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=�@GC�>��(�(0,�(�(�(�(�(�A�A0,�(�(�(B�(�(�(�(��������������������������������������������������������������������@G�(�(�(�(�(�(�(�(�(		:	Impact of Updated Recommendations for Respiratory Syncytial Virus Prophylaxis on 32-35 Weeks Preterm Infants
Olajide Dolapo, MD1, Susana Rapaport, MD2, Fernanda E. Kupferman, MD2, David Di John, MD2 , Louis Primavera, PhD3, Lourdes Cohen, MD2      

 1University of Tennessee Health Science Center, Memphis, TN
2Flushing Hospital Medical Center, Flushing, NY
3Touro College, New York, NY

Corresponding author -   Olajide  Dolapo, MD 
                                            Department of Pediatrics/Division of Neonatology  
                                            University of Tennessee Health Science Center
                                            Suite 201               
                                            853 Jefferson Avenue, Memphis, TN 38163-0001
                                            Email: HYPERLINK "mailto:odolapo1@uthsc.edu"odolapo1@uthsc.edu, phone: 9014485970, fax: 9014481691
Short Title: RSV Prophylaxis recommendations -Impact on the Late Preterm
Abbreviations: RSV � Respiratory Syncytial Virus; GA � Gestational Age, S1 � season 1; S2 � season 2. 
Key Words: palivizumab, neonatal infectious diseases, respiratory syncytial virus, prophylaxis and preterm infants
Funding source: No external funding was secured for this study
Conflict of Interest: The authors have no conflict of interest to disclose

What�s Known on This Subject
Respiratory Syncytial Virus is the leading cause of lower respiratory tract infection in infants, accounting for 20% of pediatric hospitalization. Preterm infants are at higher risk of severe disease compared with term infants. 
Recommendations limit eligibility for palivizumab among 32-35 weeks preterm infants

What This Study Adds
This study compares the severity of RSV disease among former 32-35 week preterm infants, in the seasons before and after the introduction of existing prophylaxis recommendations, with a view to determining the impact of this change



Contributor�s Statement

Olajide Dolapo: Dr Dolapo developed the study concept and designed the study. He contributed in data collection, drafted the manuscript and approved the final manuscript as submitted

Susana Rapaport: Dr Rapaport contributed to study design, collection of data from the two sites, the review of the manuscript and approved the final manuscript as submitted

Fernanda Kupferman: Dr Kupferman contributed to literature search, the design of the study, data analysis and interpretation and approved the final manuscript as submitted

David Di John: Dr Di John contributed to the study design,  data interpretation, the drafting of initial manuscript and approved the final manuscript as submitted

Louis Primavera: Dr Primavera performed the statistical analysis, contributed to data interpretation and approved the final manuscript as submitted

Lourdes Cohen: Dr Cohen conceptualized the study, contributed to literature search, the study design, supervised and coordinated data collection, analysis and interpretation and approved the final manuscript as submitted

  



















ABSTRACTObjective: To assess the severity of Respiratory Syncytial Virus (RSV) disease following the introduction of the updated palivizumab prophylaxis recommendations, among infants of 32-35 weeks gestational age (GA). Methods: A retrospective study of two groups of 32-35 weeks GA infants born and followed at two community hospitals through the RSV seasons immediately before and after the introduction of the 2009 American Academy of Pediatrics (AAP) recommendations. Databases were searched for all 32-35 week GA births and RSV hospitalizations. Dosing histories for palivizumab were obtained. Admissions for RSV infection were compared using length of hospital stay, intensive care requirement, mechanical ventilation and re-hospitalization for RSV. Results: Of the 465 infants born during the study period, 226 were in 2008-2009 season (S1) and 239 in 2009-2010 season (S2). In S1, 809 doses of palivizumab were administered and 129 doses in S2. Of the 226 infants enrolled in S1, 13 (5.8%) were subsequently hospitalized for RSV infection, and in S2, 7 of 239 infant (2.9%) had RSV hospitalization later in the season (p=0.171). Average length of hospital stay in S1 was 5.31 days, and 3.14 days in S2 (p=0.014). In S1, 7.7% of those hospitalized required intensive care and 15.4% were readmitted. These factors were absent in S2. Conclusions: There was no increase in the number of hospitalizations and severity of RSV disease in preterm infants 32-35 weeks GA following implementation of the 2009 AAP recommendations for palivizumab prophylaxis. 












