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808
Atipotsawee Tungsupreechameth, M.D., Klaita Srisingh, M.D.
Department of Pediatrics, Faculty of Medicine, Naresuan University, Phitsanulok 65000, ailand.
Factors Associated with Severe Lower Respiratory
Tract Infection from Respiratory Syncytial Virus
(RSV) in Thai Children
ABSTRACT
Objective: To determine the factors associated with severe ALRTI from RSV in children.
Materials and Methods: A retrospective study of children aged 1-60 months were conducted from 2014 to 2018.
Out of 269 patients diagnosed with RSV ALRTI, 100 children were enrolled in the study, 20 had severe RSV
ALRTI, while 80 had non-severe RSV ALRTI as identied by the ReSVinet scale. A multivariable logistic model
was conducted to select signicant variables.
Results: During the study period, 269 patients were diagnosed with RSV ALRTI. Mean age was 10.45 ± 3.53 months.
Clinical manifestations of severe RSV ALRTI group had signicant dierence in abnormal general condition
(P < 0.001), tachypnea (P < 0.001), SpO
2
< 85% (P < 0.001), poor air entry in lungs (P < 0.001), and retraction
(P < 0.001). e factors associated with severe RSV ALRTI group, were underlying congenital heart disease [aOR
32.45; 95% CI 3.38-311.87, P = 0.003] and duration of hospital stay >5 days [aOR 19.56; 95% CI 1.81-212.05,
P = 0.014].
Conclusion: Factors associated with severe RSV ALRTI in children were underlying congenital heart disease and
duration of hospital stay >5 days.
Keywords: Lower respiratory tract infections; respiratory syncytial virus; risk factor (Siriraj Med J 2021; 73: 808-814)
Corresponding author: Klaita Srisingh
E-mail: klaitas@nu.ac.th
Received 28 May 2021 Revised 6 September 2021 Accepted 21 September 2021
ORCID ID: https://orcid.org/0000-0001-6398-9555
http://dx.doi.org/10.33192/Smj.2021.105
INTRODUCTION
RSV Acute lower respiratory tract infection (ALRTI)
causes severe lower respiratory tract illness in the acute
phase, leading to hospitalization, higher hospitalization costs,
and high mortality rates, especially in young children.
1-4
Approximately 66,000-199,000 died with RSV and 99%
of these deaths occurred in developing countries.
5
A
study in ailand reported an annual incidence rate of
RSV ALRTI was 5.8-534 cases per 100,000 populations;
however, the incidence rate may vary depending on
the age demographic and the area where the study is
conducted.
6-10
ailand is one of the developing countries facing
RSV ALRTI problems and there were limited data
about severe RSV ALRTI. e data available on RSV
infection are insucient to cause change in the country’s
policy.
6-10
ailand has no specic medical treatment
and currently using supportive care as the mainstay of
management for children with RSV ALRTI, identical
to other developing countries.
11
Prophylactic passive
immunotherapy using palivizumab - a monoclonal
antibody against RSV infection is a costly treatment in
ailand. Presently, palivizumab is not routinely used
in ai children and in other countries. ere are many
socio-cultural, demographic and environmental risk
factors that predispose children to acquire respiratory
tract infections especially RSV ALRTI.
12
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Since there are no updated data for severe RSV
ALRTI in ailand or information about the factors
related to severe infection, this study aimed to identify
the factors associated with severe RSV ALRTI in children.
e benets of this study include documentation and data
conrmation in order to recommend policy changes in
ailand about vaccine prioritization plan or palivizumab
dispensation for prophylaxis of the RSV ALRTI.
MATERIALS AND METHODS
Study design and setting
A retrospective case-control study was performed
on children were admitted to the the Naresuan University
Hospital from 2014 - 2018. e Ethics Committee approved
study protocol of the Human Research Study of Naresuan
University (No.0897/2019).
Denition
Weight and height of preterm in this study refer
to the weight and height of patients’ corrected age.
Corrected age is used to adjust the age of preterm
participants calculated using the equation: [corrected
age = Chronological age + (40 - Gestational age)]
Hospital-acquired pneumonia (HAP) refers to a
pneumonia with clinical evidence of a new lung inltrate
caused by an infectious agent (new onset of fever, purulent
sputum, leukocytosis, and a decrease in oxygenation)
that occurs 48 hours or more aer hospital admission
and is not incubating at the time of admission. Cultures
obtained from endotracheal aspirates are used to identify
etiologic agents.
