European Journal of Pediatrics (2018) 177:913–920

https://doi.org/10.1007/s00431-018-3138-6

ORIGINAL ARTICLE

Characteristics of children admitted to intensive care

with acute bronchiolitis
Marwa Ghazaly 1,2 & Simon Nadel 1,3

Received: 28 December 2017 / Revised: 27 March 2018 / Accepted: 28 March 2018 / Published online: 13 April 2018
# The Author(s) 2018

Abstract
To assess factors associated with outcome in children admitted to paediatric intensive care (PIC) with bronchiolitis. A retrospec-
tive study of children admitted to the PICU at St Mary’s Hospital, London with bronchiolitis over a 6-year period (2011–2016).
All bronchiolitis admissions < 2 years were included. Data collected particularly noted risk factors for severity, demographics,
microbiology and outcome. We compared respiratory syncytial virus (RSV) with non-RSV status. Multivariate analysis was
performed. Two hundred seventy-four patients were identified. Median age was 60 days (IQR 28–150 days), 63% were male,
90% were invasively ventilated and 42% were previously healthy. Pre-existing co-morbidities were present in 38%. The most
frequently isolated pathogens were RSV (60%) and rhinovirus (26%). Co-infection was present in 45%, most commonly with
RSV, rhinovirus and bacterial pathogens. Median length of stay (LOS) was 6 days (IQR 4.75–10). Younger age, prematurity,
RSV, co-infection and co-morbidity were identified as significant risk factors for prolonged LOS. Six children died. Five of these
had documented co-morbidities.
Conclusion: RSV causes more severe bronchiolitis than other viruses. Nearly half of children admitted to PICU with RSV
were previously healthy. Current guidelines for immunoprophylaxis of RSV bronchiolitis should be re-considered.

What is Known:
• Bronchiolitis is one of the most common reasons for unplanned PICU admission. The most common virus causing bronchiolitis is RSV
• Bronchiolitis severe enough to require admission to PICU is associated with frequent morbidity but has low mortality.
What is New:
• RSV causes more severe bronchiolitis than other viruses.
• Nearly half of all children admitted to PICU with RSV were previously healthy.

Keywords Bronchiolitis . Children . Outcome . Intensive care . Ventilation . Co-morbidity . RSV

Abbreviations HFOV High-frequency oscillatory ventilation

CMV Cytomegalovirus ICU Intensive care unit
CPAP Continuous positive airway pressure IQR Interquartile range
ECMO Extracorporeal membrane oxygenation LOS Length of stay
ETT Endotracheal tube NPA Nasopharyngeal aspirate
PIC Paediatric intensive care
Communicated by Piet Leroy PICU Paediatric intensive care unit
RSV Respiratory syncytial virus
* Simon Nadel
[email protected]
Marwa Ghazaly
[email protected] Introduction
1
Paediatric Intensive Care Unit, St. Mary’s Hospital, Imperial College Acute bronchiolitis is a leading cause of hospitalization in
Healthcare NHS Trust, Praed Street, London W21NY, UK young children. Although children with bronchiolitis do not
2
Pediatric Department, Assuit University Hospital, Assuit University, usually require hospitalization, approximately 3% of affected
Assiut, Egypt children are admitted to hospital [7, 30].In the developed
3
Imperial College London, London, UK world, infants aged < 1 year with bronchiolitis account for
914 Eur J Pediatr (2018) 177:913–920

