Hypoxemia in children with pneumonia and its clinical predictors.
ABSTRACT To assess the prevalence of hypoxemia in children, 2 months to 5 years of age, with pneumonia and to identify its clinical predictors.
Children between 2-60 months of age presenting with a complaint of cough or difficulty breathing were assessed. Hypoxemia was defined as an arterial oxygen saturation of < 90% recorded by a portable pulse oximeter. Patients were categorized into groups: cough and cold, pneumonia, severe pneumonia and very severe pneumonia.
The prevalence of hypoxemia (SpO2 of < 90%) in 150 children with pneumonia was 38.7%. Of them 100% of very severe pneumonia, 80% of severe and 17% of pneumonia patients were hypoxic. Number of infants with respiratory illness (p value = 0.03) and hypoxemia (Odds ratio = 2.21, 95% CI 1.03, 4.76) was significantly higher. Clinical predictors significantly associated with hypoxemia on univariate analysis were lethargy, grunting, nasal flaring, cyanosis, and complaint of inability to breastfeed/drink. Chest indrawing with 68.9% sensitivity and 82.6% specificity was the best predictor of hypoxemia.
The prevalence and clinical predictors of hypoxemia identified validate the WHO classification of pneumonia based on severity. Age < 1 year in children with ARI is an important risk factor for hypoxemia.
Chapter: Acute Lower Respiratory Infections01/1970: pages 179-214;
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ABSTRACT: The World Health Organization (WHO) recommends using age-specific respiratory rates for diagnosing pneumonia in children. Past studies have evaluated the WHO criteria with mixed results. We examined the accuracy of clinical and laboratory factors for diagnosing pediatric pneumonia in resource-limited settings. We conducted a retrospective chart review of children under 5 years of age presenting with respiratory complaints to three rural hospitals in Rwanda who had received a chest radiograph. Data were collected on the presence or absence of 31 historical, clinical, and laboratory signs. Chest radiographs were interpreted by pediatric radiologists as the gold standard for diagnosing pneumonia. Overall correlation and test characteristics were calculated for each categorical variable as compared to the gold standard. For continuous variables, we created receiver operating characteristic (ROC) curves to determine their accuracy for predicting pneumonia. Between May 2011 and April 2012, data were collected from 147 charts of children with respiratory complaints. Approximately 58% of our sample had radiologist-diagnosed pneumonia. Of the categorical variables, a negative blood smear for malaria (χ(2) = 6.21, p = 0.013) and the absence of history of asthma (χ(2) = 4.48, p = 0.034) were statistically associated with pneumonia. Of the continuous variables, only oxygen saturation had a statistically significant area under the ROC curve (AUC) of 0.675 (95% confidence interval [CI] 0.581-0.769 and p = 0.001). Respiratory rate had an AUC of 0.528 (95% CI 0.428-0.627 and p = 0.588). Oxygen saturation was the best clinical predictor for pediatric pneumonia and should be further studied in a prospective sample of children with respiratory symptoms in a resource-limited setting.Journal of Emergency Medicine 08/2013; · 1.18 Impact Factor
Hypoxemia in Children with Pneumonia and Its Clinical
Sudha Basnet1, Ramesh Kant Adhikari1 and Chitra Kumar Gurung2
Department of Pediatrics, 1Department of Community Medicine and Family Health, 2Institute of Medicine,
Objectives. To assess the prevalence of hypoxemia in children, 2 months to 5 years of age, with pneumonia and to identify
its clinical predictors.
Methods. Children between 2-60 months of age presenting with a complaint of cough or difficulty breathing were assessed.
Hypoxemia was defined as an arterial oxygen saturation of <90% recorded by a portable pulse oximeter. Patients were
categorized into groups: cough and cold, pneumonia, severe pneumonia and very severe pneumonia.
