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http:// ijp.mums.ac.ir
Original Article (Pages: 8015-8023)
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Minor Diagnostic Factors in Ventilator Associated Pneumonia in

Children
Gholamreza Khademi1, Mojtaba Lotfi2, Elham Bakhtiari3, Bahare Imani2, *Mohammad
Hassan Aelami41
1
Neonatal Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
2
Department of Pediatric, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
3
Research Center for Patient Safety, Mashhad University of Medical Sciences, Mashhad, Iran.
4
Department of Pediatrics & Hand Hygiene and Infection Control Research Center, Mashhad University of
Medical Sciences, Mashhad, Iran.

Abstract
Background: Ventilator-associated pneumonia (VAP) is nosocomial pneumonia. Minor diagnostic
criteria in children are poorly understood. Present study aimed to determine the new diagnostic factors
for VAP in children admitted in the intensive care unit according to clinical, laboratory, and
radiological assessments.
Materials and Methods
One hundred thirty pediatric intensive care unit (PICU) admitted patients were selected and classified
as VAP (29 patients), and non-VAP (101 patients), prospectively. Clinical parameters, laboratory and
radiological findings were followed in patients with and without VAP.
Results
Among the patients, 60% (78 cases) were male. The median age was one month. All of the VAP
patients were neonates with the average age of 10.7±25.29 months. There was no significant
difference in age and gender. Duration of mechanical ventilation and ICU admission had significant
difference between groups (29.31±20.5 versus 8.45±8.76, and 32.62±21.15 versus 12.88±12.16 days,
respectively, p<0.001). Tachycardia was detected in 27 (93.1%), and 51(50.5%) patients in VAP and
non-VAP, respectively (p<0.001). Respiratory secretion was detected in 8(27.6%) and 9(8.9%) in
VAP, and non-VAP, respectively (p=0.009). Crackles was detected in 9(31%) and 15(14.9%) in VAP
and non-VAP, respectively (p=0.04). Blood and bronchoalveolar lavage (BAL) culture, need to
change device setting, O2 desaturation, WBC count and chest X- ray showed significant difference
between groups (p<0.05).
Conclusion
According to the results, some clinical and laboratory factors including WBC count, blood culture,
crackles and need to change settings should be considered as minor but new diagnostic criteria for
VAP.
Key Words: Children, Intensive Care Unit, Ventilator associated pneumonia.

*Please cite this article as: Khademi Gh, Lotfi M, Bakhtiari E, Imani B, Aelami MH. Minor Diagnostic Factors
in Ventilator Associated Pneumonia in Children. Int J Pediatr 2018; 6(7): 8015-23. DOI:
10.22038/ijp.2018.34035.3001

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*Corresponding Author:
Mohammad Hassan Aelami (M.D), Department of Pediatrics & Hand Hygiene and Infection Control Research
Center, Mashhad University of Medical Sciences, Mashhad, Iran. Fax: 98-51-37273943
Email: AelamiMH@mums.ac.ir
Received date: Jan.10, 2018; Accepted date: Mar.22, 2018

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Diagnostic Factors in Ventilator Associated Pneumonia