18% of all paediatric hospital admissions [13]. In December aged <2 years with a recorded diagnosis of bronchiolitis using
2011 in England, there were 30,451 hospital admissions for the SNOMED diagnostic code.
bronchiolitis [6]. Bronchiolitis admission rates in infants un-
der 1 year have previously been estimated to be 24.2 to 31.2
per 1000 in the UK and USA, respectively [4, 12, 21]. Exclusion criteria
Most children hospitalized due to acute bronchiolitis have
an uneventful course [3, 15]; however, approximately 2–6% Patients with missing records (two patients).
requires admission to a paediatric intensive care unit (PICU),
with 2–3% of hospitalizations requiring invasive mechanical
ventilation [13]. Acute bronchiolitis accounts for around 13% Data collection
of PICU admissions in the UK [9], thus being a significant
burden on PICU beds, with a Bwinter surge^ in activity occur- We reviewed all identified children’s medical records to
ring predictably each November to February [7, 11, 12, 29]. collect clinical data, including from the pre-hospitalization
Prior studies have identified risk factors associated with illness, the initial presentation to the emergency department
hospitalization for bronchiolitis, including prematurity, youn- and the child’s inpatient course prior to PICU admission,
ger age, environmental factors (e.g. passive smoking, crowded including vital signs, medical management and PICU out-
household) and presence of co-morbidities (e.g. chronic pul- come. We particularly noted recognized risk factors for se-
monary disease, congenital heart disease, immunodeficiency, verity, admission data, demographic data, microbiology and
neurologic disease) [4, 18, 28, 31]. However, few studies have outcome.
yet described factors associated with PICU admission and
outcome.
Despite the high hospitalization rate associated with bron- Pathology
chiolitis, it is however uncommon for bronchiolitis to cause
death. Data from children with bronchiolitis due to the most All children had standardized sample collection on admission
commonly associated cause—respiratory syncytial virus to PICU. This included nasopharyngeal aspirate (NPA) for
(RSV)—notes that deaths are rare in the developed world virus isolation, blood cultures, endotracheal tube (ETT) aspi-
and range from 2.9 (UK) to 5.3 (USA) per 100,000 children rate in intubated patients for bacteria and other relevant cul-
below 12 months [7, 30]. In October 2009 in England, there tures depending on clinical presentation. All samples were
were 72 recorded deaths of children within 90 days of hospital collected and analysed using a standardized protocol: The
admission for acute bronchiolitis [6]. NPA samples taken on PICU admission were tested for virus-
es using rapid direct immunofluorescence and/or real-time
multiplex PCR for the following respiratory panel: RSV; rhi-
Aim novirus; adenovirus; parainfluenza viruses 1, 2 and 3; and
influenza virus A and B. Extended analyses were conducted
We aimed to investigate factors associated with outcome in on NPA or ETT specimens depending on advice from the
children with a diagnosis of bronchiolitis admitted to a single Infectious Diseases Service. The results of all other bacterial
PICU over a 6-year period, between January 2011 and cultures on respiratory specimens, urine, blood, mucous mem-
December 2016. brane cultures are also recorded.
Some infants had similar diagnostic samples taken at their
local hospital, prior to PICU admission. These results were
Methods obtained and collated for each admission where available.
All patients also had routine hematology and biochemistry
Study design samples taken on admission to PICU.

We performed a retrospective observational study in children

admitted to the PICU at St Mary’s Hospital, London, UK. The Statistical analyses
PICU at St Mary’s is a general PICU, with approximately 330
admissions per year. Data were expressed as descriptive statistics as number and
percentage or median and interquartile range (IQR), as appro-
Inclusion criteria priate on Excel 2007.
Univariate analysis, Fisher exact test, chi square test and
Patients were identified using the electronic database of PICU multiple logistic regression analysis were performed using
admissions (Careview, Phillips, UK). We included all patients SPSS 16.
Eur J Pediatr (2018) 177:913–920 915

Results Co-morbidities (Table 2)

