33

Original Article

Hypoxemia in Children with Pneumonia and Its Clinical

Predictors
Sudha Basnet1, Ramesh Kant Adhikari1 and Chitra Kumar Gurung2

Department of Pediatrics, 1Department of Community Medicine and Family Health, 2Institute of Medicine,
Kathmandu, Nepal.

ABSTRACT
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 (SpO 2 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 accurate and non-invasive tool for measuring arterial
a significant cause of mortality in children under 5 years oxygen saturation, assessment of hypoxemia in
of age. The World Health Organization (WHO) estimates pneumonia has become possible. A pulse oximeter,
that acute respiratory infection (ARI), mostly in the form however, is expensive and not suitable for routine use in
of pneumonia, is the leading cause of death in children a developing country like Nepal. To overcome this
under-five, killing over 2 million children annually.1 problem, clinical signs that best predict hypoxemia in
Nepal, a developing country has an under five mortality pneumonia have been evaluated in earlier studies in other
rate of 91/1000 live births2 and an infant mortality rate of developing countries. Clinical features like cyanosis,
64/1000 live births.2 Annual incidence of pneumonia in < tachypnea, grunting, head nodding, inability to cry, no
5 years is 90/1000, with 4.2/1000 children having severe spontaneous movement during clinical examination and
pneumonia.3 Hypoxemia in pneumonia has been shown chest retractions have been identified as the best clinical
to be a risk factor for death. Hypoxic children with predictors of hypoxemia.4, 5 The Integrated Management
pneumonia are five times more likely to die than those of Childhood Illnesses (IMCI) also makes use of clinical
without in studies done in Kenya and Gambia.4, 5 Such an features to classify pneumonia into various categories
association between hypoxemia and pneumonia suggests based on severity.
that its early detection and treatment are important At the Kanti Children’s Hospital, although acute
aspects in the management of children with pneumonia. respiratory illness is the most frequent reason for
With the introduction of the pulse oximeter, a sufficiently 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
Correspondence and Reprint requests : Dr. Sudha Basnet, EPC 376, with pneumonia who really need oxygen as therapy?
GPO Box 8975, Kathmandu, Nepal. Phone: 977-1- 4412202; Fax: 977­ Would certain clinical features help us to identify hypoxic
1-4418186. E-mail: [email protected] children? This study was done to find the prevalence of

Indian Journal of Pediatrics, Volume 73—September, 2006 777

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Sudha Basnet et al

hypoxemia in children with pneumonia and identify its • Patients with pneumonia
clinical predictors. It is based on the hypothesis that • Patients with severe pneumonia
hypoxemia in pneumonia can be predicted clinically by • Patients with very severe pneumonia.
assessing the various symptoms and signs associated Patients were excluded from the study if:
with it. • 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
MATERIALS AND METHODS
mentioned above.
After completion of the examination, patients were
A cross sectional study was conducted from 14 th either sent home with treatment or admitted to the
December 1999 to 18th July 2000 at the Kanti Children’s hospital for further management.
Hospital in the Kathmandu valley that lies at an altitude Statistical analysis : This was done using the Epi Info
of about 1336 meters above sea level. Children between 2 Version 6 program in the computer. Clinical signs
months to 5 years of age who presented to the Outpatient between hypoxemic and non-hypoxemic children were
or the Emergency Department with a complaint of cough compared using the Chi square test, or by the Fisher’s
or difficulty breathing were assessed. Relevant history of exact test if the expected frequencies were less than 5.
the illness and examination was conducted according to a A p value of < or = 0.05 was considered significant. The
questionnaire prepared for the purpose of the study sensitivity and specificity of each clinical sign in its ability
before the child received any form of treatment at the to predict hypoxemia was also calculated.
hospital. During the physical examination, arterial
oxygen saturation was recorded using a portable, battery
RESULTS
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 In the study conducted over a period of seven months, a
that was stable for at least 3 minutes was noted down. total of 264 subjects were interviewed and examined. 14
Hypoxemia was defined as an arterial oxygen saturation children were excluded from the study, as they could not
of <90% recorded by pulse oximetry. An arterial oxygen be classified into any category of illness as specified in the
saturation of 90% generally corresponds to an arterial methodology.
oxygen tension of 60-70mm Hg. This relation however is The distribution of patients according to age and
affected by factors such as temperature, pH, altitude and category of illness is shown in table 1. Age range was 2 –
age. To overcome this problem, oxygen saturation by 60 months with a median of 12 months (interquartile
oximetry was recorded in children presenting with just range 6 - 26). 123(49.2%) were females and 127(50.8%)
cough and cold (assumed to be healthy children and were males. There was no difference in the number of
therefore acting as the control group) to determine the males to females in all categories of illness (p value = 0.4).
normal range in all the children entered in the study. There were a significantly higher number of infants with
Based on the clinical findings the patients were then respiratory illness (p value = 0.03). On assessment, none
categorized into four groups using the WHO guidelines 6: of the children with cough and cold had SpO2 of < 90%.
• Patients with cough and cold The mean oxygen saturation in this group was 96%

