study or in previous work.7,22
The reported proportions of children with chronic conditions hospitalized with RSV have ranged widely, possibly reflecting the variable underlying populations and study designs.6,15,17,24
Stockman et al6 recently found that
12% of RSV-hospitalized children,12 months old and 2.4% of those 12 to 23 months old had heart disease, chronic neonatal respiratory distress, or pre-maturity, as determined by RSV ICD-9-CM– coded discharge diagnoses. In compari-son, we found that 21% of RSV-hospitalized
FIGURE 1
Average rates of hospitalization for RSV infection for children,24 months of age according to weeks of gestation, 2000–2005.aWeeks of gestation:,30 weeks = very preterm; 30–33 weeks = early preterm; 34–36 weeks = late preterm;$37 weeks = term. Total number of preterm infants,37 weeks’gestation = 56 (10%); for 24 children their gestational age could not be verified.
conditions, as determined by medical chart review. Again, this difference could be explained by the inaccuracy of RSV-specific diagnostic codes, the in-creased accuracy of our laboratory-confirmed diagnoses, or by our chart review identifying comorbidities not captured by ICD-9-CM codes. Increased palivizumab use early in life could reduce the proportion of children with comorbidities among all RSV hospi-talizations during thefirst year of life compared with the second year of life, as found by Stockman et al6and
in our study.
Prematurity has been consistently as-sociated with severe RSV infection, but the degree of risk has varied.14,15,17,25Of
our children hospitalized with RSV, 10% were preterm, but their risk of hospi-talization was not significantly differ-ent from that for term infants. We did
find lower rates of hospitalization among late-preterm infants, and higher rates among very premature infants, in contrast to other studies.12,15
Variability in hospitalization rates among early-preterm, late-preterm, and term infants may primarily result from premature infants in certain gestational age ranges being too few to reliably calculate hospitalization rates by gestational weeks. Perhaps the care patterns or environmental risks are different for late-preterm infants as well. Nevertheless, the effect of pre-term infants on our overall RSV hospi-talization rates and their impact on general health care issues are limited by prematurity being relatively in-frequent among the general population. The current national population esti-mate for premature birth at ,37 weeks’gestation is 12%, which is simi-lar to what we found among children hospitalized with ARI (11%); the national estimate for premature birth at ,30 weeks’gestation is 1%.26
creased risk of children acquiring RSV disease, especially contact with other children.12,14,16,17,27,28 A recent review
examining the effect of residential crowding on RSV-associated hospital-izations among young children found significant correlations existed with severe disease in studies reporting laboratory-confirmed RSV infections.27
However, the effect varied according to age and multiple factors associated with crowding.14,17,29In our study, the
proportion of hospitalized children re-siding in homes with other children,5 years old was more than twice that of children living with older children.
Our study has several potential limi-tations. The 3 counties, although geo-graphically diverse, may not be representative of the entire United States. In addition, our data do not ac-count for local differences in medical practices that may affect RSV hospi-talization rates. In addition, we did not study the effect of the recommended and nonrecommended use of palivizumab on our RSV hospitalization rates.12,30
However, palivizumab’s effect on our overall rates of RSV hospitalization was unlikely to be appreciable, be-cause only a small proportion (,5%) of our study population was eligible for palivizumab, and its use was vari-able (30% to 70%) during most study years.30Day care attendance has also
been described as a risk factor for RSV infection,12although inconsistently7,22; the
current work is limited by not analyzing this variable.
Strengths of our study include the population-based, prospective, laboratory-confirmed surveillance, medical chart review, and unlike our previous study,7the
use of birth certificates to better quan-tify the population at risk by individual months of age rather than as blocks of age groups. Taken together, ourfindings suggest that the children most likely
#
cially those 1 month of age), those living with other young children, and those born during the peak months of RSV circulation, which in our 3 counties were December and January.
Thesefindings indicate that strategies for diminishing the health care burden from RSV infections should include appropriate prophylaxis and the de-velopment of vaccines that are effective in very young infants, even those within the first month of life. In addition, general infection control practices such as restrictions of visits from ill indi-viduals and careful hand washing should be emphasized, especially during the peak months of RSV cir-culation. In addition, these preventive measures should not be restricted to high-risk infants, but rather targeted to all infants, because most of the affected infants were previously healthy and born at full term. Until such time that universal RSV immu-nization becomes possible, our pro-spective, population-based surveillance data for laboratory-confirmed RSV hos-pitalizations stratified by month of age may assist in prioritizing preventive measures.