Results. The prevalence of hypoxemia (SpO2 of < 90%) in 150 children with pneumonia was 38.7%. Of them 100% of very
severe pneumonia, 80% of severe and 17% of pneumonia patients were hypoxic. Number of infants with respiratory illness (p
value = 0.03) and hypoxemia (Odds ratio = 2.21, 95% CI 1.03, 4.76) was significantly higher. Clinical predictors significantly
associated with hypoxemia on univariate analysis were lethargy, grunting, nasal flaring, cyanosis, and complaint of inability to
breastfeed/drink. Chest indrawing with 68.9% sensitivity and 82.6% specificity was the best predictor of hypoxemia.
Conclusion. The prevalence and clinical predictors of hypoxemia identified validate the WHO classification of pneumonia based
on severity. Age < 1 year in children with ARI is an important risk factor for hypoxemia.
[Indian J Pediatr 2006; 73 (9) : 777-781]
Key words : Pneumonia; Hypoxemia; Clinical predictors
Pneumonia is one of the common causes of morbidity and
a significant cause of mortality in children under 5 years
of age. The World Health Organization (WHO) estimates
that acute respiratory infection (ARI), mostly in the form
of pneumonia, is the leading cause of death in children
under-five, killing over 2 million children annually.1
Nepal, a developing country has an under five mortality
rate of 91/ 1000 live births2 and an infant mortality rate of
64/ 1000 live births.2 Annual incidence of pneumonia in <
5 years is 90/ 1000, with 4.2/ 1000 children having severe
pneumonia.3 Hypoxemia in pneumonia has been shown
to be a risk factor for death. Hypoxic children with
pneumonia are five times more likely to die than those
without in studies done in Kenya and Gambia.4, 5 Such an
association between hypoxemia and pneumonia suggests
that its early detection and treatment are important
aspects in the management of children with pneumonia.
With the introduction of the pulse oximeter, a sufficiently
Correspondence and Reprint requests : Dr. Sudha Basnet, EPC 376,
GPO Box 8975, Kathmandu, Nepal. Phone: 977-1- 4412202; Fax: 977
1-4418186. E-mail: email@example.com
accurate and non-invasive tool for measuring arterial
oxygen saturation, assessment of hypoxemia in
pneumonia has become possible. A pulse oximeter,
however, is expensive and not suitable for routine use in
a developing country like Nepal. To overcome this
problem, clinical signs that best predict hypoxemia in
pneumonia have been evaluated in earlier studies in other
developing countries. Clinical features like cyanosis,
tachypnea, grunting, head nodding, inability to cry, no
spontaneous movement during clinical examination and
chest retractions have been identified as the best clinical
predictors of hypoxemia.4, 5 The Integrated Management
of Childhood Illnesses (IMCI) also makes use of clinical
features to classify pneumonia into various categories
based on severity.
A t the Kanti Children’s Hospital, although acute
respiratory illness is the most frequent reason for
admission and second most frequent cause of death, there
is no provision to assess the degree of hypoxemia.
Oxygen also does not seem to be given as frequently as
one would think it should be used. Who are the children
with pneumonia who really need oxygen as therapy?
Would certain clinical features help us to identify hypoxic
children? This study was done to find the prevalence of
Indian Journal of Pediatrics, Volume 73—September, 2006 777
Sudha Basnet et al
hypoxemia in children with pneumonia and identify its
clinical predictors. It is based on the hypothesis that
hypoxemia in pneumonia can be predicted clinically by
assessing the various symptoms and signs associated
MATERIALS AND METHODS
A cross sectional study was conducted from 14th
December 1999 to 18th July 2000 at the Kanti Children’s
Hospital in the Kathmandu valley that lies at an altitude
of about 1336 meters above sea level. Children between 2
months to 5 years of age who presented to the Outpatient
or the Emergency Department with a complaint of cough
or difficulty breathing were assessed. Relevant history of
the illness and examination was conducted according to a
questionnaire prepared for the purpose of the study
before the child received any form of treatment at the
hospital. During the physical examination, arterial
oxygen saturation was recorded using a portable, battery
powered pulse oximeter (Mini SPO2T manufactured by
the Criticare Systems, USA) with the sensor device placed
over the finger (index or middle) or the big toe. A reading
that was stable for at least 3 minutes was noted down.