Table 1. Distribution of Children According to Age and Diagnosis

Diagnosis

AGE Cough & Cold Pneumonia Severe Pneumonia Very Severe Pneumonia Total

2-12 months 46 (46.0)* 56 (53.3) 16 (64.0) 16 (80.0) 134 (53.6)

13-60 months 54 (54.0) 49 (46.7) 9 (36.0) 4 (20.0) 116 (46.4)
Total 100 (100.0) 105 (100.0) 25 (100.0) 20 (100.0) 250 (100.0)

(Figures in brackets are percentages unless otherwise stated.)

TABLE 2. Prevalence of Hypoxemia in Cases With Pneumonia.

Diagnosis

Oxygen Saturation Pneumonia Severe Pneumonia Very Severe Pneumonia Total

<90%SpO2 18 (17.0)* 20 (80.0) 20 (100.0) 58 (38.7)

> or =90%Sp O2 87 (83.0) 5 (20.0) 0 92 (61.3)
Total 105 (100.0) 25 (100.0) 20 (100.0) 150 (100.0)

*(%)

778 Indian Journal of Pediatrics, Volume 73—September, 2006

35

Hypoxemia in Children with Pneumonia and Its Clinical Predictors

(standard deviation of 2.123). In children with Sensitivity and specificity of clinical signs and
pneumonia, the SpO2 recorded ranged from 50% to 99%. symptoms : Table 3 also shows the sensitivity and
Prevalence of hypoxemia in children with pneumonia specificity of signs and symptoms in hypoxemic and non-
was 38.7%. Hypoxemia in children categorized according hypoxemic children that were significantly associated
to the severity of their illness is given in table 2. with hypoxemia. Chest indrawing had a sensitivity of
On comparing oxygen saturation between the two age 68.9% and specificity of 82.6%. Tachypnea in both age
groups of patients with pneumonia (Fig. 1), infants had a groups were found to be useful clinical signs with
higher frequency of hypoxemia and the difference sensitivity of 90% and specificity of 43.6% in 2-12 month
observed was statistically significant. (p value = 0.02, olds and sensitivity of 100% with specificity of 43.2% in
Odd’s ratio 2.21, 95% CI 1.03, 4.76). 13-60 months of age. A complaint of difficulty breathing
and fast breathing in a child by the caretakers, crepitations
Age group vs oxygen saturation on auscultation of the chest and fever on examination
60 were sensitive but non-specific indicators of hypoxemia.
Total Number

50
40 2-12 m On the other hand, inability to feed, lethargy, nasal
30
13-60m flaring, cyanosis and grunting were highly specific but
20
10 relatively insensitive signs.
0
<90%Spo2 > or =90%Spo2

Arterial Oxygen Saturation DISCUSSION

Fig. 1. Age Group Versus Oxygen Saturation.

