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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 9  |  Issue : 4  |  Page : 124-130

Outbreak of respiratory syncytial virus infection in Eastern India during COVID-19 pandemic: An observational study from a single pediatric intensive care unit


1 Department of Pediatrics, Medical College and Hospital, Kolkata, West Bengal, India
2 Department of Pediatrics, North Bengal Medical College and Hospital, Siliguri, West Bengal, India

Date of Submission30-Mar-2022
Date of Decision23-Jun-2022
Date of Acceptance24-Jun-2022
Date of Web Publication20-Jul-2022

Correspondence Address:
Dr. Manas Kumar Mahapatra
Doctors Chummery Hostel, 41 Eden Hospital Road, Kolkata - 700 073, West Bengal
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jpcc.jpcc_27_22

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  Abstract 


Background: After the peak of the second wave of COVID-19 pandemic, we faced a surge of respiratory syncytial virus (RSV) infection. This study was aimed to estimate the severity, clinical course, and outcome of RSV-infected children admitted in pediatric intensive care unit and to identify the predictors of development of acute respiratory distress syndrome (ARDS).
Subjects and Methods: This retrospective study included children below 5 years with influenza-like illnesses (ILI) due to RSV infection. The clinical, laboratory, treatment, and outcome-related parameters were assessed and a compared between ARDS and non-ARDS group.
Results: Out of 44 ILI patients, 36 had RSV infection. Most of them (88.9%) were infants. Twenty-four (66.7%) patients developed ARDS and 9 (25%) were ventilated. Infants below 6 months, low birth weight (LBW) babies, consolidations (≥3 zones), interstitial edema (≥3 zones) in lung ultrasound, high pediatric sequential organ failure assessment (pSOFA), and Pediatric Risk of Mortality III score were significantly associated with ARDS.
Conclusions: RSV-infected children with young age (1–6 months), LBW, higher lung ultrasound, and pSOFA score should alert physicians for progression to ARDS.

Keywords: Acute respiratory distress syndrome, influenza-like illnesses, pediatric intensive care unit, respiratory syncytial virus


How to cite this article:
Mandal B, Roychowdhoury S, Barui P, Konar MC, Bhakta S, Nandi M, Uz Zaman MA, Sarkar M, Mahapatra MK. Outbreak of respiratory syncytial virus infection in Eastern India during COVID-19 pandemic: An observational study from a single pediatric intensive care unit. J Pediatr Crit Care 2022;9:124-30

How to cite this URL:
Mandal B, Roychowdhoury S, Barui P, Konar MC, Bhakta S, Nandi M, Uz Zaman MA, Sarkar M, Mahapatra MK. Outbreak of respiratory syncytial virus infection in Eastern India during COVID-19 pandemic: An observational study from a single pediatric intensive care unit. J Pediatr Crit Care [serial online] 2022 [cited 2022 Aug 16];9:124-30. Available from: http://www.jpcc.org.in/text.asp?2022/9/4/124/351514




  Introduction Top


Respiratory syncytial virus (RSV) is one of the most common viruses to cause acute respiratory tract (ARI) infection in children and adult. Usually, it causes mild symptoms such as cough, sneeze, nasal congestion, and discharge.[1],[2] However, children usually develop more severe manifestations such as breathing difficulty and sometimes require oxygen therapy or respiratory support. RSV infection is contagious and spread by direct contact with respiratory tract secretion or droplet. In developing countries, RSV infection rate varies between 6% and 83% every year.[2] Acute lower respiratory tract infection (LRTI) is one of the leading causes of morbidity in <5-year-old children. Infants with a history of prematurity, bronchopulmonary dyspepsia, congenital heart disease, congenital immunodeficiency, and Down's syndrome have increased risk of severe infection.

