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-1-Journal of Nepal Paediatric Society January-June, 2010/Vol 30/Issue 1

Original Article January-June, 2010/Vol 30/Issue 1

Is Low Hemoglobin Level a Risk Factor for Acute Lower 

Respiratory Tract Infections?

Malla T1, Pathak OK2, Malla KK3 

1Dr. Tejesh Malla, MBBS, MD, Assistant Professor, 2 Dr. Om K Pathak, MBBS, Medical Officer, 3Dr. Kalpana K Malla, MBBS, 
MD, Associate Professor. All from the Department of Paediatrics, Manipal College of Medical Sciences, Pokhara, Nepal.

Address for correspondence: Dr. Tejesh Malla, E-mail: tejeshmalla@hotmail.com

Abstract
Objective: This prospective study was conducted to evaluate whether a low hemoglobin level, was a 
risk factor for Acute Lower Respiratory Tract Infections (ALRTI) in children. Methods: 150 Children of 
all age groups who came to the outpatient department and those admitted for ALRTI were included in 
the study. Age and sex-matched 140 children, not having any respiratory illness, were taken as control. 
The study period was from March 2006 - March 2007. Detailed clinical and laboratory evaluation of the 
enlisted patients was done. All were subjected to detail investigations. Results: Radiological evidence of 
pneumonia was present in 70 (50 %) children.Hyperinflated lungs were seen in 40 (29%) and was normal 
in 30 (21.4%) cases. Blood culture was positive in 14 (10%) children of study group and none among 
control group. Klebsiella was the commonest organism isolated 6 (4.2%) in blood culture positive cases. 
The mean Hemoglobin (Hb) level of study group was 9.88 gm% and it was 12 gm% in control group.96 
(68.6%) of study group and 30 (21.42%) of control group had anemia. Of the anemic children, 79 (82.3%) 
in study group had iron deficiency, and 17 (17.7%) had normocytic normochromic anemia. These values 
were 18 (33.3%) and 36 (66.6%) respectively for control group. Low hemoglobin level was a risk factor 
(p<0.001) ALRTI. Conclusion: Anemic children were 3.2 times more susceptible to ALRTI compared to 
the control group and and iron deficiency anemia was predominating. Supplemental iron therapy may 
reduce the incidence of ALRTI. Prevention of anemia, due to whatever etiology is also essential.

Key words: ALRTI, anemia, hemoglobin.

Introduction

Anemia is a major nutritional global problem of immense public health signifi cance, affecting 
persons of all ages, sex and economic group. It is ranked 
as the commonest chronic malady of mankind affecting 
approximately 30% i.e. 1500 million people all over the 
world. Iron defi ciency anemia in children occurs most 
frequently between the age of 6 months to 3 years1, the 
age when repeated infection occurs. On an average, 
children below 5 years of age suffer about 5-6 episodes 
of ALRTI per year2. With this view the present study was 
conducted to see if children with iron defi ciency anemia 
were at higher risk of ALRTI.

Methods

This prospective study was carried out for a 
period of one year from March 2006 – March 2007 in 
pediatric department of Manipal Teaching Hospital, 
Pokhara. A total of 290 (150 cases and140 controls) 
children from 1 month to 5 years of age attending out 
patient department and those hospitalized were studied. 
Controls were age and sex matched children not having 
respiratory problems. The inclusion criteria for cases 
were children with fever, cough, and fast respiratory 
rate, chest indrawing as per WHO criteria, and ronchi 
or crepitations on auscultation. The exclusion criteria 
was children suffering from other systemic illnesses like 



-2-January-June, 2010/Vol 30/Issue 1 Journal of Nepal Paediatric Society

Congenital heart disease, tuberculosis (any evidence 
plus Montaux test positive cases) and Protein Energy 
Malnutrition (PEM > Grade III as per Indian Academy 
of Pediatrics (IAP) classifi cation). Children who already 
received antibiotic from outside were also excluded 
from the study. The purpose of the study was explained 
to the parents or guardians. Then consent was taken 
from parents or guardians before they were subjected 
to investigations. The investigations in both case and 
control included; complete blood count (CBC) with a 
peripheral smear, blood culture and sensitivity test, and 
X-ray chest, serum iron and serum iron binding capacity. 
Serumferritin level was not done. Syanmeth method by 
colorimeter was used to identify Hb level. Hemglobin 
level < 10 gm % will be considered low in this study. Data 
were analysed using SPSS 10.0 by logistic multinomial 
regression analysis.