In the study conducted at an altitude of approximately

Symptoms and Signs Associated with Hypoxemia : 1300m above sea level, prevalence of hypoxemia (SpO 2 of
Table 3 shows the distribution of prompted symptoms < 90%) in children 2-60 months old with pneumonia was
and clinical signs that were significantly associated with 38.7%. Studies reporting prevalence of hypoxemia
hypoxemia. Among symptoms, breathing difficulty, fast measured by pulse oximetry show wide variations and
breathing and inability to feed/drink had significant are not comparable because the cut-off values used to
association with hypoxemia. Only 2 children with very define hypoxemia; study population, setting and the
severe pneumonia had complaints of convulsions and altitude in which they were conducted differ.4,5,7-12
that is probably the reason why the results did not reach In the present study, all the patients with very severe
statistical significance. Among the clinical signs, if the pneumonia, 80% with severe pneumonia and 18% with
child was lethargic, had nasal flaring, central cyanosis, pneumonia were hypoxic. None of the children with
grunting, chest indrawing, tachypnea, tachycardia, fever cough and cold had hypoxemia. In a systematic review of
or crepitations on auscultation, significant association published literature, Lozano also reports that the
with hypoxemia was found. Using WHO cut-off values frequency of hypoxemia (pooled prevalence) is
for defining tachypnea: in the age group 2 -12 months, determined by the severity of the illness. While outpatient
36(87.8%) of the children with hypoxemia compared with children and those with a clinical diagnosis of upper acute
53(55.8%) without were tachypneic, p value of <0.001; in respiratory illness (ARI) had a low risk of hypoxemia
the 13-60 month olds, 17(100%) of the hypoxic children (pooled estimate of 6-9%), the prevalence increased
compared with 55(56.7%) without hypoxemia were among hospitalized children (47%) and those with
tachypneic, p value of 0.001. radiographically confirmed pneumonia (72%).13

TABLE 3. Frequency of Symptoms and Signs that were Associated Significantly with Hypoxemia.

Clinical Features Hypoxemic Non-Hypoxemic P-Value Sensitivity Specificity

Children (n=58) Children (n=92)

Symptoms
Breathing difficulty 55 70 0.002 94.8 23.9
Fast breathing 54 65 <0.001 93.1 29.3
Inability To feed 16 1 <0.001 27.6 98.9
Signs
Lethargy 23 0 <0.001 39.7 100
Nasal flaring 28 2 <0.001 48.3 97.8
Central cyanosis 3 0 0.05 5.2 100
Grunting 21 1 <0.001 36.2 98.9
Chest indrawing 40 16 <0.001 68.9 82.6
Crepitations/Tachypnoea 54 71 0.01 93.1 22.8
2-12months (>=50/Min) 36 53 <0.001 90 43.6
13-60months (>=40/Min) 17 55 0.001 100 43.2