Introduction
Respiratory Syncytial Virus (RSV) is the leading cause of lower respiratory tract infection in infants and young children, accounting for 20% pediatric hospitalizations, 18% emergency departments� visits and 15% of office visits for acute respiratory infections during the winter months of the year.1,2 The significance of the burden of RSV infection in the U.S is evident , with an average annual hospitalization rates of 17 per 1000 in children under 6 months and 3 per 1000 in under 5 years.2 
Preterm birth, complex congenital heart disease and chronic lung disease are identified characteristics that increase the severity of RSV infection. 2,3,4 Among  preterm infants, especially at risk, are infants born before 32 weeks gestation, who are less than 6 months old at the onset of the winter RSV season.1,2,3,4,5These infants suffer to varying degree, worrisome complications that include prolonged hospital stay, pneumonias, middle ear infections, recurrent RSV infections, documented risk of developing asthma  later in life and even death. However, late preterm infants (34 to 36 weeks gestation), who comprise 70% of the preterm population are at higher risk of severe RSV disease compared with term infants.6,7 Previous studies suggest hospitalization and severity of RSV disease among late preterm infants may be similar to that seen in the very preterm. This may be attributable to the developmental and physiologic immaturity of late preterm infants compared to term infants. 6,7
Palivizumab (a humanized mouse monoclonal antibody, licensed in the United States for the prevention of RSV disease in infants and children) has been shown by multiple studies to decrease the rate of hospitalization for RSV infections by more than 50% in infants and children.8,9 The existing palivizumab immunoprophylaxis recommendations for RSV disease, limit the use of palivizumab among infants 32-35 weeks preterm, to fewer doses when compared to previous recommendations.1,3 According to previous reports, these modifications to palivizumab prophylaxis recommendations were introduced by the American Academy of Pediatrics (AAP) in an effort to ensure optimal balance of benefit and cost from what is considered to be an expensive intervention, thereby,   directing immunoprophylaxis to the most susceptible infants.3 Among 32-35 week gestation preterm infants, the risk of RSV infection is greatest in the first 3 months of life, or when there is exposure to child care centers �defined as a home or facility where care is provided for any number of infants or young toddlers, or when there is one or more sibling younger than 5 years in the same household.3
Few data are available to show the impact of these recommendation changes among this group of preterm infants. 
Our study aimed to assess the impact of existing immunoprophylaxis recommendations for RSV infection on hospitalization and severity of disease among preterm infants of 32-35 weeks gestational age. This, we determined by evaluating the seasons before and after the introduction of the current recommendations for this particular group of infants.
Methods  
This was a retrospective, comparative, cohort study carried out in the departments of pediatrics of two community hospitals, located in Queens, New York � Flushing Hospital Medical Center and Jamaica Hospital Medical Center. These two hospitals represent the Medisys Healthcare Network in New York. 
The study was approved by the Institutional Review Boards. 
Study population included all 32-35 week preterm infants born and followed in the two hospitals between the periods of May 1st 2008 and April 31st 2010. Selection of subjects was carried out based on the review of the hospitals� discharge codes for the following diagnosis: RSV Bronchiolitis (466.22) and RSV not otherwise specified (079.6). Hospital databases and neonatal registries were searched for all records of 32-35 weeks preterm birth and hospitalization for RSV bronchiolitis. Estimation of gestational age was based on maternal history of last menstrual period and/or a dating record from a first trimester ultrasound.  Palivizumab dosing histories were obtained from records of clinic visits, high-risk follow ups and interview with parents. Infants that were not followed post-discharge by the Medisys Health Network were not included in the study.  Infants with co-morbidities including chronic lung disease, cyanotic congenital heart disease or immunodeficiency states were also excluded. The updated guidelines for RSV prophylaxis for infants born at 32 to less than 35 weeks� gestation, as recommended by the AAP were strictly followed, according to the hospital protocol. (2006 policy for the 2008-2009 RSV season and the updated 2009 policy for the 2009-2010 RSV season)1,3. Demographic data including age, gender and birth weights were collected.
Subjects were classified into two broad groups, based on the date of birth. Season 1 (S1) were infants born between May 1st 2008 and April 30th 2009 and who received RSV prophylaxis based on the 2006 recommendations, while Season 2 (S2) represents infants born from May 1st 2009 to April 31st 2010, who based on the Medisys Network protocols were immunized with palivizumab using the updated 2009 immmunoprophylaxis recommendations. Records of RSV infection admissions on subsequent follow-up within the Network were compared between these two groups. The comparison of RSV disease severity in the two groups was determined by the following parameters: (a) Length of hospital stay (b) intensive care unit (ICU) admission (c) CPAP support (d) supplemental oxygen for oxyhemoglobin saturation level persistently below 90% (e) intubation and mechanical ventilation requirement (f) pneumonia complication (g) readmission for RSV infection in the same season (h) mortality (attributable to the RSV disease, as defined by the clinical team).
Data analyses were presented as mean� standard deviation and as percentages. Categorical variables were analyzed by using �2 test or Fisher s exact test. Continuous variables were analyzed using the Student s t-test for comparison between groups. Statistical significance was set at p value of < 0.05. SPSS software 15.0 version was used for analyses.            