Results

Out of 290 children 150 were cases among which 
10 were Mantoux positive hence was excluded from 
the study. Therefore the fi nal fi gure was 140 (99 males 
and 41 females) cases and 140 (94 males and 46 
females) controls. Among the cases 10 (8 males and 
2 females) were less than 2 months, 69 (43 M and 26 
F) were inbetween 2months – 1 year and 61 ( 48M and 
13F ) were above 1 year. Similarly for control group 
the distribution was 10 (6M/4F), 50(30M/20F), and 80 
(58M/22F) were ≤2months, 2mo-1year and >1 year 
respectively. (Table1). Fever, cough and shortness of 
breath was main clinical features in the cases whereas 
fever, pain abdomen diarrhea, vomiting, seizures was 

main clinical features in the control group (Table 2). 
Radiological evidence of pneumonia was present in 
70 (50 %) children, hyperinfl ated lungs in 40 (29%) 
cases and normal in 30 (21.4%) cases (Fig 1). Out of 
40 children who had hyperinfl ated lung fi elds 20 (50%) 
had a history of recurrent wheeze ( fi g.2) and 10 ( 25%) 
gave a positive family history of asthma. Blood culture 
was positive in 14 (10 %) children of study group (Table 
3) and none among control group. Among the culture 
positives klebsiella was isolated in 6 (4.2%), and 
growth of staphylococcus, streptococcus pneumoniea, 
acintobacter and E.coli was noted in 2 (1.43%) cases 
each. The mean Hb level of study group was 9.88 gm% 
and it was 12 gm% in control group.96 (68.6%) of study 
group and 30 (21.42%) of control group had anemia. 
Of the anemic children, 79(82.3%) in study group had 
iron defi ciency, with mean MCV 64 (fl ),Mean MCH 
17pg,MCHC 25gm/dl,Mean S. Iron 35μg/dL,Mean TIBC 
390μg/dL.17 (17.7%) had normocytic normochromic 
anemia. These values were 18 (33.3%) [With mean MCV 
68.7 (fl ), Mean MCH 15pg, Mean MCHC 27gm/dl, Mean 
S. Iron 35μg/dL, Mean TIBC 350μg/dL] and 36 (66.6%) 
respectively for control group (Table 4). There were 72 
cases of bronchopneumonia among which 62 (86%) 
of them were anemic whereas rest 68 were wheeze 
associated ALRTI (bronchiolitis & recurrent wheeze ) 
of which 34 (50%) were anemic.(Table 5). Descriptive 
data regarding multivariate logistic regression analysis 
showing the risk factor of ALRTI. Table 7 reveals the 
montaux positive cases which were excluded from the 
study.

Table 1: Age and Sex distribution of cases and control

Sex
 Age

Total
≤2 months >2mo-1yr >1 -5 year

Case ;
Male=99 (70.7%)
Female=41(29.3%)

8
2

43
26

48
13

140

Total 10 69 61 140

Control:
Male= 94 (67%)
Female=46 (32.8%) 

6
4

30
20

58
22

140

Total 10 50 80 140



-3-Journal of Nepal Paediatric Society January-June, 2010/Vol 30/Issue 1

Table 2: Symptoms and signs at presentation

Symptoms
Case Control

N (n=140) Percentage N(n=140 ) Percentage
Fever 135 96.42% 114 81.42%
Cough 140 100% 8 5.71%
Shortness of breath 81 57.85% 4 2.85%
Convulsion 10 7.14% 30 21.42%
Vomiting 29 20.71% 77 55%
Diarrhea 10 7.14% 52 37.14%
Noisy breathing 50 35.71% 0 0%
Poor feeding 80 57.14% 60 42.85%
Chest pain 4 2.85% 0 0%
Irritable 20 14.28% 30 21.42%
Fast breathing 100 71.42% 0 0%
Delayed development 0 0% 6 4.28%
Headache 0 0% 2 1.42%
Pain abdomen 0 0% 35 25%
Sore throat 0 0 % 24 17%
Signs
Chest indrawings 120 85.71% 0 0%
Ronchi 70 50% 0 0%
Crepitations 60 42.85% 0 0%
Pyoderma 0 0% 4 2.85%
Dehydration 5 3.57% 35 25%

