Indian J Pediatr
DOI 10.1007/s12098-017-2514-y
ORIGINAL ARTICLE
Etiology and Risk Factors Determining Poor Outcome
of Severe Pneumonia in Under–Five Children
Suresh Kumar Jakhar 1 & Mukul Pandey 1 & Dheeraj Shah 1 & V. G. Ramachandran 2 &
Rumpa Saha 2 & Natasha Gupta 3 & Piyush Gupta 1
Received: 5 March 2017 / Accepted: 21 September 2017
# Dr. K C Chaudhuri Foundation 2017
Abstract
Objectives To determine the etiology of severe pneumonia
(pneumonia with chest indrawing) in under-five children,
and to study the risk factors for poor outcomes viz., ‘treatment
failure’, ‘need for change in antibiotics’, ‘prolonged hospital
stay’, ‘need for mechanical ventilation’ and ‘mortality.’
Methods Children (age 2 mo to 5 y) with pneumonia and chest
drawing were enrolled prospectively from October 2012
through September 2013. Clinical history was recorded, and
examination, anthropometry and investigations (including
chest X-ray, blood culture and nasopharyngeal swab culture)
were performed. Children were managed as per standard guide-
lines, and recovery outcomes were recorded in form of ‘treat-
ment failure’ (defined as persistence of features of severe pneu-
monia after 72 h or worsening of clinical condition before 72 h),
need for change of antibiotics and prolonged (>5 d) hospital
stay. The associations between the clinical, anthropometric and
diagnostic risk factors and the recovery outcomes were evaluat-
ed by univariate and multivariate logistic regression analysis.
Results Out of 120 children enrolled in the study, 36 (42%)
were culture positive (nasopharyngeal/blood); most common
bacteria isolated were Streptococcal pneumoniae and
Staphylococcal aureus, respectively. Treatment failure was seen
in 15 (12.5%), 34 (28.3%) needed change of antibiotics, and 50
* Dheeraj Shah
shahdheeraj@hotmail.com
1
Department of Pediatrics, University College of Medical Sciences &
GTB Hospital, Dilshad Garden, Delhi 110095, India
2
Department of Microbiology, University College of Medical
Sciences & GTB Hospital, Dilshad Garden, Delhi, India
3
Department of Radiology, University College of Medical Sciences &
GTB Hospital, Dilshad Garden, Delhi, India
(41.6%) children required prolonged hospitalization. Low birth
weight, overcrowding, general danger signs (lethargy/unable to
drink), clinical rickets, crepitation, leukocytosis and positive
blood culture were significant risk factors for treatment failure,
prolonged hospital stay and antibiotics change. On multivariate
logistic regression analysis, respiratory rate of >70/min (OR
19.94, 95%CI 1.42–280.29), lethargy/unconsciousness (OR
114.2, 95%CI 3.14–4147.92), and positive blood culture (OR
15.24, 95%CI 2.53–91.67) had more chances of treatment fail-
ure. Duration of hospital stay was prolonged in those who had
inability to drink (OR 3.89, CI 1.37–10.99) or abnormal chest
X-ray (OR 8.45, CI 3.56–20.04). Children with rickets (OR
3.69, CI 1.14–11.96), and those with abnormal chest X-ray
(OR 9.66, CI 2.62–35.53) had a higher odds of change in anti-
biotics. Presence of wheeze was a protective factor for treatment
failure (OR 0.03, CI 0.00–0.37) and change of antibiotics (OR
0.24, CI 0.07–0.74).
Conclusions Staphylococcus aureus and Streptococcus
pneumoniae are the predominant organisms causing severe
pneumonia in our setting. Children with risk factors such as
respiratory rate >70/min, rickets, lethargy/unconsciousness,
not able to drink, abnormal chest X-ray or positive blood
culture are likely to have a delayed recovery or need of change
of antibiotics, whereas those with wheeze are likely to recover
faster with less chances of treatment failure.
Keywords Severe pneumonia . Risk factors . Treatment
failure
Introduction
Pneumonia accounts for nearly one-fifth of childhood deaths
worldwide [1]. India contributed 14.9% of deaths of children
under 5 y of age in the year 2015 [2]. In view of high mortality