1- INTRODUCTION visceral adipose tissue (VAT). Therefore,

the diagnosis of VAP might be
Hospital-acquired pneumonia (HAP) is
complicated in critically ill patients. Chest
the second most common nosocomial
radiograph and bacterial culture of
infection in the Intensive Care Unit (ICU)
endotracheal aspirate or bronchoalveolar
(1). HAP is a major threat to the health of
lavage (BAL) specimen are required for an
admitted children in neonatal intensive
accurate diagnosis of respiratory tract
care unit (NICU). It leads to mortality,
infections. In respiratory tract infections,
prolongation of hospital stay and cost
in-time treatment with antibiotics for
treatment increment. Eighty-six percent of
multidrug-resistant pathogens is suggested.
HAP is associated with mechanical
Using serial surveillance of endotracheal
ventilation (MV) which leads to ventilator-
aspirate specimens is an efficient method
associated pneumonia (VAP) (2). The
to identify multidrug-resistant pathogens
incidence rate of VAP varies from 1.7 to
and their antibiotic susceptibilities (17).
8.9 per 1,000 ventilator/days (3). VAP
Present cross sectional study was carried
occurs in 5% of young children admitted
out evaluating the minor but new effective
in ICU. About one-fifth of children with
factors on diagnosis of VAP in ICU
VAP will expire (4). International
admitted children based on clinical,
Nosocomial Infection Control Consortium
laboratory and imaging evidence.
(INICC) reported that the incidence rate of
VAP was 13.6 per 1,000 ventilators/days
2- MATERIALS AND METHODS
in Asia, Latin America, Africa and Europe
from 2003 to 2008 (5). VAP is a common 2-1. Method
cause of HAP among newborns (6.8 to Present cross sectional descriptive
32.2%) (8). Gram-negative bacteria study was performed in Pediatric Intensive
aspiration by endotracheal tube and spread Care Unit (PICU) of Dr. Sheikh Hospital,
of upper respiratory tract bacteria to lower Mashhad University of Medical Sciences,
respiratory tract to lower are the main Mashhad- Iran, from 2014 to 2015. The
causes of VAP (9). Therefore, the risk of study participants included 130 children
VAP in patients with MV is very high (1). admitted in ICU, mechanically ventilated
VAP leads to antibiotic use increment and for over 48 hours, aged less than 16 years.
antibiotic-resistance (10). According to Parental informed consent was obtained
Centers for Disease Control (CDC), prior to the study. The patients were
aspiration reduction and colonization divided into two groups as with VAP (29
prevention decreased the incidence rate of patients), and without VAP (101 patients).
VAP (11). Because VAP leads to This study was approved by Mashhad
increased hospitalization, prevention is a University Medical Ethics Committee.
priority (12). Determination of actual rate
of VAP in children is difficult since the Patients were excluded if they were
difference between children and adults diagnosed with VAP less than 72 hours
diagnostic procedures as well as after birth. VAP was defined according to
identifying radiological pneumonia could CDC criteria which is presented in Table.1
be quite problematic (13). VAP risk (18). Primary outcome was the
factors in children include low birth- development of VAP. The secondary
weight, Mechanical Ventilation (MV) outcomes included the length of MV,
duration, tracheal intubation, suction and duration of hospitalization, biochemical
treatment with opioid (14-16). The changes, C-reactive protein (CRP), new
diagnostic criteria for VAP are overlapped radiological findings as well as mortality
with other similar syndromes such as and morbidity.

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Khademi et al.

Table-1: CDC diagnostic criteria for VAP in children (18).

Age range Criteria
Onset >72 h after birth and one of the following
radiologic criteria:
−new or progressive infiltrates
−consolidations
−adhesions or fluid in lobar fissures/pleura
and
Worsening gas exchange (SaO2 ↓; O2 requirement ↑;
Ventilation parameters ↑)
and
Four of the following signs and symptoms:
Neonates −fever (>38.0°C), hypothermia (<36.5°C), or
temperature instability
−new onset or increasing bradycardia (<80/min) or
tachycardia (>200/min)
−new onset or increasing tachypnea (>60/min) or
apnea (>20 seconds)
−new onset or increasing signs of dyspnea
(retractions, nasal flaring, grunting)
−increasing production of respiratory secretions and
need for suctioning
−purulent tracheal secretion
−isolation of a pathogen in respiratory secretions
−elevated C-reactive protein (>20 mg/L)
I/T-ratio >0.2

One of the following radiologic criteria:

−new or progressive infiltrate
−consolidations
−cavitations
−pneumatoceles
And
Worsening gas exchange (SaO2 ↓; O2 requirement ↑;
Ventilation parameters ↑)
2-11 months
And
Three of the following signs and symptoms:
−fever (>38.0°C), hypothermia (<36.5°C), or
temperature instability
−leucopenia (<4000 WBC/mm3) or yspneaosis
(≥15,000 WBC/mm3) with left shift (≥10% band
forms)
−new onset of purulent sputum, or change in
character of sputum, or increased respiratory
secretions, or increased suctioning requirements
−apnea or yspnea (yspneao, nasal flaring,
retraction of chest wall, grunting)
−wheezing, rales, or rhonchi
−cough
−bradycardia (<100/min) or tachycardia (>170/min).

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Diagnostic Factors in Ventilator Associated Pneumonia

One of the following radiologic criteria:

−new or progressive and persistent infiltrate
−consolidation
−cavitation
and
Three of the following signs and symptoms:
−fever (>38.4°C) or hypothermia (<36.5°C)
−leukopenia (<4000 WBC/mm3) or yspneaosis
1-16 years
(≥15,000 WBC/mm3)
−new onset of purulent sputum or change in
character of sputum or increased respiratory
secretions or increased suctioning requirements
−new onset or worsening cough or yspnea,
apnoea, or tachypnea
−rales or bronchial breath sounds
−worsening gas exchange (SaO2 ↓; O2 requirement ↑;Ventilation parameters ↑)
SaO2: Oxygen saturation; WBC: White blood cells; VAP: Ventilator-associated pneumonia.