Table 3: Blood culture of cases and control

Case (n=140) Control (n=140) 

Blood culture Number Percentage Number Percentage 
No growth
Growth 
Klebsiella
Staphylococcus
S. Pneumniea
Acintobacter 
E.coli

126
14
6
2
2
2
2

90 %
10%
4.2%

1.43%
1.43%
1.43%
1.43%

140
0

100%
0%

0

10

20

30

40

50

Ser

0%

0%

0%

0%

0%

0%

pneum
ies1 50

monia h
0%

50%

yperinflation
29%

29%

norma
21.40%

21.4

al
%

40%

Series1

Fig. 1: Radiological fi ndings of cases



-4-January-June, 2010/Vol 30/Issue 1 Journal of Nepal Paediatric Society

Table 4: Hemogram of Cases and Control.

Case (n=140) Control (n=140) 

Hemoglobin Number Percentage Number Percentage 
Mean Hb 9.88gm % 12gm %

Hemoglobin
≤10gm%±
>10gm%

96 
44

68.6%)
31.4%

54
86

38.6%
61.4%

Anemia type 
MH*
NN**

79
17

82.3%
17.7%

18
36

33.3%
66.6%

MH anemia NN anemia MH anemia NN anemia
Mean MCV(fl )*** 64  80 68.7 79
Mean MCH(pg)**** 17  25 15 27
Mean MCHC(gm/dl)***** 25  32 27 34
S. Iron 35μg/dL  95 35 μg/dL 100
Mean TIBC+ 390 μg/dL  268 350 μg/dL 270

Note : Anemic± = Hb< 10gm/dl (Normal Hb in < 2mo 9 – 14 gm/dl and > 2months 11.5-15.5gm/dl)3 MH*= Microcytic 
Hypochromic, NN**=Normocytic Normochromic, MCV***=Mean Corpuscular Volume ( 1month- 6 yrs = 76-
88(fl ),4MCH****=Mean Corpuscular Hemoglobin ( 1month- 6 yrs= 24-30 (pg ),4 MCHC*****= Mean corpuscular 
Hemoglobin Concentration ( 1month- 6 yrs=30-36gm/dl),4 S.Iron (infants =100-400 μg/dL and above Infancy =250-400 
μg/dL)3,TIBC+ -Total Iron Binding Capacity (all age =22-184 μg/dL )3

50% 50%
h

N

h/o wheezing  

No Wheezing

Fig. 2: Histrory of wheezing 

0

5

10

15

20

1 7 13 19 25 31 37 43 49 55 61 67 73 79 85 91 97 103 109 115 121 127 133 139

children in case and control

H
b 

le
ve

l i
n 

gm
%

Series1 Series2

Fig. 3: Graph showing range of Hb in case and control



-5-Journal of Nepal Paediatric Society January-June, 2010/Vol 30/Issue 1

Discussion

Acute lower Respiratory tract infection (ALRTI) is 
a leading cause of mortality in children below 5 years 
of age in developing countries5. Hence it is important to 
control the risk factors to prevent deaths from ALRTI. 
Along with many risk factors like low birth weight, lack 
of breast feeding, severe malnutrition, smoke, cooking 
fuel6, low hemoglobin may also be a risk factor. Present 
study was carried out to prove this fact.There were 140 
cases (M=99 & F= 41) and 140 controls (M=94&F=46) 
among which in cases maximum children were between 
2month – 1 year.This signifi es that ALRTI is most 
common in age group 2month to 1 year. This is the time 
when a child starts having low hemoglobin levels and 
also this is the period of adding supplemental feed which 
may be inadequate and inappropritate. The reasons for 
higher number of males may be gender biasness by the 
parents to bring them for hospital care. Sign symptoms of 
patient had usual presentation of ALRTI. These patients 
came to us only after 4-5 days of illness or when the 
child became more ill as with less illness people of this 
region do not visit hospital. Radiologically evidence of 
pneumonia was higher 70 (50 %) than hyperinfl ated 
lungs (bronchiolitis, recurrent wheeze) 40 (29%).This 

Table 5: Low Hemoglobin with type of ALRTI

Bronchopneumonia (N= 72)
Wheeze associated LRTI bronchiolitis / 

recurrent wheezing (N= – 68 )

Number percentage Number percentage

Hemoglobin
≤10gm%
>10gm%

62
10

86.0 %
13.9 %

34
34

50 %
50 %

Total =140 72 100% 68 100%

Table 6: Multivariate Logistic Regression Analysis Showing the Risk factor of ALRTI 

Parameters OR 95% CI Signifi cance
HB≤10 5.6 2.7-11.7 df=1, p<0.001
S.Iron 15.6 8.2-29.6 df=1, p<0.001
TIBC 1.7 0.86-3.4 df=1, p= 0.119

C.I: Confi dence interval, OR: Odds Ratio,df:degree of freedom, LRTI- Lower Respiratory Tract Infection.