Indian Journal of Pediatrics, Volume 73—September, 2006 779

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Sudha Basnet et al

Of the 250 enrolled children in this study there were a the findings differ, all studies are able to show that chest
significantly higher number of infants and they were also indrawing is not uniformly sensitive but a fairly specific
noted to have significantly higher frequency of sign in the prediction of hypoxemia. Absence of this sign
hypoxemia. Infants are vulnerable to acute respiratory is likely to miss only a small percentage of patients with
infections because, not only do they have less mature pneumonia who are also hypoxemic.
immune systems14 but are also unable to clear secretions. Tachypnea in patients 2-12 months of age (respiratory
They also cannot verbally communicate their distress and rate of > or = 50/min) predicted hypoxemia with a
this may predispose them to present with hypoxemia on sensitivity of 90% and specificity of 43.6% in the present
arrival at the hospital. Other studies on hypoxemia in study. In Lozano’s study similar respiratory rates in
children with ARI have not assessed the role of age as a infants had a sensitivity of 76% and specificity of 71%. 8 In
risk factor.13 On the other hand, age below 12 months has Smyth’s study in the same age group of children higher
been identified as a predictor of mortality in children with respiratory rate of >70/min had 63% sensitivity and 89%
pneumonia.15, 16 Although these studies do not prove that specificity.10 In Onyango’s study sensitivity of 86% and
the children who were at risk of dying were hypoxemic, specificity of 56% with respiratory rate of > or = 60/min
other studies have found an association between changed to 51% sensitivity and 83% specificity when
hypoxemia and mortality in children with pneumonia .4, 5 respiratory rate was > or = 70/min in infants. 4 Similarly
Symptoms reported by caretakers of difficulty in the study by Kabra, increasing the respiratory cut off
breathing, fast breathing and inability to feed/drink was by 10/minute lead to a decline in sensitivity from 82.1%
significantly associated with hypoxemia in the present to 53.6% and increment in specificity from 51.8% to 77.8%.
study. Severely reduced feeding in studies by Usen5 and 11
The present study was also able to demonstrate a
Weber 10 and history of difficult respiration in infants by decrease in sensitivity (42%) and rise in specificity (73%)
Onyango4 was significantly associated with hypoxemia. when analysis was done using a respiratory rate of >/=
The signs significantly associated with hypoxemia in 70/min in infants. An elevated respiratory rate in a sick
the study were lethargy, nasal flaring, central cyanosis, child with pneumonia could result from the metabolic
grunting, chest indrawing, crepitations and tachypnea. A acidosis secondary to the dehydration from fever, panting
child was called lethargic if he/she was drowsy and not and inability to drink as well as decreased peripheral
showing interest in what was happening. Impaired perfusion. This would limit the usefulness of increasing
rousability 5 , unresponsiveness 4 and noted as being respiratory rate in assessing the degree of hypoxia.17 In the
drowsy 12 in other studies had good correlation with age group of 13-60 months, a respiratory rate of > or =40/
hypoxemia. In these studies grunting was also min was 100% sensitive and 43.2% specific in its ability to
significantly associated with hypoxemia. 4,5,12 Nasal flaring predict hypoxemia. While Lozano reported 73%
and cyanosis was significantly associated with hypoxemia sensitivity and 61% specificity using the same cut-off
in other studies. 5, 9, 12 Presence of chest indrawing in values, 8 other studies have used higher respiratory rates
children with pneumonia is used to categorize to calculate the sensitivity and specificity. Further analysis
pneumonia as severe and requiring admission.6 This sign using higher respiratory rates to compare findings was
was also significantly associated with hypoxemia in the not done in this sub-group.
studies done in Kenya 4 and Delhi. 11 Other studies This study shows a higher frequency of hypoxemia in
showing significant association between crepitations and children with increasing severity of pneumonia. Clinical
hypoxemia were those by Onyango4, Usen5, Smyth10 and predictors significantly associated with hypoxemia on
Kabra.11 univariate analysis (lethargy, grunting, nasal flaring,
Tachypnea in the present study was defined using cut­ cyanosis, and complaint of inability to breastfeed/drink)
off values based on age according to WHO guidelines. 6 are those used for the recognition of very severe
Higher respiratory rates used in studies by Onyango4 (> pneumonia in 2-60 month old children by WHO. 6 The
or = 60/min and 70/min), Usen5 (>60/min, 70/min and study therefore validates WHO criteria for the recognition
90/min) and Smyth10 (>70/min) in infants were found to of children with severe and very severe pneumonia. It
be significantly associated with hypoxemia. In order to also supports the findings by Lozano that hypoxemia is
compare findings with these studies a respiratory rate of more frequent in those with increasing severity of ARI. 13
> or = 70/min was analyzed and found to be significantly Age < or = 12 months as a risk factor for hypoxemia in
associated with hypoxemia. children with ARI, which has not been reported in other
Chest indrawing with a sensitivity of 68.9% and studies is an important finding of this study. These are the
specificity of 82.6% was the best clinical predictor of strengths of this study.
hypoxemia in this study. In studies done by Reuland7 and This study and a review of the literature of similar
Weber9, sensitivity/specificity of chest indrawing as a studies show that no single clinical sign can predict
predictor of hypoxemia in 2-60 month old children was hypoxemia with both high sensitivity and specificity.
35/94 and 49/60 respectively. Similarly in the study by Other studies have used combination models to improve
Kabra 11, chest indrawing had a sensitivity of 35.7% and the predictive value of clinical signs. While constructing
specificity 86.4% in children < 5 years of age. Although models, addition of signs improves sensitivity but