from severe pneumonia in developing countries, it is neces-
sary to understand the factors determining poor outcome of
pneumonia. Studies from different regions have identified
some risk factors for mortality viz., young age of the child,
acute malnutrition, lack of breastfeeding, and presence of ra-
diological abnormality. However, most studies are from
African or South American regions, and have focused on
mortality without assessing other important outcomes such
as treatment failure, need for change of antibiotics, and dura-
tion of hospitalization. There is a paucity of prospectively
collected data on etiology or risk factors determining poor
outcome of severe pneumonia from developing country set-
ting. The authors conducted this descriptive study to deter-
mine the etiology and various risk factors in predicting poor
outcome of severe pneumonia in under-five children in India.
Material and Methods
This was a hospital-based, descriptive, cohort study, conducted
between October 2012 to September 2013 in the Departments of
Pediatrics and Microbiology at a medical college affiliated hos-
pital mainly catering to the urban poor population of East Delhi
and Western Uttar Pradesh, India. Children aged between 2 mo
to 5 y with diagnosis of severe pneumonia (on the day of pre-
sentation to the hospital) were included after obtaining written
informed consent from parents. Severe pneumonia was defined
as presence of lower chest indrawing (definite inward movement
of lower chest during quiet breathing) and/or with general danger
signs (not able to drink, persistent vomiting, convulsions, lethar-
gy or unconscious, stridor in calm child or severe malnutrition),
in children presenting with cough or difficult breathing [3].
Children with non-respiratory (e.g., congestive cardiac failure,
metabolic acidosis, neurogenic hyperventilation), non-
infectious (e.g., foreign body aspiration, hydrocarbon ingestion)
causes of respiratory distress, and those with two or more epi-
sodes of wheezing illness in past were excluded. Children who
had received parenteral antibiotics before presenting to the hos-
pital were also excluded. The study was approved by the
Institutional Ethical Committee of University College of
Medical Sciences, New Delhi.
History was obtained pertaining to symptomatology, diet (in-
cluding details of breastfeeding and complementary feeding),
birth weight and immunization status, and home environment.
Socioeconomic status was determined by using modified
Kuppuswamy scale [4]. Physical examination included
recoding of vital signs (temperature, heart rate, and respiratory
rate); and assessment of fast breathing, chest indrawing (definite
inward movement of lower chest during quiet breathing), signs
of hypoxia (head nodding, grunting, and cyanosis), clinical
signs of rickets; and chest auscultation for crepitation/wheezing.
Anthropometry, including weight, length/height and mid-upper
arm circumference (MUAC), was recorded using standard
Indian J Pediatr
techniques. Severe acute malnutrition (SAM) was defined as
weight for height Z score < −3 standard deviation (SD) or
MUAC <11.5 cm [5]. Respiratory rate was measured for a full
minute and if it was fast (RR >50/min for age 2 mo–1 y and
>40/min for 1–5 y), it was measured again and the average of
two readings was noted. The count was done at a time when the
child was quiet. Baseline oxygen saturation was measured using
a pulse oximeter with a probe on a finger or toe, in room air.
Hypoxia was defined as oxygen saturation < 92% in room air
[3]. A blood sample was obtained for hemoglobin, total leuco-
cyte count, serum electrolytes, serum 25(OH)D levels and blood
culture at the time of hospitalization. Chest X-ray was obtained
in all children and interpreted by a radiologist blinded to the
clinical details. Nasopharyngeal swabs were obtained for iden-
tification of Haemophilus influenzae and Streptococcus
pneumoniae within 24 h of enrolment. A sterile swab was in-
troduced into the nasopharynx, parallel to palate and kept there
for 30 s. Then the swab was rotated, removed and plated imme-
diately on blood agar along with staphylococcal streak, and on
chocolate agar. Plates were incubated for 18–24 h at 37 °C in 5–
10% CO2, and bacteria were identified by colony morphology,
gram stain and their biochemical reactions [6].
Patients were treated with antibiotics for severe pneumonia
as per guidelines of Indian Academy of Pediatrics [7]. Children
were monitored for respiratory rate, chest indrawing, oxygen
saturation, auscultatory findings, fever, feeding, cyanosis and
mental status every 8 hourly. Intravenous antibiotics were
switched to oral antibiotics after 48–72 h, if the lower chest
indrawing disappeared by that time. The child was discharged
only when the child was afebrile (temperature < 100.4 °F) and
there was no fast breathing for at least 24 h.
The main outcomes of interest were to study the bacterial
etiology and outcome as ‘treatment failure’, defined as persis-
tence of features of severe pneumonia after 72 h or worsening of
clinical condition before 72 h [8]. The secondary outcomes in-
cluded need for change of antibiotics (as per treating clinician’s
perception of non-improvement), need for mechanical ventila-
tion (if airway and breathing was compromised) [3], prolonged
(more than five days) hospitalization and death. The risk factors
assessed were socio-demographic and clinical parameters
(breastfeeding, smoking member in family, overcrowding, so-
cioeconomic status, cooking fuel other than LPG), nutritional
status of the child (presence of wasting, severe wasting, stunting,
MUAC <11.5 cm), immunization status, presence of anemia
(defined as hemoglobin <11 g/dl) [3], rickets, auscultation find-
ing of wheezing, presence of general danger signs, and investi-
gations (presence of anemia, hypovitaminosis D [9], chest X-ray
abnormalities and positive blood culture).
The data were entered in Microsoft Excel worksheet and
analyzed with SPSS Version 17.0. Chi-square test or Fischer
Exact test (as applicable) was used to study the associations
between the categorical risk factors and the outcome.
Continuous parameters were compared by using unpaired
Indian J Pediatr