Eligibility criteria
is study enrolled children aged between 1-60
months with acute lower respiratory tract infection
(ALRTI) diagnosis from Respiratory Syncytial Virus
(RSV) at time of data collection period.
Selection of cases and controls
e data collectors identied children diagnosed
with RSV ALRTI then used the ReSVinet scale as the
clinical scoring method to assess the disease severity.
13
e subjects were divided into two groups: the severe RSV
ALRTI group (cases) and non-severe RSV ALRTI group
(controls). e evaluation process utilized 7 parameters
(feeding intolerance, medical intervention, respiratory
diculty, respiratory frequency, apnea, general condition,
fever) that were assigned dierent values (from 0 to 3)
for a total of 20 points. A score greater than or equal to
14 is classied as severe RSV ALRTI. e control group
was selected based on ReSVinet scale score below 14
points, and applied gender matching.
Laboratory method
Nasopharyngeal swab specimens are processed
using the Quick Navi
TM
-RSV2 immunoassay (immuno-
chromatographic assay technique) (Denka Seiken Co.,
Ltd., Tokyo, Japan) to identify RSV.
Sample size determination
Population was estimated from the study of Zhang XB
and et al.
14
using a case-control study with binary formula
outcomes. Low birthweight, congenital heart disease,
bronchopulmonary dysplasia, and airway abnormalities
were found to be risk factors for severe respiratory syncytial
virus-associated acute lower respiratory tract infections
(p < 0.001).
P(exposure|case) = e proportions of exposure to
severe respiratory syncytial virus-associated acute lower
respiratory tract infections was 0.315.
P(exposure|control) = e proportions of exposure
to non- severe respiratory syncytial virus-associated
acute lower respiratory tract infections was 0.685.
Twenty patients from case group (severe RSV ALRTI)
and 80 patients from control group (non-severe RSV ALRTI)
were results of the calculations using P(exposure|case) =
0.315, P(exposure|control) = 0.685, Ratio (case:control)
= 1:4, Alpha = 0.05, Beta = 0.20.
Sampling procedure
e subjects were patients diagnosed with RSV
ALRTI. ose who scored greater than or equal to 14
in the ReSVinet scale were assigned to the severe RSV
ALRTI group (case group), while subjects with scores
below 14 points were in the non-severe RSV ALRTI
(control group). Matlab-program
15
was used to generate
a 1:4 (case: control) ratio, matching the sex and age of
the participants at random to complete the data.
Collected data
Naresuan University Hospital is a tertiary-care
University hospital in the lower northern part of ailand,
all admissions were recorded in the hospital’s database.
Coders enter the of clinical diagnoses information using
the International Classication of Disease 10
th
revision
(ICD-10). We identified subjects with a principal
diagnosis of acute bronchitis, bronchiolitis, pneumonia,
laryngotracheobronchitis and epiglottitis using the ‘J20,
J21, J12, J05’ ICD-10 codes (J205- acute bronchitis due
to respiratory syncytial virus, J209 - acute bronchitis,
unspecied, J210-acute bronchiolitis due to respiratory
syncytial virus, J219-acute bronchiolitis, unspecied;
J121- Respiratory syncytial virus pneumonia, J129
-viral pneumonia, unspecied; J050-Acute obstructive
laryngitis[croup], J051-Acute epiglottitis). We conrmed
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the RSV diagnosis through laboratory reports. Data
gathered were reviewed from the medical records.
Collected data comprised of the date of admission,
age, gender, weight, height, preterm birth, underlying
diseases, length of hospital stay, daycare attendance,
history of exposure to sick patients, second-hand smoke,
duration of illness prior to admission. Two physicians
(1 medical doctor, 1 pulmonologist) determined the
ReSVinet scale scores based on the patients admission
records and scores were used to categorize the case and
control groups. e data of illness were collected such
as general condition, fever, respiratory frequency, lung
sound, chest wall retraction, SpO
2
, history of apnea,
decreased appetite, and complications (e.g. secondary
bacterial infection), the clinical course (e.g. requiring
intensive care, mechanical ventilation, requiring oxygen
supplement).