Results
During the study period from May 2008 to April 2010, a total of 465 infants born in the hospitals met the eligibility criteria and were selected for the study. 226 infants were enrolled in S1 for the 2008-2009 RSV season and 239 infants in S2 which denotes the 2009-2010 RSV season. A total of 113/226 (50%) were male sex in S1 and 128/239 (53.8%) were males in S2. Mean birth weights of infants in the two seasons were identical as shown in Table 1. Similarly, the mean gestational ages of infants recruited in the two seasons were comparable (S1 =33.6 weeks, SD  QUOTE  1.1 and S2 = 33.8 weeks, SD QUOTE   Expectedly, significantly more doses of palivizumab prophylaxis was given in the first season (809 doses vs. 129 doses).
Of the 226 infants enrolled in S1, 13 (5.8%) were subsequently hospitalized for RSV infection, and in S2, 7 of 239 infants (2.9%) had RSV hospitalization later in the season. This difference was not statistically significant. (p=0.171)
In S1, 7 of the 13 (53.8%) RSV admissions required up to 10 days or longer period of hospitalization, and the mean length of hospital stay in S1 was  5.31 days (SD �2.1) compared to all 7 (100%) of  S2 infants requiring less than 5 days hospital stay and an average length of hospital stay of 3.14 days (SD � 1.2).  53.8% of hospitalized infants in S1 had superimposed pneumonia with consolidations on chest radiographs, and associated clinical and/or biochemical evidence of bacterial infection, as diagnosed by the clinical team, requiring management with antibiotics, in addition to the conventional management of bronchiolitis. Only 2 of 7 (28.6%) S2 infants had pneumonia complication and were managed with antibiotics. Furthermore, 7 of 13 (53.8%) of infants admitted in S1 were on supplementary oxygen support, for oxyhemoglobin saturation level that fell persistently below 90%. No documentation of increased oxygen requirement in S2 infants.  In S1, 1 of 13 infants (7.7%) was transferred to intensive care unit for further management and required CPAP support for 48 hours, there was however no intubations or mechanical ventilation required and no mortality cases. There was no ICU admission in S2. Similarly, 2 of 13 (15.4%) in S1 were readmitted for a repeat episode of RSV bronchiolitis, while there was no repeat hospitalization in S2.