We identified 274 children who fulfilled the inclusion criteria. Excluding extreme prematurity, previously existing co-
The total number of PICU admissions in this period was 1967 morbidities were recorded in 103 (38%) of children, with
patients; therefore, children with bronchiolitis constituted 60% of these having more than one co-morbidity. The most
13.5% of all PICU admissions. frequently observed known co-morbidities were gastroesoph-
The majority of patients (173, 63%) were males and 100 ageal reflux disease (47, 17%), cardiac anomalies (44, 16%),
(36%) were Caucasian (Table 1). The median age of children chronic lung disease (including bronchopulmonary dysplasia)
admitted to PICU with bronchiolitis was 60 days (IQR 28– in 36 (13%) and known neurological abnormality in 19 (7%).
150 days). Across all years of the study, children in the first
42 days of life were the most common age group admitted.
Overall, children < 1 year of age accounted for 97% of admis- Microbiology (Table 3)
sions with bronchiolitis.
Respiratory syncytial virus (RSV) was the most frequently
isolated pathogen, being found in 165 (60%) children. In 85
Risk factors for severe disease children, RSV was the only organism isolated, and in 80 chil-
dren, this was found in association with another pathogen.
Children born during the UK RSV season (October to March) Rhinovirus was the next most frequently detected pathogen,
accounted for 173 (63%) of cases; 174 (64%) children were found in 71 (26%) children, and 21 (8%) were infected with
bottle fed; 41 (15%) children were living with a single parent; human metapneumovirus.
33 (12%) of children were living in a household with at least Detection of multiple pathogens was common and seen in
one smoker. The mean number of householders was 4.4 with 123 (45%) of children. Any virus found together with a bac-
range 3–13. A positive family history of allergy was present in terial co-isolate was recorded in 95 (36%) children. The most
44 (16%) of patients. commonly isolated bacteria were Haemophilus influenzae and
One hundred twenty-six (46%) of PICU admissions with Staphylococcus aureus. The most common sites to find asso-
bronchiolitis were ex-premature infants (≤ 37 completed ciated bacteria were endotracheal aspirate in 54 (19.7%) and
weeks gestation), 30 (11%) had been born at ≤ 28 weeks ges- blood culture in 19 (7%) children. No patients had bacteria as
tation. Eighty-five (31%) infants had been previously admit- the sole organism identified as a cause of bronchiolitis. The
ted to a neonatal ICU; 35 (12%) infants were admitted only to blood culture positivity was primarily thought to be contami-
a special care baby unit (SCBU). Median birth weight of all nants. We do not routinely carry out throat cultures in infants
admissions was 2.1 kg (IQR 1.6–2.9 kg) in cases where birth admitted with presumed viral bronchiolitis. No organism was
weight data were available (n = 107). Median PICU admission detected in 28 (10%) of children.
weight was 4 kg (IQR 3–6.2 kg). Apnea was the primary Ten children had received palivizumab during the same
cause for admission in 102 (37%) of the cases, two thirds of season they were admitted (three had a cardiac indication; five
these being ex-premature infants (n = 68). had chronic lung disease of prematurity; two were extremely

Table 1 Demographics and admission characteristics of bronchiolitis- Table 2 Co-morbidities identified in children admitted to PICU with
related ICU admissions, 2011–2016 bronchiolitis

Bronchiolitis-related ICU admissions (n) 274 (%) Number 103 (38%)

Male sex 173 (63%) Gastro-esophageal reflux disease 47 (17%)
Caucasian 100 (36%) Cardiac abnormality 44 (16%)
Median age in days (range) 60 (28–150 days) Chronic lung disease 36 (13%)
Exclusively breastfed 80 (29%) Neurological 19 (7%)
Exclusively bottle fed 174 (63%) Airway abnormality 18 (7%)
Median birth weight (available 2.3 kg Trisomy 21 7 (3%)
in only 107 patients where available) Other chromosomal abnormalities 6 (2%)
Prematurity 126 (46%) Allergy 5 (2%)
Household smoking 32 (12%) Renal anomaly 4 (1.5%)
Previous NICU admission 85 (31%) Other syndromes 4 (1.5%)
Pre-existing co-morbidity 103 (38%) Congenital infection 3 (1%)
Family history of atopy 44 (16%) Immune deficiency 3 (1%)
Median (range) number of house holders 4.4 (3–13)
Please note: 60% of these patients had more than one co-morbidity
916 Eur J Pediatr (2018) 177:913–920