Data and statistical analysis
e patients were divided into two groups, severe
RSV ALRTI and non-severe RSV ALRTI, based on the
score of the ReSVinet scale. Continuous variables were
compared between the two groups using the Student’s
t-test. Categorical variables were compared using the
Chi square test or Fisher’s exact test. Multiple logistic
regression analysis was used to identify the independent
factors associated with severe RSV ALRTI. All potential
risk factors showing a p value of <0.2 in the univariate
analysis were included in the regression model. Odds
ratios (OR) and 95% condence intervals (95% CI) were
calculated. Multiple logistic regression analysis was
performed to evaluate adjusted odds ratio (AOR) and
95% condence interval (95% CI). A two-tailed p-value
of <0.05 was considered statistically signicant. e
statistical analysis was performed using SPSS version
20.0 for Windows (SPSS Inc., Chicago, IL, USA).
RESULTS
Two hundred sixty-nine children between 1-60
months old were diagnosed with RSV ALRTI and were
admitted in Naresuan University hospital during the
course of the study. e participants were divided into
two groups using the ReSVinet scale method: twenty in
the severe RSV ALRTI group and 249 in the non-severe
RSV ALRTI group. e 249 patients in non-severe RSV
ALRTI were further divided using Matlab-program to
generate 80 participants randomly matched by sex and
age, and to satisfy the 1:4 (case:control) ratio (Fig 1). e
record showed RSV ALRTI from March to November, but
the upsurge of cases was between August to November
and documented the highest number in September. Mean
age was 10.45 ± 3.53 months. e mean weight in severe
Fig 1. Method of study.
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RSV ALRTI group was considerably lower than non-
severe RSV ALRTI group (7.20±1.18 kg vs. 9.71±0.45 kg,
P = 0.022). e mean height in the severe RSV ALRTI
group was 67.25±16.12 cm. and non-severe RSV ALRTI
group was 76.03±13.64 cm. (P = 0.015). Non-severe RSV
ALRTI cases group had a higher attendance rate at the
daycare center than severe RSV ALRTI group (32.5%
vs 5.0%, P = 0.013). e age, history of exposure to sick
patients, preterm birth, and second-hand smoke contact
had no signicant dierence in both groups. ere was
a statistically signicant dierence in the proportion of
patients with underlying disease between two groups,
70.0% in severe RSV ALRTI group while only 21.2%
non-severe RSV ALRT group (P < 0.001). Congenital
heart disease and pulmonary disease were the most
prevalent underlying conditions in severe RSV ALRTI
group (30.0% and 20.0%, respectively). e occurrence
bronchopulmonary dysplasia (BPD) in severe RSV ALRTI
group was higher than the non-severe RSV ALRTI group
but not signicantly dierent (10.0% vs 1.3%, P = 0.287).
ere was a substantial dierence in the duration of illness
before hospitalization ≤3 day-period and the duration
of hospital stay in >5 day-period. e respective results
were 65.0% vs. 38.7% (P = 0.034) and 95.0% vs. 62.5%
(P = 0.005) in severe RSV ALRTI group and non-severe
RSV ALRTI group. (Table 1).
TABLE 1. Characteristics data and factors associated of participants with severe RSV ALRTI and non-severe RSV
ALRTI.