Discussion
Our findings provide a comparative view of RSV infection burden among former 32-35 week gestation, preterm infants, following the introduction of the updated recommendations for palivizumab prophylaxis for RSV infection for this subset of preterm infants. In our population, the rate of hospitalization for RSV infection in the season prior to the updated recommendations (2008-2009) was two times as high as observed in the following season (2009-2010), even though the proportion of children receiving palivizumab prophylaxis was significantly lower in the 2009-2010 season. Reason(s) for this remain unclear, though the possibility of a more virulent viral strain of RSV for the 2008-2009 season was considered. Earlier RSV surveillance studies documented different strains of RSV viruses as dominant in these 2 seasons. RSV-A strain was more prevalent in the 2008-2009 season, while RSV �B strain genotype BA was dominant in the 2009-2010 season.15 The differences in antigenicity could however not be used as an explanation for the variability in clinical severity of the disease caused. This was emphasized by Kneyber et al in a previous study where the relationship between the clinical severity of RSV infection and the distribution of subtype A and B of RSV virus, was investigated. 232 children were enrolled, where 150 (64.7%) were infected with subtype A and 82(35.3%) with subtype B. They concluded that such a relationship did not exist. 16 
We also observed a significantly higher incidence in the markers of disease severity, including ICU admission, length of hospital stay and greater need for oxygen in children hospitalized for RSV infection during the 2008-2009 season, compared to the 2009-2010 season, which does not reflect the increased antiviral immunoprophylaxis use among the former group of infants. The readmission rate for RSV infection was also higher in the same subset of infants from the 2008-2009 season.  There was however no difference in the incidence of other disease severity markers such as the need for endotracheal intubations, mechanical ventilation and mortality observed in the two seasons.
Earlier surveillance reports of RSV infection and hospitalizations have not indicated a decrease in trend as it pertains to the two seasons looked at, so a possibility of an overall higher incidence of RSV infection in the 2008-2009 season could not be proven.17
Some of the difficulties that occur with the implementation of the updated recommendations for palivizumab prophylaxis such as poor or inadequate compliance in primary practice, was addressed by our study, through the restriction of enrolled infants to those receiving pediatrician follow-up within the Medisys Network, where the AAP guidelines for the use of palivizumab are strictly followed, based on institutional protocol. The problem of inappropriate or inadequate use of palivizumab could however not be completely ruled out.
Our study was limited by the small sample size and the retrospective collection of data over two season period, which were the available periods at the time of the study. An extension to include more years will give a clearer and more accurate assessment of the impact of the change in the prophylaxis recommendations. 
In conclusion, our findings demonstrated no apparent increase in susceptibility to RSV infection, among former 32-35 week gestation, preterm infants, who have received none or fewer doses of palivizumab prophylaxis following the implementation of the 2009 AAP guidelines.