On the other hand, the recent COVID-19 pandemic (World Health Organization [WHO] declared in March 2020) mandated the use of preventive measures such as avoidance of social gathering, maintaining recommended social distancing, wearing of mask and frequent handwashing among peoples in most part of the word.[3] These measures caused the breakdown of transmission chain of droplet and direct contact infection spread and drop in the infection rate of other common respiratory viruses during the peak of pandemic.[4] However, at the same time, this has led to increase in the number of susceptible persons in the society and increase the chance of infection by the common respiratory viruses when the activities were resumed with relaxation of preventive measures.[5]

After the peak of the second wave of COVID-19 pandemic, eastern part of India faced such a peak of respiratory viral infection.[6] Many children required hospitalization and even intensive care admission and most of them were diagnosed to have RSV infection. Hence, this study was aimed to estimate the severity, clinical course, different treatment measures, and outcome of RSV-infected children admitted in the pediatric intensive care unit (PICU) and to identify the predictor of development of acute respiratory distress syndrome (ARDS).


  Materials and Methods Top


This descriptive observational study was performed by retrospective data analysis of children admitted in PICU in the age group of 1 month–5 years, over the period of 2 months (August 21–September 21) in a tertiary care facility in eastern India. After obtaining institutional ethics committee approval (Ref No. MC/KOL/IEC/NON-SPON/1225/11/202; Dated November 20, 2021), case records of all patients admitted to PICU during the study period were screened to identify the children having influenza-like illnesses (ILI). ILI was defined and classified as per the government of India guideline.[7] RSV infections were confirmed by respiratory viral panel from nasopharyngeal swab by the nucleic acid amplification test. On admission, swab was sent to regional Indian Council Medical Research Institute laboratory in a viral transport medium provided from the laboratory. The samples were analyzed for Influenza A (H1N1), RSV A, RSV B, human metapneumovirus; Parainfluenza 1, 2, 3, 4; Adenovirus, Rhinovirus. COVID-19 reverse transcription polymerase chain reaction (RT-PCR) and RAT test was negative in all cases.

Demographic, clinical, and radiographic data and different relevant laboratory parameters were extracted from the medical records during the PICU stay. Investigations performed within 24 h of PICU admission were taken for the analysis. Basic laboratory investigations such as hemoglobin, total white blood cell (WBC) count, platelet count, C-reactive protein (CRP), serum sodium, creatinine, serum glutamic pyruvate transaminase (SGPT), and international normalized ratio were taken into our records and cutoff values were defined as per the age-specific standards.[8]

Patients were treated with existing protocol for the management of ILI in the PICU. We collected the data on the requirement of types of respiratory support with duration, nebulization (bronchodilators/epinephrine/3% sodium chloride [NaCl]), IV antibiotics, intravenous fluids, and inotropes requirements.

Patients having pneumonia or bronchiolitis with saturation below 92% were administered O2 through O2 mask and any nonimprovement or deterioration on serial monitoring, the support was escalated to high-flow nasal cannula or noninvasive ventilation (NIV) or invasive mechanical ventilation (IMV) according to the severity of respiratory distress/failure and arterial blood gas (ABG) parameters. Hemodynamically unstable patients or those who were unable to maintain airway were directly ventilated. In ventilated patients, mini bronchoalveolar lavage (Mini BAL) was sent within 24 h. of intubation for bacterial culture.

Definition from the WHO was used to define pneumonia and respiratory distress with its severity.[9] ARDS and it's severity were defined using PALICC criteria in respect to oxygenation index in invasively ventilated children and PaO2/FiO2 ratio in nonintubated children.[10] The management of ARDS was based on lung-protective ventilation strategy. Those who were invasively ventilated were started on pressure control or pressure regulated volume control mode in MAQUET Servo-i ventilator, as per the running protocol of our PICU. ABG measurements, ventilator modes and settings, oxygenation-related variables, maximum ventilator settings required, and their duration were extracted from our records.