780 Indian Journal of Pediatrics, Volume 73—September, 2006

37

Hypoxemia in Children with Pneumonia and Its Clinical Predictors

decreases specificity and this would be of benefit in hypoxemia in Gambian children. BMJ Jan 1999; 318 : 86-91.
settings where oxygen is freely available.18 In a developing 6. Management of the child with a serious infection or severe
malnutrition. Guidelines For Care At The First Referral Level In
country like Nepal, with scarce resources the wastage of
Developing Countries. World Health Organization, 2000.
oxygen needs to be minimized. In this study, a 7. Reuland DS, Steinhoff MC, Gilman RH et al. Prevalence and
combination model using signs for the prediction of prediction of hypoxemia in children with respiratory infection
hypoxemia in settings with limited supply of oxygen was in the Peruvian Andes. J Pediatr Dec 1991; 119(6) : 900-906.
not constructed. This is a major limitation of this study. 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.
CONCLUSION 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;
The increasing frequency of hypoxemia in children with 76 : 310-314.
10. Smyth A, Carty H, Hart CA. Clinical predictors of hypoxemia
more severe illness and the clinical predictors identified in in children with pneumonia. Ann Trop Pediatr Mar 1998; 18(1):
the study validate the WHO classification of pneumonia 31-40.
based on severity. In Nepal where pulse oximeters may 11. Kabra SK, Lodha R et al. Can clinical symptoms and signs
not always be available, simple clinical signs can still be accurately predict the prevalence of hypoxemia in children
used to identify hypoxemia, classify pneumonia as severe with acute lower respiratory infections Indian Pediatrics 2004;
41 : 129-135.
to very severe and administer oxygen. Children below 1
12. Laman M, Ripa P, Vince J et al. Can clinical signs predict
year of age with ARI are more likely to present with hypoxemia in Papua New Guinean children with moderate
hypoxemia according to our findings. This subgroup of and severe pneumonia. Ann Trop Paediatr 2005; 25 : 31-40.
children should either be admitted for closer observation 13. J.M. Lozano Epidemiology of hypoxemia in children with
and frequent monitoring or followed up more vigorously. acute lower respiratory tract infection. Int J Tuberc Lung Dis
2001; 5(6): 496-504.
In the absence of pulse oximeters, they should receive
14. Regelmann WE, Hill HR, Cates KL, Quie PG. Immunology of
oxygen earlier if they fail to respond to conservative the newborn. In: Feigin RD, Cherry JD, eds. Textbook of Pediatric
management. Infectious Diseases. 3rd ed. Philadelphia: WB Saunders
Company, Harcourt Brace Jovanovich Inc, 1992 876–887.
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subjects hospitalized with acute lower respiratory tract
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Division, Department of Health Services. Preliminary Report.
17. Dyke T, Brown N. Hypoxia in pneumonia: better detection
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18. Usen S, Weber M. Clinical signs of hypoxemia in children with
4. Onyango FE, Steinhoff MC et al. Hypoxemia in young Kenyan
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Int J Tuberc Lung Dis 2001; 5(6): 505-510.
March 1993; 306 : 612-614.
5. Usen S, Weber M, Mulholland K et al. Clinical predictors of

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