Table 3 Infectious agents identified in children with bronchiolitis Table 4 Mode of ventilation and outcome of children admitted to
paediatric intensive care with bronchiolitis
Microbiology result Single Co-infection Total Percent
infection Non-invasive ventilation (CPAP) only 27 (10%)
Invasive ventilation 247 (90%)
Viruses
High-frequency oscillation 50 (18%)
RSV 85 80 165 60%
Median length of PICU stay (interquartile range) days 6.5 (5–10)
Rhinovirus 17 54 71 26%
Need for CPAP after extubation 144 (53%)
Adenovirus 1 17 18 7%
Mortality 6 (2%)
Human 6 15 21 8%
Complications 47 (17%)
Metapneumovirus
Parainfluenza 2 7 9 3%
CPAP continuous positive airway pressure
Influenza A 1 1 2
Influenza B 1 0 1
sepsis. Ten children had vascular complications (i.e. deep ve-
CMV 0 4 4 1%
nous thrombosis or arterial thrombosis).
Bacteria 95 95 36%
H. influenzae 0 27 27 10%
Predictors of length of PICU stay as a measure
Staph. aureus 0 22 22 8%
of severity of bronchiolitis
Enterobacter sp. 0 14 14 5%
Streptococcus species 0 10 10 4% To identify predictors of length of PICU stay as a marker of
Moraxella catarrhalis 0 10 10 4% severity of illness, we performed multiple linear regression
Pseudomonas aeruginosa 0 12 12 4% analyses. The following factors were noted to be significantly
Klebsella sp. 0 8 8 3% associated with longer length of PICU stay: younger age at
E. coli 0 7 7 3% admission (p = 0.046), gestational age (p = 0.002); birth
Candida albicans 0 9 9 3% weight (p < 0.0001), invasive ventilation (p < 0.0001), RSV
Coagulase—negative 0 6 6 2% infection (p = 0.0065), co-morbidity (p = 0.0005), co-
Staph
Others 0 4 4 1%
infection (p = 0.0001).
We also carried out further regression analysis using days
RSV respiratory syncytial virus, CMV cytomegalovirus of invasive ventilation days as the outcome in order to exclude
bias. The high proportion of co-morbidity and prematurity in
premature). Three of these had RSV infection identified as the our cohort is likely to have been associated with a requirement
cause of their PICU admission. for longer duration of invasive ventilation, requirement for
non-invasive ventilatory support post-extubation and hence
Outcome (Table 4) prolonged LOS. Following this further regression analysis,
the only significant risk factor was the age at admission (p =
All children admitted to PICU required some form of respira- 0.04).
tory support. The median length of PICU stay was 6.5 days
(range 18 h to 52 days); 247 (90%) children required tracheal Differences between children with RSV and non-RSV
intubation and mechanical ventilation. Fifty of these were bronchiolitis (Table 5)
treated with high-frequency oscillatory ventilation (HFOV)
for a period of their mechanical ventilation. To determine if infection with RSV was particularly associat-
One hundred forty-four (58%) patients who required inva- ed with differences in outcome compared to infection with
sive ventilation required non-invasive respiratory support with other pathogens, we compared the demographic characteris-
continuous positive airway pressure (CPAP) following tics and risk factors in children who were infected with RSV
extubation. Twenty-seven (10%) patients required only and those without RSV. RSV infection was more common in
CPAP during their PICU admission. term infants than preterm; the median gestational age in chil-
Complications were observed in 47 (17%) infants, most of dren with RSV was 38 weeks, compared with 36 weeks in the
them related to their current illness or management. Twelve non-RSV group (p < 0.02).
(4%) patients suffered with pulmonary haemorrhage within RSV was also more common in younger infants; the me-
24 h following extubation, all requiring re-intubation; 10 pa- dian age for admission was 48 days in babies with RSV, com-
tients were diagnosed with co-existent shock (defined by the pared with 90 days in non-RSV patients (p < 0.004).
need for fluid resuscitation and inotropic support); 9 children Seventy percent of the children with RSV bronchiolitis
had a pneumothorax at the time of admission; 4 had cardiac were ≤ 2 months of age compared with 41% of those without
failure and arrthymia; and 4 had coagulopathy associated with RSV (p < 0.0005). Forty-five percent of the children with
Eur J Pediatr (2018) 177:913–920 917

Table 5 Comparison between

RSV positive and non-RSV Demographic characteristics RSV positive Non-RSV p value
children (n = 165) (n = 109)

Median gestational age of admissions (weeks) 38 36 0.02

Mean weight on admission, kg 4.5 ± 2.2 5.17 ± 2.7 0.03
Median age, days 48 90 0.004
0–2 months 104 45 0.0005
3–5 months 33 28
6–11 months 19 30
1 2–24 months 9 6
Male 99 (60%) 75 (70%) 0.12
Female 66 (40%) 34(30%)
Risk factors
Prematurity, gestational age at birth: weeks 0.03
≤ 28 11 19
29–32 17 14
32–35 31 13
35–37 12 11
Congenital heart disease 24 20 0.4
Chronic lung disease 14 22 0.0063
Other co-morbidity 90(55%) 68(62%) 0.18
Co-infection 85(52%) 53(48%) 0.6
Parameters of disease severity
Median length of stay, (IQR [25th–75th percentile]) 7 days (5–11) 6 days (4–9) 0.02
Invasive ventilatory support 152 94 0.11
Patients receiving HFOV 31 19 0.77
Patients treated only with NIV 12 15 0.08
Need for CPAP after extubation 98 48 0.01
Complications 34 15 0.15