ACKNOWLEDGMENTS
Walker, John Copeland, Dean Erdman, and James Alexander at the Centers for Disease Control and Prevention.
This article is dedicated to the memory of Caroline Breese Hall, MD, a true leader in RSV clinical research,
a respected mentor for many trainees and faculty alike, and a valued col-league to the authors.
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(Continued fromfirst page) Dr Hall is deceased.
Drs Hall, Weinberg, Szilagyi, and Iwane conceptualized and designed the study; acquired, analyzed, and interpreted the data; drafted the manuscript and critically revised it for important intellectual content; obtained funding; provided administrative, technical, and material support; and supervised the study; Mr Blumkin acquired, analyzed, and interpreted the data; critically revised the manuscript for important intellectual content; and performed critical statistical analyses of the data; Drs Edwards, Staat, and Griffin conceptualized and designed the study; acquired, analyzed, and interpreted the data; drafted the manuscript and critically revised it for important intellectual content; obtained funding; and supervised the study; Mr. Schultz acquired, analyzed, and interpreted the data; critically revised the manuscript for important intellectual content; performed critical statistical analyses of the data; and provided administrative, technical, and material support; Dr Poehling conceptualized and designed the study; acquired, analyzed, and interpreted the data; drafted the manuscript and critically revised it for important intellectual content; and supervised the study; Dr Williams conceptualized and designed the study; acquired, analyzed, and interpreted the data; critically revised the manuscript for important intellectual content; and supervised the study; Drs Zhu and Grijalva acquired, analyzed, and interpreted the data; performed critical statistical analyses of the data; and critically revised the manuscript for important intellectual content; and Ms Prill acquired, analyzed, and interpreted the data; performed critical statistical analyses of the data; critically revised the manuscript for important intellectual content; and provided administrative, technical, and material support. All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the Centers for Disease Control and Prevention.
www.pediatrics.org/cgi/doi/10.1542/peds.2013-0303
doi:10.1542/peds.2013-0303
Accepted for publication May 16, 2013
Address correspondence to Geoffrey A. Weinberg, MD, Department of Pediatrics, University of Rochester School of Medicine and Dentistry, PO Box 690, 601 Elmwood Ave, Rochester, NY 14642. E-mail: geoff_weinberg@urmc.rochester.edu
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2013 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE:Dr Hall has consulted for GlaxoSmithKline (GSK) and MedImmune and has received research support from MedImmune. Dr Weinberg has served on speakers’bureaus for GSK, Merck, and SanofiPasteur. Dr Edwards has received research funding from Novartis for nonrelated vaccine trials. Dr Staat has received research support from GlaxoSmithKline, Merck, and MedImmune; has consulted for GSK, Merck, and MedImmune; and has been on the speakers’ bureaus for GSK and Merck. Dr Poehling has received research support from BD Diagnostics. Dr Griffin has consulted for Novavax and MedImmune. Dr Williams serves on the Scientific Advisory Board for Quidel. The other authors have indicated they have nofinancial relationships relevant to this article to disclose.
DOI: 10.1542/peds.2013-0303 originally published online July 22, 2013;
2013;132;e341
Pediatrics
Prill and Marika K. Iwane
Szilagyi, Marie R. Griffin, John V. Williams, Yuwei Zhu, Carlos G. Grijalva, Mila M.
Edwards, Mary A. Staat, Andrew F. Schultz, Katherine A. Poehling, Peter G.
Caroline Breese Hall, Geoffrey A. Weinberg, Aaron K. Blumkin, Kathryn M.
Than 24 Months of Age
Associated Hospitalizations Among Children Less
−
Respiratory Syncytial Virus
Services
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DOI: 10.1542/peds.2013-0303 originally published online July 22, 2013;
2013;132;e341
Pediatrics
Prill and Marika K. Iwane
Szilagyi, Marie R. Griffin, John V. Williams, Yuwei Zhu, Carlos G. Grijalva, Mila M.
Edwards, Mary A. Staat, Andrew F. Schultz, Katherine A. Poehling, Peter G.
Caroline Breese Hall, Geoffrey A. Weinberg, Aaron K. Blumkin, Kathryn M.
Than 24 Months of Age
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