2-2. Statistical analysis 29.31±20.50 and 8.45±8.76 days in the

VAP and non-VAP group with a
A sample size study population of 130 significant difference (p<0.001). Both
patients was considered appropriate to groups were ventilated via orotracheal
achieve a reasonable statistical analysis. method (89% in case versus 96% in
Statistical analysis was performed using control). Mean duration of ICU admission
SPSS software version 16.0 (SPSS was 32.62±21.15 and 12.88±12.16 days in
Institute, Inc., Chicago, IL, USA). All VAP and non-VAP group, respectively
experimental values are presented as with a significant difference (p<0.001).
mean ± standard deviation (SD) or
frequency. The comparison between 3-2. Clinical characteristics
groups was done by independent t- test.
The relationship between qualitative There was not any relationship between
variables was evaluated by Chi-square test. type of ICU including general and surgical
P -value less than 0.05 was considered and VAP. 41.4% (n= 12) and 58.4% (n=
significant. 59) of the patients in VAP and non-VAP
group were admitted in general ICU. The
3- RESULTS difference was not significant (p>0.05).
38.5% (n= 10) and 22.1% (n= 21) of the
3-1. Baseline Characteristics patients were preterm infants in the VAP
Among the 130 patients, 60% (78 and non-VAP groups, respectively
cases) were male; 29 patients were in VAP (p>0.05). The rate of caesarean delivery
group, and 101 patients were in non-VAP among the patient's mothers in VAP group
group. The median of age was one month. was 62.5% (n= 15) versus 43.3% (n= 39)
The average age of patients in VAP and in control (p>0.05). The causes of the
non-VAP groups was 10.7±25.29 and patients’ referral to the ICU were different.
19.7±41.37 months, respectively. There Tracheoesophageal fistula was the most
was not any significant difference in common cause in both groups with no
baseline characteristics including gender significant difference (p>0.05). Nutritional
and age between VAP and non-VAP group status was also evaluated for its probable
(p>0.05). The duration of MV was effect in the diagnosis of VAP. 51.7%

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Khademi et al.

(n=15) in VAP group, and 64.4% (n=65) subjects without VAP. The cerebrospinal
in non-VAP group had total parenteral fluid (CSF) culture was negative in both
nutrition (TPN). There was no significant groups. 93.1% (n= 27), and 94.1% (n= 95)
difference between groups (p>0.5). of patients in VAP and non-VAP groups
respectively, had negative results in urine
3-3. Clinical symptoms culture. The BAL culture was performed
for 24.1% (n=7) of the VAP-patients and
The body temperature, respiratory status
3.4% (n=1) of them had a positive result,
(tachypnea, apnea, dyspnea), purulent
versus 1% (n=1) in non-VAP patients. The
tracheal secretions, and bandemia more
difference between groups was significant
than 10%, did not show significant
(p<0.05). The blood culture was conducted
difference between VAP and non-VAP
for all the patients in the VAP group and
group (p>0.05). In contrast, the heart rate
95% (n= 96) of the non-VAP patients.
(tachycardia) showed significant
There was a significant difference between
difference between VAP and non-VAP
both groups (p<0.001).
group (p<0.001). Respiratory secretion
was observed more among patients with 3-5. Chest radiography
VAP (27.6%, n=8) in comparison with
non-VAP patients (8.9%, n= 9) (p<0.05). The chest X-ray results were abnormal in
The patients with VAP had greater all patients in the VAP group, while there
frequency of positive crackles in was normal result in 93.1% (n= 94) of
comparison with non-VAP patients non-VAP group. There was significant
(p=0.04). Also, the need for device change difference between VAP and non-VAP
setting was observed more among the group in consolidation, new infiltration,
VAP-patients (p=0.002). O2 desaturation progressive infiltration and pleural
was reported in 93.1% (n= 27) of VAP effusion (p<0.05). Consolidation was the
patients versus 5.9% (n= 6) in non-VAP main lesion in 58.6% (n= 17) of VAP
patients (p =0.001). patients. Significant differences between
VAP and non-VAP groups were presented
3-4. Laboratory tests in Table.2.
The level of C-reactive protein (CRP) was 3-6. Recovery and mortality rates
positive in some patients in both groups in
different times of measurement. The 57.4% (n= 13) of the patients without VAP
difference was not significant (p>0.05). and 44.8% (n= 58) of VAP-patients made
The white blood cells (WBCs) showed a complete recovery; 6.9% (n= 2) and
significant difference between VAP and 11.9% (n= 12) of the patients with and
non-VAP group (p<0.001). The rate of without VAP made a partial recovery,
leucopenia was similar in groups, while respectively. Also, 48.3% (n= 14) of VAP-
the incidence of leukocytosis in VAP- patients and 30.7% (n= 31) of non-VAP
patients was considerably higher than the patients expired (p=0.203).