IQR interquartile range, HFOV high-frequency oscillation ventilation, NIV non-invasive ventilation, CPAP con-
tinuous positive airway pressure

RSV bronchiolitis were previously healthy, with no obvious Only one child who died had no underlying co-morbidity
identifiable risk factors. or prematurity. This was a previously healthy child with acute
Disease severity was significantly worse in children with adenovirus infection who died after referral for ECMO.
RSV bronchiolitis in some of the parameters evaluated, in- Four children who died were ex-premature babies; two had
cluding median length of PICU stay, need for continuing re- underlying immunodeficiency, one had trisomy 21, one had
spiratory support after extubation and need for supplemental severe chronic lung disease of prematurity and one had con-
oxygen after extubation, and there was a trend toward more genital myotonic dystrophy. Two of the deaths had multiple
severe disease observed in other parameters, such as the need congenital anomalies.
for tracheal intubation, requirement for HFOV and develop-
ment of complications.
Microbiology in children who died

Mortality Three (50%) children who died had RSV; one had only RSV
infection; one had RSV, adenovirus and Bordetella pertussis
Six deaths in children with bronchiolitis were recorded over (this patient was sent for ECMO and died on ECMO); one had
the study period (2.2% of all bronchiolitis-related PICU ad- RSV and Pneumocystis jiroveci. Three had rhinovirus; one of
missions). The median age of children who died was these had rhinovirus and E. coli; one had rhinovirus, adenovi-
4.5 months (range: 56–270 days). Median LOS among deaths rus and Enterobacter sp.; and one had rhinovirus and
was 20 days (range 6–63 days). Pseudomonas aeruginosa.
918 Eur J Pediatr (2018) 177:913–920