To monitor organ function, pediatric sequential organ failure assessment (pSOFA) score was taken within 24 h of PICU admission.[11] Disease severity was assessed with Pediatric Risk of Mortality (PRISM III) score.[12] Bedside lung ultrasonography (USG) was done by Philips HD7 (Philips Healthcare, Netherlands) with the high frequency linear probe (L 7–12 mHz) at the time of PICU admission and score was calculated in 12 zones for each patient.[13] Available echocardiography findings of the patients were noted. According to our PICU protocol, ejection fraction <55% by modified Simpson's method was considered as systolic dysfunction.

The outcome was measured in the form of PICU stay, hospital stay, and mortality. Different clinical and laboratory and outcome-related parameters were compared between those who had ARDS and those who didn't.

Data were entered and analyzed using the statistical package SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA) version 23. The continuous variables were expressed as median, interquartile range (IQR), and mean, standard deviation (SD), whereas categorical variables as numbers and percentages. The comparison of different clinical and laboratory parameters between the two groups (ARDS and Non-ARDS) was analyzed by Fischer's exact test or Chi-square test for categorical variables, and unpaired t-test for continuous variable if normally distributed data otherwise Mann–Whitney U-test was done. P < 0.05 was considered statistically significant.


  Results Top


A total of 93 patients were admitted with ILI during the study period in hospital, among them 44 (47.3%) required PICU admission. All were negative for COVID-19 RAT test or RT-PCR test. Respiratory viral panel report was positive for RSV in 36 (81.8%) PICU admitted ILI patients which constitutes 48% of total hospitalized RSV (n = 75) infection [Figure 1].
Figure 1: Distribution of ILI patients admitted in hospital. ILI: Influenza-like illnesses, PICU: Pediatric intensive care unit, RSV: Respiratory syncytial virus, ARDS: Acute respiratory distress syndrome

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Among the PICU admitted patients 32 (88.9%) were infant and 21 (58.3%) of them were male. All the children had respiratory distress, 30 (83.3%) had coryzal symptoms, 34 (94.4%) had subcostal retractions, and 33 (91.7%) had tachypnea. Mean saturation of oxygen on admission was 87.9% (SD: 3.5). Twenty-five (69.4%) patients were febrile and maximum temperature was 101.3°F (IQR 100.8–101.6). Eleven (34.4%) patients had shock. Congenital heart disease (16.7%) was the most common comorbidity present among the RSV affected children admitted in PICU. A total of 24 patients fulfilled the criteria of ARDS and 14 patients had moderate to severe ARDS. Among these children, 11 born premature, 17 were low birth weight (LBW) [Table 1].
Table 1: Demographic, clinical profile, and risk factors of pediatric intensive care unit admitted children with respiratory syncytial virus infection (n=36)

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Basic blood investigations showed: Mean hemoglobin level 10.4 (SD: 1.4) g/dl; WBC, absolute neutrophil count, platelet counts were within normal limits. CRP, SGPT, and creatinine level were raised in 52.8%, 13.8%, and 16.7% patients, respectively. Blood lactate was high in 13 (36.1%) patients. Blood cultures were positive in 5 (13.8%) patients (methicillin sensitive Staphylococcus aureus-2, methicillin-resistant Staphylococcus aureus (MRSA)-1, Pseudomonas-1, Burkholderia-1) and 2 intubated (out of 9) patients had mini-BAL culture positive for MRSA. The most common finding in chest X-ray was bronchopneumonia (44.4%) followed by interstitial pattern (22.2%). Bedside USG lung revealed consolidations (≥3 zone) in 19 patients and interstitial edema pattern (≥3 zone) in 28 patients. Point of care functional echocardiogram showed myocardial dysfunction in three patients [Table 2].
Table 2: Investigation parameters of pediatric intensive care unit admitted children with respiratory syncytial virus infection (n=36)