Table 7: History, Clinical fi nding and CXR of Mantoux positive cases.

Cases with Mantoux positive 1 2 3 4 5 6 7 8 9 10
Recurrent ARI + + - + - + + + + +
ESR > 50mm/1st hr + + + + + + + + + +
Contact with TB - - + + + _ _ - + -
Weight loss + + + + - - + + + +
CXR – compatible with tuberculosis + + - - - - - - + +
Gastric lavage for AFB _ _ _ _ _ _ _ _ _ _
Crofton, Horne and Miller scoring > 7 9 9 8 10 8 7 8 9 9 8

may indicate that low hemoglobin has higher risk for 
pneumonia than bronchiolitis. Table 5 reveals that among 
pneumomia cases 86% were anemic whereas only 50% 
cases were anemic among bronchiolitis cases.There 
was no specifi c golden criterion to differentiate bacterial 
(pneumonia) or viral (bronchiolitis) ALRTI but ill looking 
child, CRP positive,neutrophilic leukocytosis,blood 
culture positive was considred bacterial infection and 
viral infection were assessed clinically and leucopenia 
was considered. Literature related to this fi nding was 
not available. It was observed that 20(50%) children 
with hyperinfl ated lung fi elds had a history of wheeze 
and 10 ( 25%) gave a positive family history of asthma.
This maybe due to the fact that bronchiolitis is more 
prone to occur if there is a genetic predisposition or has 
a history of Atopy rather than low hemoglobin. These 
population was not excluded from the study as they had 
features of secondary infection clinically with high fever, 
ill looking, not feeding well and biochemically with either 
neutrophilic leukocytosis or CRP positive. Blood culture 
showed growth in only 10 % of cases and klebsiella was 
most common (4.2%) organism isolated. In this study 
Hb ≤ 10gm/dl was considered anemia (Normal Hb = 



-6-January-June, 2010/Vol 30/Issue 1 Journal of Nepal Paediatric Society

<2mo 9-14gm/dl and > 2months -11.5 – 15.5gm/dl)3.
Mean Hb level in this study was 9.58 gm% for cases 
&12gm% for Control group. Ramakrishnan K, Harish 
PS in their study found that anemic children were 5.75 
times more susceptible to LRTI7 which was 3.2 times 
in this study. Several risk factors for developing ALRTI 
had been reported in different studies. Baskaran et al8 in 
their study in children between 3-5 years had found 83% 
with pneumonia had hemoglobin less than 11 g/dL. In 
this study microcytic and hypochromic picture was seen 
in maximum children (82.3%). In another study of iron 
defi ciency anemia and respiratory infection by De-Silva 
A et al9, an over all prevalence of anemia was found in 
52.6%. The role of low hemoglobin level per se, as a 
risk factor for developing ALRTI are reported only in few 
literatures7. They had found that reduced hemoglobin 
level due to whatever etiology was a signifi cant risk 
factor for developing ALRTI. Unlike those studies here 
it was found that low hemoglobin due to Iron defi ciency 
anemia was the main cause for ALRTI. Iron defi ciency 
anemia was detected based on low MCV(normal=76-88 
fl ), low MCH(Normal=24-30 pg ), low MCHC(Normal=30-
36gm/dl), low S.Iron [Normal=infants 100-400 μg/dL 
and above Infancy 250-400 μg/dL] and increased TIBC[ 
Normal =all age=22-184 μg/dL]. Serum ferritin level was 
not done due to unavailability of this test and ferritin 
level is not reliable in cases with infection as it increases 
probably as acute phase protein10. If you look at the 
normal function of Hemoglobin it facilitates oxygen 
(O2) and carbon dioxide (CO2) transport. It caries and 
inactivates nitric oxide (NO) and also play the role of a 
buffer11. Hemoglobin in the blood is mainly responsible 
for stabilizing the oxygen pressure in the tissues 12. 
Therefore quantitative and/or qualitative reduction in 
Hb, may adversely affect the normal functions. Iron 
is principally required for haemoglobin synthesis.13 
Intestinal iron absorption is related to erythropoietic 
requirements, although the regulatory mechanism(s) 