Discussion diagnostic methods are sub-optimal, and in these critical

cases, it may be appropriate to carry out extended methods
Our study presents a comprehensive review of the character- for pathogen detection. However, with no effective antiviral
istics and clinical outcomes of children admitted to a single therapies yet available, the necessity to do this for diagnostic
PICU in London, UK, with a clinical diagnosis of acute bron- purposes, rather than for infection control or public health
chiolitis. While only examining a single unit’s admissions, we measures, remains unclear.
feel this is a representative sample of admissions to PICUs in Consistent with previous studies [8, 9], the median length
the UK. Our unit is primarily a medical PICU, taking predom- of PICU stay among bronchiolitis admissions was ~ 6 days.
inantly unplanned acute admissions. The proportion of chil- This was significantly longer in those children with RSV in-
dren admitted to this PICU is reflective of the data observed fection compared to the non-RSV group. As seen in these
by Green et al., who found that infants aged < 1 year previous studies, RSV infection also appeared to be associated
accounted for 93% of all PICU bronchiolitis admissions in with relatively more severe disease, as determined by higher
England and 11.8% (95% CI 10.5 to 13.1%) of PICU admis- numbers of children requiring post-extubation respiratory sup-
sions in England each year. They estimated the PICU admis- port and supplemental oxygen.
sion rate for bronchiolitis to be between 1.3 and 1.6 per 1000 Length of stay in the PICU may not be a very objective
infants aged < 1 year [9]. endpoint to evaluate disease severity as it is confounded by
In our study, infants aged < 1 year accounted for 97% of all other factors such as co-morbidity. For example, patients may
admissions to our PICU with bronchiolitis. The majority of be observed for longer on PICU or clinicians may have a
our cases were infants aged ≤ 2 months (n = 150), and 70% of lower threshold for initiating CPAP after a period of mechan-
these were RSV positive, suggesting that younger infants are ical ventilation. Therefore, duration of invasive mechanical
more vulnerable to severe RSV disease, which is consistent ventilation may be a better endpoint from this point of view.
with the findings from previous studies [12, 18, 28].The asso- Our regression analysis confirmed this, and only age on ad-
ciation of younger age and prematurity with an increased risk mission was found to be a statistically significant factor when
of PICU admission was not unexpected and has been well allowing for pre-existing co-morbidity.
described previously. Prematurity was common in our cohort of patients, ac-
RSV was the most common virus identified in our study counting for nearly half (46%) of all patients, with extremely
(60%). In most studies, it accounts for 60–80% of bronchiol- preterm infants (≤ 28 weeks gestation) accounting for 11% of
itis cases in children below 12 months of age [14, 22, 23, 26]. cases admitted to PICU, compared to only 3% of hospitalized
Rhinovirus was the second most common virus detected children in previous studies [9, 21], although no other studies
(26%), followed by human metapneumovirus (7%), have focused purely on PICU admission with bronchiolitis.
parainfluenza, adeno- and influenza viruses (1–8%). Dual in- One study from Taiwan which examined risk factors associ-
fections were found in 46% of children in our study, while it ated with death in patients with severe RSV found that almost
has been reported in 20–40% of patients in previous studies 50% of their patients admitted to their PICU were premature,
[14, 20, 22, 23, 26]. Some studies suggest that co-infection is and 25% had a nosocomial RSV infection [16]. None of our
associated with more severe disease [5]. However, it is some- patients was found to have a nosocomial cause for their acute
times hard to determine the pathogenicity of co-infecting vi- bronchiolitis illness. Moreover, we found prematurity partic-
ruses, particularly rhinovirus. Co-infection was also a signifi- ularly associated with admission for apnea, being found in
cant determining factor for length of PICU stay in our study. 66% of all admissions to PICU for apnea in the context of
Richard et al. [25], also reported an increased risk of admis- bronchiolitis [27].
sion to the ICU when a dual viral infection was found, but the In our study, 38% of the admissions to PICU with bronchi-
population in their study included many premature infants and olitis had documented co-morbidities prior to admission or
children with underlying chronic illnesses. In contrast, discovered during their admission for bronchiolitis. This dif-
Marguet et al. [17] did not find any difference in bronchiolitis fers from previous studies which identified co-morbidity in
severity in patients solely infected with RSV compared to only 24–27% of hospital admissions with bronchiolitis [8,
those with RSV—rhinovirus co-infection. As the numbers of 12] but is fewer than the study from Taiwan quoted above,
children with co-infection in our cohort and in other reports where 72% of patients admitted to PICU with RSV had a co-
are significant, efforts to determine the contribution of more morbidity [16]. However, this is an important message—in
than one infecting virus would be an important element in any children admitted to PICU with bronchiolitis, a careful search
efforts to promote antiviral or preventative therapy for for underlying cardiac, pulmonary, or neurological disease
bronchiolitis. should be undertaken in what are thought to be previously
Eight percent of children in our study had rhinovirus as the healthy children. This may unmask a condition that may pre-
only identified pathogen and 10% of children had no pathogen dispose the infant to more frequent or more severe respiratory
identified at all. This suggests that our current routine infection.
Eur J Pediatr (2018) 177:913–920 919

There is evidence that children with underlying co- Compliance with ethical standards
morbidities who should have received RSV-prophylaxis do
not always receive it [1]. Our study and other studies have Conflict of interest The authors declare that they have no conflict of
interest.
demonstrated that current guidelines for RSV-prophylaxis
may exclude many patients who are at high risk but who do
Ethical approval All procedures performed in studies involving human
not fulfil the current guidelines for prophylaxis and suggests participants were in accordance with the ethical standards of the institu-
that further analysis to determine those patients who may ben- tional and/or national research committee and with the 1964 Helsinki
efit most from RSV-prophylaxis is required. Use of agents declaration and its later amendments or comparable ethical standards.
This study was discussed the with local Ethics committee, and they
such as palivizumab has been shown to reduce the burden of decided that ethical approval was not required due to the retrospective
hospitalization and mortality in bronchiolitis in a cost- nature of the study and the fact that all subject data was anonymized.
effective manner [2, 19, 24]. However, if our data is represen-
tative of PICU admissions for bronchiolitis across the devel- Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://
oped world, other factors may need to be taken into account creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
when deciding on eligibility for palivizumab or other similar distribution, and reproduction in any medium, provided you give appro-
agents. Additionally, developments in RSV vaccines suggest priate credit to the original author(s) and the source, provide a link to the
that many admissions to PICU could be prevented by effective Creative Commons license, and indicate if changes were made.
maternal immunization [10].

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