Student t-test. To find out the independent contribution of each nasopharyngeal or blood culture. Children with wheeze had
factor towards the outcome, multivariate logistic regression lesser frequency of bacterial infection in comparison to those
analysis was used. The authors calculated odds ratio and without wheeze (17.2% vs. 52.6%; P < 0.001).
95% confidence interval for the parameters, which were found Treatment failure occurred in 15 (12.5%); 34 (28.3%) needed
to be significant in univariate analysis. A P value of less than change of antibiotics, and 50 patients (41.6%) required
0.05 was considered statistically significant. prolonged hospitalization. No patient needed mechanical venti-
lation and no one died. Risk factors for poor outcome (treatment
failure, prolonged hospital stay and antibiotics change) are de-
Results tailed in Table 2. On univariate analysis, low birth weight, over-
crowding, general danger signs (lethargy/unable to drink), clin-
A total of 120 children (74 boys and 46 girls) aged between 2 ical rickets, crepitation, total leukocyte counts and positive
mo to 5 y with diagnosis of severe pneumonia were enrolled. blood culture were statistically significant risk factors for treat-
Out of these 79 (66%) were aged less than one year. Baseline ment failure, prolonged hospital stay and antibiotics change.
anthropometry, immunization status, clinical and laboratory Children who were never breastfed, smoking in family, mean
profile is shown in Table 1. oxygen saturation, anemia and mean vitamin D levels were not
Streptococcus pneumoniae was isolated in 22 (26%) chil- significantly associated with any of the poor outcome.
dren from nasopharyngeal swabs. In blood culture, On multivariate logistic regression analysis (Table 3), re-
methicillin-sensitive and methicillin-resistant (sensitive to spiratory rate of >70/min, lethargy/unconsciousness and pos-
vancomycin and linezolid) Staphylococcal aureus was isolat- itive blood culture had more chances of treatment failure.
ed in 14 and 2 children respectively. Klebsiella spp. was iso- Duration of hospital stay was prolonged in those who had
lated from blood culture in 2 patients, E.coli in 1 patient and inability to drink or abnormal chest X-ray. Children with rick-
Acinetobacter spp. in 1 patient. Thirty-six (42%) children with ets, and those with abnormal chest X-ray had a higher odds of
severe pneumonia had an organism isolated from either change in antibiotics. Presence of wheeze was a protective
factor for treatment failure and change of antibiotic.
Table 1 Baseline anthropometric, immunization, clinical, and
laboratory profile of study children (N = 120)
Discussion
Parameter Value
Mean ± SD; Median (Range) The authors studied the etiology and various socio-demo-
Age (months) 11.9 ± 11.5; 8 (2, 60) graphic, clinical and laboratory parameters associated with
Anthropometry poor outcomes in 120 under-five children hospitalized with
Weight (kg) 7.15 ± 2.25; 7 (2.5, 15) WHO-defined severe pneumonia. Streptococcus pneumoniae
Length / height (cm) 69.3 ± 10.9; 68 (48, 116)
Weight for age Z-score (WAZ) −1.97 ± 1.36; −1.71 (−6.29, 1.14)
(nasopharyngeal swab) and Staphylococcal aureus (blood)
Length / height for age Z-score (HAZ) −1.43 ± 1.61; −1.28 (−6.49, 2.71) were the predominant organisms isolated in children with
Weight for height Z-score (WHZ) −1.47 ± 1.54; −1.47 (−5.08, 3.32) pneumonia. Children having lethargy/unconsciousness, not
MUAC#(cm) 13.14 ± 0.62; 13.05 (11.5, 14)
Immunization status*; N (%)
able to drink, clinical rickets, positive blood culture or abnor-
Completely immunized 71 (59) mal chest X-ray had significantly poor outcomes in term of
Partially immunized 40 (33) treatment failure, prolonged hospital stay or antibiotics
Unimmunized 9 (7.5)
change; whereas presence of wheeze predicted lesser chance
Clinical features; N (%)
Not able to drink 85 (71) of treatment failure or antibiotic change.
Lethargy or unconscious 7 (6) Major limitation of index study was evaluation of etiological
Anemia 37 (31) organism by nasopharyngeal aspirate and lack of investigations
Rickets 30 (25)
Crepitations 37 (31) for viruses, chlamydiae or mycoplasmae. Isolation of bacteria
Wheeze 23 (19) from only nasopharynx may not necessarily mean that these are
Crepitations + Wheeze 58 (48) responsible for pneumonia. The authors only excluded children
Laboratory
Vitamin D[25(OH) D3] $ level 12.73 ± 7.3; 11.03 (2.02, 37.32) who received parenteral antibiotics before presenting to the hos-
Radiological features; N (%) pital. Few patients could have received oral antibiotics before
Infiltrates 43 (36) being referred to the hospital, and this could have affected yield
Consolidation 7 (6)
Pyo-pneumothorax 2 (2) of organisms from cultures. In authors’ set-up, most patients are
not given prescriptions for oral drugs received in the unorga-
*As per Delhi Government Schedule nized set-up, and it is often difficult to obtain a history of receipt/
#
Mid upper arm circumference available in 88 children non-receipt of oral antibiotics. The authors could not identify
$
Done in 100 children risk factors for mortality and requirement of mechanical
 Indian J Pediatr