remain unknown. The usual source of iron in the 
lung is serum iron which is derived from catabolised 
erythrocytes and absorbed iron13. Probably it may be 
the reason for low hemoglobin level found to be as a 
serious risk factor for developing ALRTI. Further studies 
including other risk factors like low birth weight, lack of 
breast feeding, severe malnutrition, smoke, cooking fuel 
etc along with low hemoglobin should be considred as 
future perspective.

Conclusion

To conclude Hb was a risk factor for LRTI (p<0.001). 
Iron defi ciency anemia was the main cause detected. 
Anemia was responsible for pneumonia more than 
bronchilitis.Iron supplementation in age group 1month to 
5 years may reduce the incidence of LRTI and prevention 

of anemia, due to whatever etiology is also essential. 
The limitation of this study is that other variables 
were not considered in this study. It is diffi cult to correlate 
the one point prevalence of pneumonia with anaemia as 
the control group could present with pneumonia within 
another few months. Only way to see is to follow a group 
of children with normal and low haemoglobin over a 
period of time for an episode of pneumonia.

Acknowledgements: We thank all the children who had 
participated in this study. A special thanks to Dr. Praveen 
shrestha who had helped with data collecton.

Funding: None

Confl ict of Interest: None

References

1. DeMaeyer EH, Adiels - Tegman M. The prevalence 
of anemia in the world. World Health Statistics 
1985, 38, 302-316.

2. Wald ER. Recurrent and non Resolving Pneumonia 
in 20 children. Sem Resp Infect 1993; 8: 46-58.

3. Michael A.Pesce. Reference Ranges for Laboratory 
Tests and procedures. In Richard E. Behrman, 
Robert Kleigman, Hal B Jenson, ed. Nelson Text 
Book of Pediatrics. 18th ed. Philadelphia; Saunders, 
2008: 2944.

4. Forfar & Arneil. Text Book of Pediatrrics 5th Edition 
1998; Campbell A.G.M. & McIntosh N, BPC 
Wheatons Ltd; Exeter; 1939.

5. Rasmussen Z,Pio A, Enarson P. Case Management 
of Childhood Pneumonia in Developing Countries: 
Relevant Research and Current Initiatives. Int J 
Tuber Lung Dis 2000:4;807-827

6. Behrman S. Epidemiology of Acute Respiratory 
Infection in Children of Developing Countries. Rev 
Infect Dis 1991: (suppl): S454-S462. 

7. Ramakrishnan K, Harish PS. Hemoglobin Level as 
a Risk Factor for Lower Respiratory Tract Infections. 
Indian J Pediatr. 2006:73:10:881-883.

8. Bhaskaran P, Madhavan Nair K, Balakrishnan 
N. Serum transferrin receptors in children  with 
respiratory infections. Eur J  Nutr. 2003; 57: 75-80.

9. De-Silva A, Atukorola S, Weerasinghel. Iron 
supplementation improves iron status and reduces  
morbidity in childrenwith or with out URTI. Am J 
Clin Nutr 2003; 77: 234-241.



-7-Journal of Nepal Paediatric Society January-June, 2010/Vol 30/Issue 1

10. Ryan TP, Krzesicki RF, Blakeman DP, et al. 
Pulmonary Ferritin: Differential Effects of Hyperoxic 
Lung Injury on Subunit mRNA Levels. Free Radic 
Biol Med 1997;22:901-908

11. William F Ganong. Gas transport between the  lungs 
and the tissues. Review of Medical   Physiology. 
22nd ed. New York; Mc Graw-Hill, 2005: 666-669

12. Guyton & Hall. Effect of hemoglobin to ‘Buffer’ the 
tissue PO2. Text Book of Medical   Physiology. 11th 
ed. Philadelphia; Saunders, 2006: 507-508.  

13. Fernando Mateos, Jeremy H Brock, José Luis 
Pérez-Arellanoa. Iron metabolism in the Lower 
Respiratory Tract. Thorax. 1998; 53:594-600.