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As maximum respiratory support, 10 (27.8%) patient needed high flow nasal canula oxygen, 14 (38.9%) required NIV, and 9 (25%) required IMV. Median duration of invasive ventilation requirement was 5 days (IQR: 4–10). 3% NaCl was the most common agent (n = 11, 30.5%) used for nebulization therapy. Ten patients (27.7%) required fluid bolus (≥20 ml/kg) and 11 patients required inotropic support. Six patients required steroid, most common indication was ARDS, followed by shock and myocardial dysfunction. One patient was given IV IG due to myocardial dysfunction. Median PICU stay was 7 days (IQR: 5–8) and hospital stay was 10 days (IQR: 8–14). Two (5.6%) patients died, and both were premature with preexisting comorbidity [Table 3].
Table 3: Treatment and outcome profile of pediatric intensive care unit admitted children with respiratory syncytial virus infection (n=36)

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Further detailing of respiratory support required by the children has been elaborated in [Supplementary Table 1].



[Table 4] shows that younger infants (1–6 months) and children born with LBW were predictors (P = 0.007 and 0.014, respectively) of ARDS. ARDS children had significantly high pediatric SOFA and PRISM score, lung consolidations (≥3 zone), and pulmonary interstitial edema (≥3 zones) detected by point of care USG.
Table 4: Predictor of risk factors of pediatric acute respiratory distress syndrome and nonpediatric acute respiratory distress syndrome pediatric intensive care unit admitted children with respiratory syncytial virus infection

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  Discussion Top


RSV is a known pathogen causing ARI infection in children. By 2 years of age, more than 80% of children have been infected at least once with RSV.[14] During the COVID-19 pandemic, reports from around the world suggested about 98% reduction of the RSV infection.[15],[16] However, as the restrictions due to COVID-19 pandemic relaxed, there was a surge of RSV infection. A group researcher from Australia reported rise in the number of cases during their spring months and peaked in their summer, instead of the typical fall and winter months. This study also reported the infection rate in under five population was higher than the expected.[17] News report from Texas of USA showing a stiff rise of RSV cases in the months of summer, which is not the typical season for the outbreak in that area.[18] Another early report from Japan also confirmed RSV outbreak.[19] We also experience similar observation in a tertiary care hospital from eastern India.

In our study, almost half (n = 44; 47.3%) of the ILI cases required PICU admission which constitutes 38.3% cases of total PICU admissions during August–September'21. Majority (81.8%) of the PICU admitted ILI cases were due to RSV infection which also constitutes about half (48%) of the total hospitalized RSV infection. Most of them (88.9%) were from infant age group. Nine (25%) PICU admitted RSV patient were intubated. Median hospital stay was 10 days (IQR 8–14). Like our study, another research from New York also described a delayed seasonal outbreak of RSV induced ILI, where almost 66.7% children got admitted in the hospital and out of them majority (81%) required PICU admission. Six patients were ventilated. The mean age of the cohort was 6 months and median hospital stay was 4 days.[20] In our study, hospital stay was longer as we only included PICU admitted children.

Bronchiolitis is one of the important manifestations of RSV infections. In United States, 72.4% of the virologically confirmed bronchiolitis cases are caused by RSV.[21] In our study, eight patients had X-ray pattern suggestive of bronchiolitis. Twenty-four patients (66.7% of PICU admitted RSV) fulfilled the criteria of ARDS. Although RSV traditionally is not considered as cause of ARDS, an 80% of a cohort of 1-to 4-month-old infants with RSV infection needing mechanical ventilation support fulfilled the clinical criteria of ARDS (Berlin) early upon admission.[22] Similarly, 15%–20% of the children with ARDS had RSV infection as underline trigger.[23],[24] There is significant gap to ascertain the role of viral infection in the development and progression of pediatric ARDS. Majority of information is mostly extrapolated from adult literature. In a recent study by López-Fernández et al. found that 19.8% of patients admitted to the PICU with ARDS tested positive for RSV, with a mortality of 13.7%.[25] Another study conducted in Netherlands over a period of 12 years analyzed 155 patients mechanically ventilated for RSV and they found that 83% of them progressed to ARDS.[22]