Hypoxemia was defined as an arterial oxygen saturation
of <90% recorded by pulse oximetry. An arterial oxygen
saturation of 90% generally corresponds to an arterial
oxygen tension of 60-70mm Hg. This relation however is
affected by factors such as temperature, pH, altitude and
age. To overcome this problem, oxygen saturation by
oximetry was recorded in children presenting with just
cough and cold (assumed to be healthy children and
therefore acting as the control group) to determine the
normal range in all the children entered in the study.
Based on the clinical findings the patients were then
categorized into four groups using the WHO guidelines 6:
• ? Patients with cough and cold
Table 1. Distribution of Children According to Age and Diagnosis
• ? Patients with pneumonia
• ? Patients with severe pneumonia
• Patients with very severe pneumonia.
Patients were excluded from the study if:
• ? A murmur was detected on auscultation of the heart
indicating the presence of heart disease.
• ? They could not be grouped into any of the categories
After completion of the examination, patients were
either sent home with treatment or admitted to the
hospital for further management.
Statistical analysis : This was done using the Epi Info
V ersion 6 program in the computer. Clinical signs
between hypoxemic and non-hypoxemic children were
compared using the Chi square test, or by the Fisher’s
exact test if the expected frequencies were less than 5.
A p value of < or = 0.05 was considered significant. The
sensitivity and specificity of each clinical sign in its ability
to predict hypoxemia was also calculated.
In the study conducted over a period of seven months, a
total of 264 subjects were interviewed and examined. 14
children were excluded from the study, as they could not
be classified into any category of illness as specified in the
The distribution of patients according to age and
category of illness is shown in table 1. Age range was 2 –
60 months with a median of 12 months (interquartile
range 6 - 26). 123(49.2%) were females and 127(50.8%)
were males. There was no difference in the number of
males to females in all categories of illness (p value = 0.4).
There were a significantly higher number of infants with
respiratory illness (p value = 0.03). On assessment, none
of the children with cough and cold had SpO2 of < 90%.
The mean oxygen saturation in this group was 96%
AGE Cough & Cold Pneumonia Severe Pneumonia Very Severe Pneumonia Total
(Figures in brackets are percentages unless otherwise stated.)
T ABLE 2. Prevalence of Hypoxemia in Cases With Pneumonia.
Oxygen Saturation Pneumonia Severe Pneumonia Very Severe Pneumonia Total
> or =90%Sp O2
778 Indian Journal of Pediatrics, Volume 73—September, 2006
Hypoxemia in Children with Pneumonia and Its Clinical Predictors
(standard deviation of 2.123). In children with
pneumonia, the SpO2 recorded ranged from 50% to 99%.
Prevalence of hypoxemia in children with pneumonia
was 38.7%. Hypoxemia in children categorized according
to the severity of their illness is given in table 2.
On comparing oxygen saturation between the two age
groups of patients with pneumonia (Fig. 1), infants had a
higher frequency of hypoxemia and the difference
observed was statistically significant. (p value = 0.02,
Odd’s ratio 2.21, 95% CI 1.03, 4.76).
Age group vs oxygen saturation
<90%Spo2 > or =90%Spo2
Arterial Oxygen Saturation
Fig. 1. Age Group V ersus Oxygen Saturation.
Symptoms and Signs A ssociated with Hypoxemia :
Table 3 shows the distribution of prompted symptoms
and clinical signs that were significantly associated with
hypoxemia. Among symptoms, breathing difficulty, fast
breathing and inability to feed/ drink had significant
association with hypoxemia. Only 2 children with very
severe pneumonia had complaints of convulsions and
that is probably the reason why the results did not reach
statistical significance. Among the clinical signs, if the
child was lethargic, had nasal flaring, central cyanosis,
grunting, chest indrawing, tachypnea, tachycardia, fever
or crepitations on auscultation, significant association
with hypoxemia was found. Using WHO cut-off values
for defining tachypnea: in the age group 2 -12 months,
36(87.8%) of the children with hypoxemia compared with
53(55.8%) without were tachypneic, p value of <0.001; in
the 13-60 month olds, 17(100%) of the hypoxic children
compared with 55(56.7%) without hypoxemia were
tachypneic, p value of 0.001.