Demographic data Severe RSV ALRTI Non-severe RSV ALRTI P value
(n=20) (n=80)
Age (months) (mean, SD) 10.45 (3.53) 14.94 (1.32) 0.160
c
Sex number (%) 0.158
a
Male 6 (30.0%) 24 (30.0%)
Female 14 (70.0%) 56 (70.0%)
Weight (kg) (mean, SD) 7.20±1.18 9.71±0.45 0.022
c
*
Height (cm.) (mean, SD) 67±16.12 76.03±13.64 0.015
c
*
Daycare attendance 1 (5.0%) 26 (32.5%) 0.013
a
*
History of exposure to sick patients 4 (20.0%) 28 (35.0%) 0.198
a
Preterm birth 6 (30.0%) 9 (11.2%) 0.072
b
Exposure to second-hand smoke 0 (0.0%) 0 (0.0%) N/A
Underlying disease 14 (70.0%) 17 (21.2%) <0.001
a
*
Congenital heart disease 6 (30.0%) 3 (3.8%) 0.002
b
*
Pulmonary disease 4 (20.0%) 9 (11.3%) 0.287
b
Asthma and allergic rhinitis 2 (10.0%) 8 (10.0%)
BPD 2 (10.0%) 1 (1.3%)
Hematologic disease 1 (5.0%) 2 (2.5%) 0.492
b
Neurologic disease 2 (10.0%) 2 (2.5%) 0.178
b
Other underlying disease 1 (5.0%) 1 (1.3%) 0.362
b
Duration of illness prior to admission
≤3 days 13 (65.0%) 31 (38.7%) 0.034
a
*
>3 days 7 (35.0%) 49 (61.3%)
Duration of hospital stay >5 days 19 (95.0%) 50 (62.5%) 0.005
a
*
Complications
HAP 19 (95.0) 38 (47.5) < 0.001
a
*
Requiring ICU 18 (90.0) 3 (3.8) < 0.001
a
*
Oxygen supplementation < 0.001
b
*
Low ow 1 (5.0) 74 (92.5)
High ow and non-invasive 5 (25.0) 6 (7.5)
Mechanical ventilator 14 (70.0) 0 (0.0)
a
Chi-Square Tests,
b
Fisher's Exact Test,
c
Independent t-test, *p<0.05,
Abbreviations: N/A = Not available, BPD = Bronchopulmonary dysplasia, HAP= Hospital-acquired pneumonia, ICU= intensive care unit
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On rst-time admission, clinical manifestations
of patients with severe and non-severe RSV ALRTI
had signicant dierences in tachypnea (for infant <2
months, respiratory rate >60 /min; for children 2-12
months, respiratory rate >50 /min; for children >1-5
years, respiratory rate >40 /min) (P < 0.001), SpO
2
<85%
(P < 0.001), lung sound (poor air entry) (P < 0.001),
and all retraction (suprasternal notch, intercostal and
subcostal retraction) (P < 0.001). In contrast, there were
no statistical dierences in relation to abnormal general
condition (e.g. lethargy, discomfort, agitation), fever
and decreased appetite in both groups. No apnea was
observed in all patients.
When compared to patients with non-severe RSV
ALRTI, patients with severe RSV ALRTI had a higher
rate of HAP (95.0% vs. 47.5%, P < 0.001). e common
pathogens of HAP found in our study were aerobic
gram-negative bacilli [Acinetobacter baumannii (95%),
Pseudomonas aeruginosa (2%), Escherichia coli (1.8%),
Klebsiella pneumoniae (1%), Enterobacter spp. (0.2%)].
In addition, the number of patients with severe
RSV ALRTI that required intensive care and mechanical
ventilation was higher than the number of cases of non-
severe RSV ALRTI (90.0% vs 3.8%, P < 0.001 and (70.0%
vs.0.0%, P < 0.001, respectively). All patients needed
oxygen supplementation during admission.
Our research recorded four patient deaths (4.0%),
three of them had underlying congenital heart diseases
[1 case with dextrocardia, ventricular inversion, pulmonary
stenosis (PS), patent ductus arteriosus (PDA); 1 case with
CoA; and 1 case with ventricular septal defect (VSD)],
and one had underlying asthma, all of whom were in
the severe RSV ALRTI group.
e results of the multiple logistic regression analysis
adjusted by sex, age, daycare center attendance, and
duration of illness prior to admission 3 days revealed the
following risk factors for severe RSV ALRTI: underlying
cardiovascular disease [aOR 32.45; 95% CI 3.38-311.87,
P = 0.003], and hospital stay >5 days [aOR 19.56; 95%
CI 1.81-212.05, P = 0.014] (Table 2).
DISCUSSION
is study showed that underlying cardiovascular
diseases particularly congenital heart disease is one of
the risk factors for severe RSV ALRTI (aOR = 32.45),
which is comparable to previous studies.
14,16-21
Infants
with congenital heart disease have increased risk for
severe RSV ALRTI with higher morbidity (need for
assisted ventilation and longer duration of oxygen
supplementation) and higher mortality rate of 37% as
rst reported by MacDonald, et al.