Table 2 Association of various factors with treatment failure, prolonged hospital stay and change in antibiotics

Parameters Treatment failure P value Prolonged hospital stay P value Antibiotics changed P value
(n = 15) (n = 50) (n = 34)

Age (months) Mean ± SD 7.26 ± 6.35 0.096 12.36 ± 11.88 0.711 12.64 ± 12.80 0.655
Sex (Male) 9 (60%) 0.887 25 (50%) 0.026 18 (53%) 0.216
Birth weight (kg) Mean ± SD 2.13 ± 0.37 0.039 2.26 ± 0.68 0.005 2.18 ± 0.48 0.006
Unimmunized 4 (27%) 0.025 6 (12%) 0.266 18 (53%) 0.383
Never breast fed 2 (13.3%) 0.471 5 (10%) 0.655 5 (14.7%) 0.62
Smoking in family member 4 (27%) 0.390 14 (34%) 0.608 10 (29.4%) 0.301
Overcrowding 14 (93%) 0.012 37 (74%) 0.058 27 (79%) 0.048
Lower Socioeconomic status* 14 (93%) 0.112 40 (80%) 0.285 28 (82%) 0.242
Cooking fuel other than LPG 6 (40%) 0.083 15 (30%) 0.103 1 (35%) 0.014
SAM 5 (33%) 0.039 10 (20%) 0.121 10 (29%) 0.007
Lethargy or unconscious 4 (27%) 0.005 5 (10%) 0.127 4 (12%) 0.099
Not able to drink 15 (100%) 0.004 43 (86%) 0.002 29 (85%) 0.028
Sign of rickets 7 (47%) 0.054 18 (36%) 0.019 15 (44%) 0.002
Respiratory rate (Mean ± SD) 68 ± 7 <0.001 63 ± 7 0.058 62 ± 7 0.120
SPO2 (Mean ± SD) 95 ± 2 0.070 96 ± 1 0.058 95 ± 1 0.080
Crepitations 13 (87%) <0.001 23 (46%) <0.001 23 (68%) <0.001
Hemoglobin (g/dL) Mean ± SD 9.40 ± 1.96 0.230 9.5 ± 1.85 0.025 9.12 ± 2.05 0.016
High TLC count (/cumm) Mean ± SD 24,126 ± 15,390 <0.001 16,764 ± 11,218 0.001 19,605 ± 12,233 0.001
Vitamin D level (ng/mL) Mean ± SD 10.42 ± 7.32 0.205 14.31 ± 8.74 0.086 12.72 ± 7.65 0.997
Abnormal Chest X- ray 15 (100%) <0.001 36 (72%) <0.001 30 (88%) <0.001
Positive Nasopharyngeal aspirate culture 8 (53%) 0.001 12 (24%) 0.175 10 (30%) 0.049
Positive Blood culture 10 (68%) <0.001 15 (30%) 0.001 13 (38%) <0.001