Sensitivity and specificity of clinical signs and
symptoms : Table 3 also shows the sensitivity and
specificity of signs and symptoms in hypoxemic and non-
hypoxemic children that were significantly associated
with hypoxemia. Chest indrawing had a sensitivity of
68.9% and specificity of 82.6%. Tachypnea in both age
groups were found to be useful clinical signs with
sensitivity of 90% and specificity of 43.6% in 2-12 month
olds and sensitivity of 100% with specificity of 43.2% in
13-60 months of age. A complaint of difficulty breathing
and fast breathing in a child by the caretakers, crepitations
on auscultation of the chest and fever on examination
were sensitive but non-specific indicators of hypoxemia.
On the other hand, inability to feed, lethargy, nasal
flaring, cyanosis and grunting were highly specific but
relatively insensitive signs.
In the study conducted at an altitude of approximately
1300m above sea level, prevalence of hypoxemia (SpO2 of
< 90%) in children 2-60 months old with pneumonia was
38.7%. Studies reporting prevalence of hypoxemia
measured by pulse oximetry show wide variations and
are not comparable because the cut-off values used to
define hypoxemia; study population, setting and the
altitude in which they were conducted differ.4,5,7-12
In the present study, all the patients with very severe
pneumonia, 80% with severe pneumonia and 18% with
pneumonia were hypoxic. None of the children with
cough and cold had hypoxemia. In a systematic review of
published literature, Lozano also reports that the
frequency of hypoxemia (pooled prevalence) is
determined by the severity of the illness. While outpatient
children and those with a clinical diagnosis of upper acute
respiratory illness (ARI) had a low risk of hypoxemia
(pooled estimate of 6-9%), the prevalence increased
among hospitalized children (47%) and those with
radiographically confirmed pneumonia (72%).13
T ABLE 3. Frequency of Symptoms and Signs that were Associated Significantly with Hypoxemia.
Clinical Features Hypoxemic
P-V alue Sensitivity Specificity
Inability To feed
2-12months (>=50/ Min)
13-60months (>=40/ Min)
Indian Journal of Pediatrics, Volume 73—September, 2006 779
Sudha Basnet et al
Of the 250 enrolled children in this study there were a
significantly higher number of infants and they were also
noted to have significantly higher frequency of
hypoxemia. Infants are vulnerable to acute respiratory
infections because, not only do they have less mature
immune systems14 but are also unable to clear secretions.
They also cannot verbally communicate their distress and
this may predispose them to present with hypoxemia on
arrival at the hospital. Other studies on hypoxemia in
children with ARI have not assessed the role of age as a
risk factor.13 On the other hand, age below 12 months has
been identified as a predictor of mortality in children with
pneumonia.15, 16 Although these studies do not prove that
the children who were at risk of dying were hypoxemic,
other studies have found an association between
hypoxemia and mortality in children with pneumonia .4, 5
Symptoms reported by caretakers of difficulty
breathing, fast breathing and inability to feed/ drink was
significantly associated with hypoxemia in the present
study. Severely reduced feeding in studies by Usen5 and
Weber 10 and history of difficult respiration in infants by
Onyango4 was significantly associated with hypoxemia.
The signs significantly associated with hypoxemia in
the study were lethargy, nasal flaring, central cyanosis,
grunting, chest indrawing, crepitations and tachypnea. A
child was called lethargic if he/ she was drowsy and not
showing interest in what was happening. Impaired
rousability5, unresponsiveness4 and noted as being
drowsy12 in other studies had good correlation with
hypoxemia. In these studies grunting was also
significantly associated with hypoxemia. 4,5,12 Nasal flaring
and cyanosis was significantly associated with hypoxemia
in other studies.5, 9, 12 Presence of chest indrawing in
children with pneumonia is used to categorize
pneumonia as severe and requiring admission.6 This sign
was also significantly associated with hypoxemia in the
studies done in K enya4 and Delhi.11 Other studies
showing significant association between crepitations and
hypoxemia were those by Onyango4, Usen5, Smyth10 and
Tachypnea in the present study was defined using cut
off values based on age according to WHO guidelines. 6
Higher respiratory rates used in studies by Onyango4 (>
or = 60/ min and 70/ min), Usen5 (>60/ min, 70/ min and
90/ min) and Smyth10 (>70/ min) in infants were found to
be significantly associated with hypoxemia. In order to
compare findings with these studies a respiratory rate of
> or = 70/ min was analyzed and found to be significantly
associated with hypoxemia.