22
Congenital heart
disease and RSV-related rehospitalization rate were
recorded at 3.0-16.4% in developed countries.
16-19,21,23,24
is study supports the hypothesis that congenital heart
disease (CHD) increases the risk for severe RSV ALRTI.
Furthermore, the present study revealed that a hospital
stay of more than 5 days is also a concomitant risk factor
for severe RSV ALRTI, which is approximately 20 times
more common than non-severe RSV ALRTI. is nding
may suggest that care providers pay more attention to this
group due to the slow recovery from disease and the need
to avoid HAP. In our study, HAP was found to be 95.0%
in the severe RSV ALRTI group. As a result, patients may
undergo procedures to avoid disease-related complications,
such as the insertion of intravenous catchers for uid
resuscitation and dehydration, intravenous antibiotics
in case of bacterial superinfection, or airway suctioning
for clearing secretions. Appropriate management which
consists of alcohol-based disinfection and hand washing
with alcohol-based rubs or soaps, is extremely eective in
reducing RSV transmission and preventing nosocomial
infections. We found that nosocomial infection was
associated with severe RSV ALRTI group (P < 0.001) and
the most common pathogen was Acinetobacter baumannii
TABLE 2. Multivariable analysis of risk factors of severe RSV-associated acute lower respiratory tract infections.
Factors
Multivariable analysis
AOR 95% CI P value
Underlying cardiovascular disease 32.45 3.38-311.87 0.003
Duration of hospital stay >5 days 19.56 1.81-212.05 0.014
Adjusted by sex, age, daycare center attendance, duration of illness prior to admission ≤ 3 days
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as reported by other studies.
20,22,25,26
e number of infants
admitted to hospitals during RSV season can be very
high, resulting in overcrowded pediatric wards and an
excessive workload for the sta. Furthermore, staying in
the hospital for longer periods of time may increase the
risk of cross-bacterial antimicrobial resistance infections.
us, the importance of systematic preventive measures
such as isolation of infected infants in single rooms, and
handwashing are highly recommended.
Groothuis, et al
27
were the rst to study the burden
of early rehospitalization in infants with BPD due to
RSV infection. However, we do not consider preterm
birth and BPD as associated factors for severe RSV ALTI
(P 0.287). is is so because our study had recorded
preterm births of 6 out of 20 patients with severe RSV
ALRTI (30.0%) and 9 out of 80 from non-severe RSV
ALRTI group (11.2%) (P = 0.072). Moreover, the number
of patients with underlying BPD was small (2 out of 20
(10.0%) patients from severe RSV ALRTI group and 1
out of 80 (1.3%) from non-severe RSV ALRTI group),
and the majority of the patients in both groups were
born at term (70% in severe RSV ALRTI and 89.8% in
non-severe RSV ALRTI).
Multivariable analysis revealed that daycare attendance,
direct contact with sick patients prior to hospital admission,
duration of illness prior to admission, and history of
exposure to sick patients were not considered as risk
factors for severe RSV ALTI, which contradicted the
results of previous studies conducted in developed
countries.
16,23,28
is is partly explained by the limited
utilization of daycare centers in the study population
particularly in patients with severe RSV ALRTI (5%).
A number of limitations should be considered in
this current study. First, this research is retrospective,
wherein the ReSVinet scores of the participants were
based on their admission records instead on the peak
of severity of the disease. Second, this cross-sectional
study has small sample size. Finally, a full range PCR
for the respiratory viral panel could not be performed.
Notwithstanding these limitations, prospective studies
should be carried out to clarify the correlation of associated
factors.
CONCLUSION
Our study demonstrated that factors associated
with severe RSV ALRTI in children include underlying
cardiovascular diseases and duration of hospital stay >
5 days.
ACKNOWLEDGMENTS
e authors would like to thank Miss Kornthip
Jeephet, Statistics Technical Ocer, Research Center
of the Faculty of Medicine, Naresuan University for
statistical analysis, and Miss Judely Marish Cañete, Miss
Daisy Gonzales, International Relations Section, Faculty
of Medicine, Naresuan University for their assistance in
revising and editing the manuscript.
Conicts of interest: ALL of the authors declare no
conict of interest.
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