Potential Conflicts - All authors: No conflicts
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American Academy of Pediatrics - Committee on Infectious Diseases. Redbook  2006; 560-561
Hall CB, Weinberg GA, Iwane MK et al. The Burden of Respiratory Syncytial Virus Infection in Young Children. New England Journal of Medicine. 2009;360:588-589
American Academy of Pediatrics - Committee on Infectious Diseases: Policy Statements � modified recommendations for use of Palivizumab for Prevention of Respiratory Syncytial Virus Infections. Pediatrics. 2009; 124(6):1694-1701
Hervas D, Reina J, Yanez A et al. Epidemiology of Hospitalization for Acute Bronchiolitis in Children: Differences between RSV and non-RSV Bronchiolitis. European Journal of Clinical Microbiology and Infectious Diseases. 2012; 31(8): 1975-1981
Meissner HC, Long SS and Committee on Infectious Diseases, and Committee on Fetus and Newborn. Revised Indications for the Use of Palivizumab and Respiratory Syncytial Virus Immune Globulin Intravenous for the Prevention of Respiratory Syncytial Virus Infections. Pediatrics 2003; 112:1447-1452
Engle WA, Tomashek KM, Wallman C. �Late Preterm� Infants: A Population at Risk. Pediatrics 2007; 120(6): 1390-1401
Lanari M, Silvestri M, Rossi GA. Respiratory Syncytial Virus Risk Factors in Late Preterm Infants. Journal of Maternal-Fetal and Neonatal Medicine 2009; 22(3): 102-107
Canfield SD, Simoes EA. Prevention of Respiratory Syncytial Virus - RSVIG and Palivizumab. Pediatric  Annals 1999; 28: 507-514
Groothius JR, Simoes EA, Levin et al. Prophylactic administration of Respiratory Syncytial Virus Immune globulin to High Risk Infants and Young Children. New England Journal of Medicine. 1993;329:1524-1530
Krilov LR, Weiner LB, Yogev R, et al. The 2009 COID recommendations for RSV prophylaxis: issues of efficacy, cost, and evidence-based medicine. Pediatrics. 2009;124(6):1682-1684 
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Dapat IC, Shobugawa Y, Sano Y et al. New Genotypes within Respiratory Syncytial Virus Group B Genotype BA in Niigata, Japan. Journal of Clinical Microbiology  2010;48(9):3423-3427 
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Neves Barreira J, Fonseca C, Cardoso M et al. Relationship between Respiratory Syncytial Virus Subtype and Clinical Severity in Bronchiolitis. Anales Espanoles de Pediatria. 2001; 54(6):559-566
Domachowske JB, Rosenberg HF. Respiratory Syncytial Virus Infection: Immune Response, Immunopathogenesis and Treatment. Clinical Microbiology Reviews. 1999; 12(2): 289-309















Table 1: Demographics of Cohorts in the two seasons, showing similarities in birth weights and gestational ages.

Table 2:  Showing total no of palivizumab prophylaxis doses received by 32-35 week preterm infants in the 2008/2009 and 2009/2010 RSV seasons. Total no of 809 doses were administered in season 1 vs. 129 doses in season 2.

Figure 1: Showing the severity of hospital admissions observed in the two seasons.

Table 3: Comparison of RSV infection severity in the 2008/2009 season vs. 2009/2010 season 








Table 1:
2008-2009 RSV Season  (n=226) 
Mean (SD)2009-2010 RSV Season (n=239)
Mean (SD)p valueBirth weight (grams)2085 � 4312139 � 4760.201Gestational Age (weeks)33.7 � 1.1033.8 � 1.090.325Male  %113 (50%) 128 (53.8%)Female %113 (50%)111 (46.2%)










 Table 2:
No of Palivizumab Dose Received2008/2009 RSV Season 
(Total no of Infants)2009/2010 RSV Season 
 (Total no of Infants)                           0                      45                          178                           1                      8                          16                           2                      7                          22                           3                      17                          23                           4                      9                          0                           5                      140                          0








Figure 1:
 EMBED MSGraph.Chart.8 \s 





Table 3:

Comparison of RSV infection severity in the 2008/2009 season vs. 2009/2010 season 


VariableS1S2P valueHospitalized for RSV infection 13/ 809 (5.8%)7/ 129 (2.9%)0.171Mean length of hospital stay in days + SD5.31 (SD �2.1)3.14 (SD � 1.2)0.0001Superimposed pneumonia7/13 (53.8%)2 /7 (28.6%)0.372Supplementary oxygen support due to hypoxia7 of 13 (53.8%)0/7 (0%)0.044Transferred to ICU and required CPAP1 of 13 infants (7.7%)0/7 (0%)1.000Readmition for a repeat episode of RSV bronchiolitis2 /13 (15.4%)0/7 (0%)0.521








 PAGE   \* MERGEFORMAT 17



% of Infants Hospitalized for RSV Infection

0

0

0

15.4

0

7.7

0

0

7.7

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