Chest indrawing with a sensitivity of 68.9% and
specificity of 82.6% was the best clinical predictor of
hypoxemia in this study. In studies done by Reuland7 and
Weber9, sensitivity/ specificity of chest indrawing as a
predictor of hypoxemia in 2-60 month old children was
35/ 94 and 49/ 60 respectively. Similarly in the study by
Kabra 11, chest indrawing had a sensitivity of 35.7% and
specificity 86.4% in children < 5 years of age. Although
the findings differ, all studies are able to show that chest
indrawing is not uniformly sensitive but a fairly specific
sign in the prediction of hypoxemia. Absence of this sign
is likely to miss only a small percentage of patients with
pneumonia who are also hypoxemic.
Tachypnea in patients 2-12 months of age (respiratory
rate of > or = 50/ min) predicted hypoxemia with a
sensitivity of 90% and specificity of 43.6% in the present
study. In Lozano’s study similar respiratory rates in
infants had a sensitivity of 76% and specificity of 71%. 8 In
Smyth’s study in the same age group of children higher
respiratory rate of >70/ min had 63% sensitivity and 89%
specificity.10 In Onyango’s study sensitivity of 86% and
specificity of 56% with respiratory rate of > or = 60/ min
changed to 51% sensitivity and 83% specificity when
respiratory rate was > or = 70/ min in infants. 4 Similarly
in the study by Kabra, increasing the respiratory cut off
by 10/ minute lead to a decline in sensitivity from 82.1%
to 53.6% and increment in specificity from 51.8% to 77.8%.
11 The present study was also able to demonstrate a
decrease in sensitivity (42%) and rise in specificity (73%)
when analysis was done using a respiratory rate of >/ =
70/ min in infants. An elevated respiratory rate in a sick
child with pneumonia could result from the metabolic
acidosis secondary to the dehydration from fever, panting
and inability to drink as well as decreased peripheral
perfusion. This would limit the usefulness of increasing
respiratory rate in assessing the degree of hypoxia.17 In the
age group of 13-60 months, a respiratory rate of > or =40/
min was 100% sensitive and 43.2% specific in its ability to
predict hypoxemia. While Lozano reported 73%
sensitivity and 61% specificity using the same cut-off
values, 8 other studies have used higher respiratory rates
to calculate the sensitivity and specificity. Further analysis
using higher respiratory rates to compare findings was
not done in this sub-group.
This study shows a higher frequency of hypoxemia in
children with increasing severity of pneumonia. Clinical
predictors significantly associated with hypoxemia on
univariate analysis (lethargy, grunting, nasal flaring,
cyanosis, and complaint of inability to breastfeed/ drink)
are those used for the recognition of very severe
pneumonia in 2-60 month old children by WHO.6 The
study therefore validates WHO criteria for the recognition
of children with severe and very severe pneumonia. It
also supports the findings by Lozano that hypoxemia is
more frequent in those with increasing severity of ARI. 13
Age < or = 12 months as a risk factor for hypoxemia in
children with ARI, which has not been reported in other
studies is an important finding of this study. These are the
strengths of this study.
This study and a review of the literature of similar
studies show that no single clinical sign can predict
hypoxemia with both high sensitivity and specificity.
Other studies have used combination models to improve
the predictive value of clinical signs. While constructing
models, addition of signs improves sensitivity but
Indian Journal of Pediatrics, Volume 73—September, 2006 780
Hypoxemia in Children with Pneumonia and Its Clinical Predictors
decreases specificity and this would be of benefit in
settings where oxygen is freely available.18 In a developing
country like Nepal, with scarce resources the wastage of
oxygen needs to be minimized. In this study, a
combination model using signs for the prediction of
hypoxemia in settings with limited supply of oxygen was
not constructed. This is a major limitation of this study.