In our study, it was found that younger infants (1–6 months) and LBW infants significantly developed ARDS. ARDS children also had significantly high number of lung consolidations (>3 zone), pulmonary interstitial edema (>3 zones) detected by point of care USG; pediatric SOFA and PRISM III score. In a study conducted over 2147 children with LRTI due to RSV infection found that age <6 months, history of prematurity, chronic respiratory disease or congenital heart disease, and coinfection with adenovirus were significant predictors of increased disease severity.[26] Another study which analyzed both RSV and metapneumovirus-infected children found that both viruses were similarly associated with the development of PARDS and severe PARDS. However, neurologic comorbidity and higher PIM 3 score were found to be related with PARDS.[27]

Co-morbidity was present among one fourth children of our study cohort. Seventeen (47.2%) had LBW and one third (30.6%) were born premature. Two (5.6%) patients died, and they had comorbidities. Mortality is generally low (<1%) in the normal population. However, patients with chronic respiratory disease, cardiac disease, or immunodeficiency have an increased (3%–5%) risk of mortality.[28]

Bacterial culture from blood was positive in four patients among the ARDS group (vs. 1 in non-ARDS), but it was not statistically significant. Mini-BAL bacterial cultures were done in intubated patient only and our nasopharyngeal swab RT PCR test does not include bacterial pathogens; hence, we were not able to estimate the bacterial co-infection of respiratory tract. The study done by López-Fernández et al. found that 38% of RSV infection with PARDS patients also had a bacterial coinfection.[25]

Most of the studies conducted from India regarding RSV infection focused on epidemiology, symptomatology, and disease prevalence. Broor et al. reported the incidence rate of RSV infection (502/1000) in Indian children of 0–23 months of age.[29] We have not found any study reporting critically ill children with RSV infection from the intensive care unit (ICU) and describing their disease course and management protocol from India. Our study is the first to scientifically report this surge of ILI patients due to RSV infection and analyzed critically ill ICU admitted children. After COVID-19 s peak, RSV became one of the important causes of morbidity, ICU admission, and even mortality among the young children, especially those with co-morbidities, may be because of less exposure to the virus in previous year. This study will help the concerned authorities to develop effective management strategies and resource allocation to combat acute surge of respiratory tract infection among children.

Limitations

Our study also has some limitations. We were not able to estimate the percentage of RSV positive children required ICU admission in the entire population. We fail to compare RSV burden in our PICU with previous year, because this institution was declared as a dedicated COVID-19 unit in last year. We did not exclude culture positive children, although all symptoms in these children are not due to RSV alone. Small sample size is also a limitation. Further population-based multicentric studies require to identifying true impact and risk factors of severe RSV infection.


  Conclusions Top


Children in our study population with RSV infection predominantly presented with moderate to severe pneumonia and ARDS, in contrary to the typical bronchiolitis like presentation. Half of the admitted children received PICU support. Infants were most commonly infected. Early infancy (1–6 months) and LBW were the risk factors for developing ARDS. Although RSV can cause severe disease in vulnerable infants, mortality depends on underlying systemic comorbidity.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
McIntosh NA. Pediatric Pulmonary Medicine-Respiratory Syncytial Virus (RSV). University of Michigan Health System; 2004. Available from: http://www.med.umich.edu/1libr/PedPulmonary/RSV.pdf. [Last accessed on 20 Dec 2021].  Back to cited text no. 1
    
2.
Sricharoenchai S, Palla E, Pasini FL, Sanicas M. Epidemiology of respiratory syncytial virus lower respiratory tract infection (RSV-LRTI) in children in developing countries. J Trop Dis Public Health 2016;3:212.  Back to cited text no. 2
    