LPG Liquified petroleum gas; SAM Severe acute malnutrition; SPO2 Oxygen saturation; TLC Total leucocyte counts
*Lower SES include class IV and class V

ventilation because none of the patient died and no one required
mechanical ventilation. Absence of long term follow-up for any
recurrence was also a limitation.
In a study by Mathew et al. [10], S. pneumoniae (79%) and
Staphylococcal aureus (30%) were the predominant isolates in
nasopharyngeal aspirate and blood culture, respectively; results
which are matching with present study. Another study by El
Seify et al. [11] showed the most common bacterial causes of
pneumonia to be Staphylococcus aureus (13.3%), followed by
Streptococcus pneumoniae and Klebsiella pneumoniae (7.8%
each) from nasopharyngeal swab and blood. The possible dif-
ference could be due to pneumococcal vaccine being adminis-
tered to children in the study area. S. aureus, as a predominant
organism isolated from blood culture in children with severe
pneumonia has been reported earlier from studies conducted in
the South East Asia region [12].

Table 3 Risk factors for treatment failure, prolonged hospital stay and change in antibiotics as identified by multivariate logistic regression

Parameters Treatment failure OR (95% CI) Prolonged hospital OR (95% CI) Antibiotics changed OR (95% CI)
(n = 15) (%) stay (n = 50) (%) (n = 34)(%)

Age < 12 mo 12 (80) 2.27 (0.60–8.55) 30 (60) 0.64 (0.30–1.38) 21 (61.8) 0.78 (0.34–1.78)
Sex (Male) 9 (60) 0.06 (0.00–0.97) 25 (50) 1.49 (0.60–3.72) 18 (52.9) 0.68 (0.17–2.60)
Never breast fed 2 (13.3) 0.51(0.00–32.85) 5 (10) 1.27 (0.16–9.78) 5 (14.7) 0.85 (0.07–9.94)
Smoking in family member 4 (26.7) 0.59 (0.04–8.45) 14 (34) 0.63 (0.24–1.65) 10 (29.4%) 0.59 (0.17–1.97)
Overcrowding 14 (93.3) 5.81(0.24–141.77) 37 (74) 0.90 (0.29–2.78) 27 (79.4) 0.95 (0.20–4.45)
Lower Socioeconomic status 14 (93.3) 3.05 (0.09–96.18) 40 (80) 1.59 (0.52–4.95) 28 (82.4) 1.20 (0.26–5.55)
Cooking fuel other than LPG 6 (40) 3.63 (0.26–50.50) 15 (30) 1.16 (0.33–4.03) 1 (35.3) 3.17 (0.92–10.93)
SAM 5 (33.3) 0.66 (0.04–11.59) 10 (20) 0.45 (0.12–1.70) 10 (29.4) 0.84 (0.19–3.67)
Lethargy or unconscious 4 (26.7) 114.2(3.14–4147.92) 5 (10) 1.21 (0.15–9.48) 4 (11.8) 1.76 (0.20–15.40)
Not able to drink 15 (100) * 43 (86) 3.89 (1.37–10.99) 29 (85.3) 2.06 (0.49–8.62)
Sign of rickets 7 (46.7) 1.02 (0.05–19.04) 18 (36) 2.04 (0.76–5.44) 15 (44.1) 3.69 (1.14–11.96)
Respiratory Rate >70/min 4 (26.7) 19.94 (1.42–280.29) 5 (10) 0.79 (0.16–3.75) 4 (11.8) 0.45 (0.08–2.47)
Any wheeze# 2 (13.3) 0.03 (0.00–0.37) 25 (50) 0.83 (0.27–2.49) 11 (32.4) 0.24 (0.07–0.74)
Anemia 7 (46.7) 0.45 (0.06–3.44) 21 (42) 1.21 (0.42–3.44) 16 (47.1) 0.88 (0.23–3.33)
High TLC count (>11,000/mm3) 13 (86.7) 5.33 (0.37–76.63) 35 (70) 0.89 (0.29–2.74) 29 (85.3) 3.74 (0.83–16.77)
Abnormal Chest X- Ray 15 (100) * 36 (72) 8.45 (3.56–20.04) 30 (88.2) 9.66 (2.62–35.53)
Positive Blood culture 10 (66.7) 15.24 (2.53–91.67) 15 (30) 2.12 (0.59–7.58) 13 (38.2) 1.42 (0.32–6.24)