The increasing frequency of hypoxemia in children with
more severe illness and the clinical predictors identified in
the study validate the WHO classification of pneumonia
based on severity. In Nepal where pulse oximeters may
not always be available, simple clinical signs can still be
used to identify hypoxemia, classify pneumonia as severe
to very severe and administer oxygen. Children below 1
year of age with A RI are more likely to present with
hypoxemia according to our findings. This subgroup of
children should either be admitted for closer observation
and frequent monitoring or followed up more vigorously.
In the absence of pulse oximeters, they should receive
oxygen earlier if they fail to respond to conservative
1.? Reducing mortality from major killers of children. WHO Fact
sheet No. 178, revised September 1998
2.? Nepal Demographic and Health Survey 2001, Family Health
Division, Department of Health Services. Preliminary Report.
3.? Nepal Ministry of Health, Department of Health Services Annual
Report 2000 - 2001.
4.? Onyango FE, Steinhoff MC et al. Hypoxemia in young Kenyan
children with acute lower respiratory tract infection. BMJ
March 1993; 306 : 612-614.
5.? Usen S, Weber M, Mulholland K et al. Clinical predictors of
hypoxemia in Gambian children. BMJ Jan 1999; 318 : 86-91.
6.? Management of the child with a serious infection or severe
malnutrition. Guidelines For Care At The First Referral Level In
Developing Countries. World Health Organization, 2000.
7.? Reuland DS, Steinhoff MC, Gilman RH et al. Prevalence and
prediction of hypoxemia in children with respiratory infection
in the Peruvian Andes. J Pediatr Dec 1991; 119(6) : 900-906.
8.? Lozano JM, Steinhoff MC, Ruiz JG et al. Clinical predictors of
acute radiological pneumonia and hypoxemia at high altitude.
Arch Dis Child Oct 1994;71(4) : 323-327.
9.? Weber MW, Usen S, Palmer A et al. Predictors of hypoxemia in
hospital admissions with acute lower respiratory tract
infection in a developing country. Arch Dis Child April 1997;
76 : 310-314.
10.? Smyth A, Carty H, Hart CA. Clinical predictors of hypoxemia
in children with pneumonia. Ann Trop Pediatr Mar 1998; 18(1):
11.? Kabra SK, Lodha R et al. Can clinical symptoms and signs
accurately predict the prevalence of hypoxemia in children
with acute lower respiratory infections Indian Pediatrics 2004;
41 : 129-135.
12.? Laman M, Ripa P, Vince J et al. Can clinical signs predict
hypoxemia in Papua New Guinean children with moderate
and severe pneumonia. Ann Trop Paediatr 2005; 25 : 31-40.
13.? J.M. Lozano Epidemiology of hypoxemia in children with
acute lower respiratory tract infection. Int J Tuberc Lung Dis
2001; 5(6): 496-504.
14.? Regelmann WE, Hill HR, Cates KL, Quie PG. Immunology of
the newborn. In: Feigin RD, Cherry JD, eds. Textbook of Pediatric
Infectious Diseases. 3rd ed. Philadelphia: WB Saunders
Company, Harcourt Brace Jovanovich Inc, 1992 876–887.
15.? Sehgal V, Sethi GR, Sachdev HP et al. Predictors of mortality in
subjects hospitalized with acute lower respiratory tract
infections. Indian Pediatr Mar 1997; 34(3) : 213-219.
16.? Banajeh SM. Outcome for children under 5 years hospitalized
with severe acute lower respiratory tract infections in Yemen:
a 5-year experience. J Trop Pediatr Dec 1998; 44(6): 343-346.
17.? Dyke T, Brown N. Hypoxia in pneumonia: better detection
and more oxygen needed in developing countries. BMJ Jan
1994; 308 : 119-120.
18.? Usen S, Weber M. Clinical signs of hypoxemia in children with
acute lower respiratory infection: indicators of oxygen therapy.
Int J Tuberc Lung Dis 2001; 5(6): 505-510.
Indian Journal of Pediatrics, Volume 73—September, 2006 781
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