3.
WHO Director-General's Opening Remarks at the Media Briefing on COVID-19-11 March 2020. Available from: https://reliefweb.int/report/world/who-director-generals-opening-remarks-media-briefing-covid-19-11-august-2021?gclid=CjwKCAjwwo-WBhAMEiwAV4dybW0Ad2Z0RRIZpOYsY_Da2xwVHhEMehQD3Gkn9lua8MYA2CTangJDsxoComMQAvD_BwE. [Last accessed on 20 Dec 2021].  Back to cited text no. 3
    
4.
Karlsson EA, Mook PA, Vandemaele K, Fitzner J, Hammond A, Cozza V, et al. World Health Organization. Review of global influenza circulation, late 2019 to 2020, and the impact of the COVID-19 pandemic on influenza circulation. Wkly Epidemiol Rec 2021;96:241-64.  Back to cited text no. 4
    
5.
Mulholland K, Kretsinger K, Wondwossen L, Crowcroft N. Action needed now to prevent further increases in measles and measles deaths in the coming years. Lancet 2020;396:1782-4.  Back to cited text no. 5
    
6.
Children Dead, Hundreds in Hospital in Bengal. The Hindu; September 16, 2021. Available from: https://www.thehindu.com/news/national/other-states/hundreds-of-childrn-hospitalised-for-viral-infection-in-bengal/article36502718.ece. [Last accessed on 22 Dec 2021].  Back to cited text no. 6
    
7.
Ministry of Health and Family Welfare. Guideline on Categorization Seasonal Influenza Cases during Screening for Home Isolation, Testing, Treatment and Hospitalization; 2019. Available from: https://ncdc.gov.in/showfile.php?lid=361. [Last accessed on 20 Dec 2021].  Back to cited text no. 7
    
8.
Kliegman R. Nelson Textbook of Pediatrics. 21st ed. Philadelphia, PA: Elsevier; 2020.  Back to cited text no. 8
    
9.
World Health Organization. Pocket Book for Hospital Care of Children: Guidelines for the Management of Common Illness with Limited Resources. Geneva: World Health Organization; 2013. Available from: https://www.who.int/maternal_child_adolescent/documents/child_hospital_care/en/. [Last accessed on 22 Dec 2021].  Back to cited text no. 9
    
10.
Pediatric Acute Lung Injury Consensus Conference Group. Pediatric acute respiratory distress syndrome: Consensus recommendations from the Pediatric Acute Lung Injury Consensus Conference. Pediatr Crit Care Med 2015;16:428-39.  Back to cited text no. 10
    
11.
Matics T, Bubeck-Wardenburg J, Sanchez-Pinto N. 1332: The psofascore: A modified sequential organ failure assessment score for pediatric patients. Crit Care Med 2016;44:408.  Back to cited text no. 11
    
12.
Pollack MM, Patel KM, Ruttimann UE. PRISM III: An updated Pediatric Risk of Mortality score. Crit Care Med 1996;24:743-52.  Back to cited text no. 12
    
13.
Volpicelli G, Elbarbary M, Blaivas M, Lichtenstein DA, Mathis G, Kirkpatrick AW, et al. International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012;38:577-91.  Back to cited text no. 13
    
14.
Glezen WP, Taber LH, Frank AL, Kasel JA. Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child 1986;140:543-6.  Back to cited text no. 14
    
15.
Van Brusselen D, De Troeyer K, Ter Haar E, Vander Auwera A, Poschet K, Van Nuijs S, et al. Bronchiolitis in COVID-19 times: A nearly absent disease? Eur J Pediatr 2021;180:1969-73.  Back to cited text no. 15
    
16.
Yeoh DK, Foley DA, Minney-Smith CA, Martin AC, Mace AO, Sikazwe CT, et al. Impact of coronavirus disease 2019 public health measures on detections of influenza and respiratory syncytial virus in children during the 2020 Australian winter. Clin Infect Dis 2021;72:2199-202.  Back to cited text no. 16
    