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Diagnostic Factors in Ventilator Associated Pneumonia

Table-2: The comparison of clinical and laboratory data between VAP and non-VAP groups.
Non-VAP:101 patients
VAP group :29 patients
Clinical /laboratory characteristics Mean ±SD Or frequency P-value
Mean ±SD Or frequency (%)
(%)
Duration of MV (day) 29.31±20.50 8.45±8.76 <0.001*
Duration of ICU (day) 32.62±21.15 12.88±12.16 <0.001*
Heart rate (bit/minute)
Bradycardia 1(3.4%) 3(3%)
<0.001#
Tachycardia 27(93.1%) 51(50.5%)
Normal 1(3.4%) 47(46.5%)
Respiratory secretion (positive) 8(27.6%) 9(8.9%) 0.009#
Positive crackles 9(31%) 15(14.9%) 0.04#
Need for device change setting 8(27.6%) 7(6.9%) 0.002#
O2 desaturation 27 (93.1%) 6 (5.94%) <0.001#
Count of white blood (cell/ml)
Leucopenia 3 (10.3%) 10 (9.9%)
<0.001#
Leukocytosis 23(79.3%) 46(45.5%)
Normal 3 (10.3%) 45(44.5%)
Positive BAL culture 1 (3.4%) 1(1%) 0.009#
Positive blood culture 8(27.6%) 6 (5.9%) <0.001#
Abnormal CXR results 29(100%) 7(6.9%) <0.001#
VAP: Ventilator-associated pneumonia; MV: Mechanical ventilation; ICU: Intensive care unit; BAL:
Bronchoalveolar lavage; CXR: Chest X- ray. * Independent t test, # Chi-square.

4- DISCUSSION studies. This can be due to type of

sampling, because present study was done
Present study was carried out
in a referral pediatric surgery center.
evaluating the minor but new effective
Therefore, the number of surgical patients
factors on diagnosis of VAP in ICU
and patients with transcription elongation
admitted children based on clinical,
factor (TEF) was significant. A study by
laboratory and imaging evidences. One
Patria et al. in Italy claimed that the
hundred thirty patients aged less than 16
incidence rate of VAP was 6.6% in
years old with or without VAP were
children (20). According to another study
studied. Results showed that some of the
in Australia, the VAP rate was 7.07 per
clinical symptoms, radiological and
1,000 days of MV. In a research, the re-
laboratory findings could be involved in
intubation, absence of a feeding tube as
VAP diagnosis in ICU admitted children.
well as the absence of stress ulcer
According to present study, WBC count,
prophylaxis are the risk factors to VAP
BAL culture, the setting changes and
(21). A study in Egypt reported that the
crackles are effective factors for VAP
rate of VAP was 31.8 per 1,000 days of
diagnosis. The rate of VAP incidence is
MV (22). An Indian study explained that
different in all countries. Afjeh et al. in a
MV for more than 4 days was a risk factor
study on the newborns connected to the
for VAP. The VAP rate reported 36.2% in
ventilator for over 48 hours reported that
another study (23). The incidence rate of
VAP occurred in 17.3% of the patients,
VAP was lower in Gautam et al.’s studies
which was equivalent to 11.6 per 1000
(21) comparing with Rasslan and Awasthi
days (19). According to Elward et al., the
et al.’s report. This might be due to the
VAP rate was 11.6 per 1,000
differences in MV duration, sampling and
ventilators/days (4). The rate of VAP was
geographical diversities. Consistent with
26.7% in present study which was higher
present study, Patria’s study claimed that
than Afjeh et al.’s and Edward et al.’s
the length of MV and ICU stay are

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Khademi et al.