*95% CI cannot be calculated because not able to drink and abnormal chest X-ray was present in 100% cases of treatment failure
#
Includes all patients with wheeze on auscultation with or without other findings
Indian J Pediatr
There are only few studies in literature on outcome mea-
sures in terms of treatment failure, prolonged hospital stay or
need for change of antibiotics. Tiewsoh et al. [13] studied 200
children aged between 2 mo to 5 y with severe pneumonia,
and showed that 56.5% patients needed a change in antibi-
otics, 51% stayed for more than 5 d in the hospital, 20.5%
needed mechanical ventilation and 10.5% died. All of these
outcomes were less commonly observed in present study.
Better outcomes in index patients may be due to less serious
patients enrolled in present study as this hospital also catered
to directly reporting patients besides referred patients as com-
pared to patient enrolment from a major referral hospital in the
study by Tiewsoh et al. [13].
Tiewsoh et al. [13] identified lack of exclusive breastfeeding,
low birth weight and abnormal chest radiograph as risk factors
for change of antibiotics. In the index study, apart from abnor-
mal chest X-ray, presence of clinical rickets was also associated
with increased risk for change of antibiotics. Moreover,
breastfeeding status was not a risk factor for the same. Few other
studies have also reported abnormal chest X-ray as a risk factor
for mortality in severe pneumonia [14, 15].
Few studies have showed comparable treatment failure in
hospitalized vs. home treatment group in pneumonia with chest
indrawing [12, 16], suggesting oral antibiotics as effective alter-
natives to parenteral antibiotics. Findings from present study
have the potential to further refine the criteria for oral antibiotic
use in children with pneumonia and chest indrawing; apart from
those having general danger signs, children with signs of rickets
or abnormal chest X-ray may be treated in hospital with paren-
teral antibiotics whereas those with wheeze may be managed in
community. Children with wheeze may respond better in com-
munity as they have more chances of having a viral etiology
rather than bacterial pneumonia [17, 18]. In the index study too,
children with wheeze had significantly lesser isolation of bacte-
ria and faster recovery.
It is concluded that Staphylococcus aureus and Streptococcus
pneumoniae are the predominant organisms causing severe
pneumonia in our setting. Children with risk factors such as
rickets, not able to drink, abnormal chest radiograph or positive
blood culture are likely to have a delayed recovery, and should
therefore be managed in hospital-based settings.
Acknowledgments Dr. Rajeev, Department of Community Medicine,
for statistical analyses.
Contributions DS and PG conceptualized the study and its design.
SKJ, VGR, RS and NG: participated in data collection and diagnostic
work-up of study participants. MP and DS analyzed and interpreted the
data. MP and SKJ drafted the manuscript, which was revised after critical
inputs from PG, DS, RS, VGR and NG. All authors approved the final
version of the manuscript, as submitted.
Compliance with Ethical Standards
Conflict of Interest None.
Source of Funding None.
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