17.
Foley DA, Yeoh DK, Minney-Smith CA, Martin AC, Mace AO, Sikazwe CT, et al. The interseasonal resurgence of respiratory syncytial virus in Australian children following the reduction of coronavirus disease 2019-related public health measures. Clin Infect Dis 2021;73:e2829-30.  Back to cited text no. 17
    
18.
RSV Cases on the Rise Across Texas. News; July 23, 2021. Available from: https://spectrumlocalnews.com/tx/south-texas-el-paso/news/2021/07/23/rsv-cases-on-the-rise-across-texas. [Last accessed on 20 Dec 2021].  Back to cited text no. 18
    
19.
Ujiie M, Tsuzuki S, Nakamoto T, Iwamoto N. Resurgence of respiratory syncytial virus infections during COVID-19 pandemic, Tokyo, Japan. Emerg Infect Dis 2021;27:2969-70.  Back to cited text no. 19
    
20.
Agha R, Avner JR. Delayed seasonal RSV surge observed during the COVID-19 pandemic. Pediatrics 2021;148:e2021052089.  Back to cited text no. 20
    
21.
Papadopoulos NG, Moustaki M, Tsolia M, Bossios A, Astra E, et al. Association of rhinovirus infection with increased disease severity in acute bronchiolitis. Am J Respir Crit Care Med 2002;165:1285-9.  Back to cited text no. 21
    
22.
Schene KM, van den Berg E, Wösten-van Asperen RM, van Rijn RR, Bos AP, van Woensel JB. FiO2 predicts outcome in infants with respiratory syncytial virus-induced acute respiratory distress syndrome. Pediatr Pulmonol 2014;49:1138-44.  Back to cited text no. 22
    
23.
Dahlem P, van Aalderen WM, Hamaker ME, Dijkgraaf MG, Bos AP. Incidence and short-term outcome of acute lung injury in mechanically ventilated children. Eur Respir J 2003;22:980-5.  Back to cited text no. 23
    
24.
López-Fernández Y, Azagra AM, de la Oliva P, Modesto V, Sánchez JI, Parrilla J, et al. Pediatric Acute Lung Injury Epidemiology and Natural History study: Incidence and outcome of the acute respiratory distress syndrome in children. Crit Care Med 2012;40:3238-45.  Back to cited text no. 24
    
25.
López-Fernández Y, Azagra AM, de la Oliva P, Modesto V, Sánchez JI, Parrilla J, et al. Pediatric Acute Lung Injury Epidemiology and Natural History study: Incidence and outcome of the acute respiratory distress syndrome in children. Crit Care Med 2012;40:3238-45.  Back to cited text no. 25
    
26.
Rodriguez DA, Rodriguez-Martinez CE, Cardenas AC, Quilaguy IE, Mayorga LY, Falla LM, et al. Predictors of severity and mortality in children hospitalized with respiratory syncytial virus infection in a tropical region. Pediatr Pulmonol 2014;49:269-76.  Back to cited text no. 26
    
27.
Ravindranath TM, Gomez A, Harwayne-Gidansky I, Connors TJ, Neill N, Levin B, et al. Pediatric acute respiratory distress syndrome associated with human metapneumovirus and respiratory syncytial virus. Pediatr Pulmonol 2018;53:929-35.  Back to cited text no. 27
    
28.
Tristram DA, Welliver RC. Respiratory syncytial virus. In: Long SS, Pickering LK, Prober CG, editors. Principles and Practice of Pediatric Infectious Diseases. 2nd ed. New York, NY: Churchill Livingstone; 2003. p. 213-8.  Back to cited text no. 28
    
29.
Broor S, Parveen S, Bharaj P, Prasad VS, Srinivasulu KN, Sumanth KM, et al. A prospective three-year cohort study of the epidemiology and virology of acute respiratory infections of children in rural India. PLoS One 2007;2:e491.  Back to cited text no. 29
    


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