associated with VAP. Furthermore, methods to diagnose VAP in intubated

morality was higher in VAP children patients. According to their findings, BAL
comparing with non-VAP (20). The study was the most effective method of diagnosis
of Srinivasan et al. aimed to determine the for VAP (28). Consistent with present
risk factors of VAP. According to study, the changes on chest X- ray were
Srinivasan, VAP-children had a prolonged observed in all patients who participated in
MV and ICU admission as well as higher Afjeh et al.'s study (19). Present research
mortality rate. Srinivasan reported that the revealed that consolidation was the most
development of VAP is correlated with common lesion observed in VAP-patients.
post-surgical diagnosis as well as using In Afjeh et al.'s study, radiograph changes
narcotics (9). Inconsistent with present were found in only 50% of the patients. In
study, the study of Srinivasan et al. present study, there were no significant
acknowledged that there was a significant radiographic changes in 93.1% of the non-
difference in the gender of patients with VAP patients. Therefore, expertise is very
VAP (9). This might be due to different importance and absolutely essential to the
sampling, since MV for more than 48 correct interpretation of X-rays (19). In
hours was an inclusion criteria in spite of factors such as need to change the
Srinivasan’s experiment. The studies of setting and crackles which were not
Apisarnthanarak et al. and Almuneef et al. included in the CDC diagnostic criteria,
were conducted to determine the rate, current study showed that these symptoms
characteristics, risk factors and outcomes should be taken seriously as contributing
of VAP in extremely preterm neonates in factors in diagnosis of VAP. According to
NICU. The findings indicated that the rate present study, WBC count was a
of VAP and mortality were very high in diagnostic criterion for VAP patients
extremely preterm neonates (14, 24). which was not considered in CDC criteria.
The study of Feldman et al. on bacterial
Additionally, according to Bigham et al.’s
colonization of the endotracheal tube
study, VAP is associated with prolonged
revealed that the colonies were formed
PICU admission (25). It was also in close
within 12 hours after endotracheal tube
relation with longer MV duration and
placement and reached maximum after 96
increased mortality rate. VAP was
hours. Because the high incidence of VAP
correlated with subglottic stenosis, trauma
in intubated patients, finding new
and tracheostomy as well (25). According
approaches to prevent VAP seems
to present study, the blood and BAL
extremely necessary (30). A few other
cultures were two contributing factors in
studies concluded that the subglottic
the diagnosis of VAP. Diagnostic value of
secretion suction, directly affects the
blood culture was higher than BAL
prevention of VAP.
culture, while according to Luna et al. the
sensitivity of blood culture was low in
5- CONCLUSION
comparison to the BAL culture in
detection of same pathogenic Minor factors for diagnosis of VAP
microorganisms (26). Also, Kotgire’s need to more attention and evolution.
study indicated the limited value of blood Some clinical and laboratory factors
culture in microbiological diagnosis of including WBC count, blood culture,
VAP (27). Regarding the diagnostic effect crackles and need to change settings
of BAL culture, it has been stated that its should be considered as minor but new
invasive testing increases the accuracy and diagnostic criteria for VAP. Multi center
specificity of VAP diagnosis (10). The studies with larger sample size is
study of Sachdev et al. compared available recommended to confirm the results of
present study.

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Diagnostic Factors in Ventilator Associated Pneumonia

6- CONFLICT OF INTEREST: None. 2003-2008, issued June 2009. American

journal of infection control. 2010; 38(2):95-
7- AUTHORSHIP STATEMENT 104. e2.
The conception and design of the study: 6. Chomton M, Brossier D, Sauthier M,
Gholamreza Khademi and Mohammad Hasan Vallières E, Dubois J, Emeriaud G, et al.
Aelami, Ventilator-Associated Pneumonia and Events
in Pediatric Intensive Care: A Single Center
Analysis and interpretation of data: Bahare
Study. Pediatr Crit Care Med. 2018. doi:
Imani and Mojtaba Lotfi,
10.1097/PCC.0000000000001720.
Drafting the article: Elham Bakhtiari,
7. Venkatachalam V, Hendley JO,
Gholamreza Khademi,
Willson DF. The diagnostic dilemma of
Revising manuscript critically for important ventilator-associated pneumonia in critically ill
intellectual content: Gholamreza Khademi, children. Pediatric Critical Care Medicine.
Mohammad Hasan Aelami, Elham Bakhtiari, 2011; 12(3):286-96.
Bahare Imani and Mojtaba Lotfi.
8. Garland JS. Strategies to prevent
Final approval of the version to be submitted: ventilator-associated pneumonia in neonates.
Gholamreza Khademi, Mohammad Hasan Clinics in perinatology. 2010; 37(3):629-43.
Aelami, Elham Bakhtiari, Bahare Imani and
Mojtaba Lotfi. 9. Srinivasan R, Asselin J, Gildengorin
G, Wiener-Kronish J, Flori HR. A prospective
8- ACKNOWLEDGMENT study of ventilator-associated pneumonia in
children. Pediatrics. 2009; 123(4):1108-15.
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