Indian Pediatrics 2001; 38: 1361-1369  

Risk Factors for Severe Acute Lower Respiratory Tract Infection in Under-Five Children

S. Broor+, R.M. Pandey*, M. Ghosh, R.S. Maitreyi+, Rakesh Lodha, Tanu Singhal and S.K. Kabra

From the Department of Pediatrics, *Biostatistics and +Microbiology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110 029, India.

Correspondence to: Dr. S.K. Kabra, Additional Professor, Department of Pediatrics, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110 029, India. E-mail: skkabra@ hotmail.com

Manuscript received: May 2, 2001, Initial review completed: June 13, 2001,
Revision accepted: August 22, 2001.

Background: Acute lower respiratory infection (ALRTI) is the leading cause of death in children below five years of age. Identification of modifiable risk factors of severe ALRTI may help in reducing the burden of disease. Methods: A hospital based case control study was undertaken to determine risk factors associated with severe lower respiratory tract infection (LRTI) in under-five children. A case definition of severe ALRTI as given by World Health Organization (WHO) was used for cases. Healthy children attending Pediatrics out patient department for immunization during study period were enrolled as controls. Details of potential risk factors in cases and controls were recorded in pre-designed proforma. Results: 512 children including 201 cases and 311 controls were enrolled in the study. On stepwise logistic regression analysis it was found that lack of breastfeeding (OR: 1.64; 95% CI: 1.23–2.17); upper respiratory infection in mother (OR: 6.53; 95% CI: 2.73–15.63); upper respiratory infection in siblings (OR: 24; 95% CI: 7.8–74.4); severe malnutrition (OR: 1.85; 95% CI: 1.14–3.0); cooking fuel other than liquid petroleum gas (OR: 2.5; 95% CI: 1.51–4.16); inappropriate immunization for age (OR: 2.85; 95% CI 1.59–5.0) and history of LRTI in the family (OR 5.15, 95% CI 3.0–8.8) were the significant contributors of ALRTI in children under five years. Sex of the child, age of the parents, education of the parents, number of children at home, anemia, inadequate caloric intake, type of housing were not documented to be significant risk factors of ALRTI. Conclusion: Lack of breast-feeding, upper respiratory infection in mother, upper respiratory infection in siblings, severe malnutrition, cooking fuel other than liquid petroleum gas, inappropriate immunization for age and history of LRTI in the family were the significant risk factors associated with ALRTI.

Key words: Breastfeeding, Malnutrition, Passive smoking, Pneumonia.

ACUTE lower respiratory tract infection (ALRTI) is a leading cause of mortality in children below five years of age in the developing countries(1). Behrman in a review of epidemiology of ALRTI in developing countries identified low birth weight, malnutrition, vitamin A deficiency, lack of breastfeeding and passive smoking as risk factors for ALRTI(2). Recent studies have added other risk factors to the list including poor socioeconomic status, large family size, family history of bronchitis, advanced birth order, crowding, young age, air pollution, and the use of non-allopathic treatment in early stages of illness(3-13). More recent reviews suggest that indoor air pollution is one of the major risk factor for acute lower respiratory tract infection in children in developing countries(14-15). Many of the factors mentioned are amenable to corrective measures and may help in reducing the alarmingly high global burden of ALRTI. We, therefore, undertook this study to identify the risk factors for ALRTI in hospitalized children in North India.

The study was carried out from March 1995 to February 1997 in the Pediatric wards of our hospital which is a tertiary care hospital situated in Northern India. Children admitted with severe acute lower resiratory tract infection (ALRTI) in the absence of under-lying chronic illnesses during the study period were enrolled in the study as cases.

Acute respiratory tract infection was defined as presence of cough with or without fever for less than two weeks. Severe ALRTI was defined as presence of lower chest in-drawing with respiratory rates of more than 60 per minute in an infant less than 2 months, more than 50 per minute in infants between age group 3-12 months and more than 40 per minutes in children between 13-60 months of age(16). Controls included in the study were healthy children below 5 years of age attending Pediatric out-patient department during the study period for immunization.

For both cases and controls, clinical review including history and physical examination, was undertaken to elicit various potential risk factors and these were recorded in a pre-designed proforma. Age of the child was recorded in completed months and the age of mother and father were recorded in completed years. Education of mother and father was recorded in completed years of formal education. If a mother or father of the child were not able to read or write they were labeled as illiterate. For analysis, ages of the mother, father and child were converted to categorical variables (mother as £ 25 years and > 25 years, father £30 years and >30 years, children £1 year and >1 year). History of immunization was elicited from parents and verified by checking the written document wherever available. A child was assessed to be completely immunized if he/she had received all vaccinations due for his age according to national immunization schedule(17).

History of smoking by various members in the family and details of cooking fuel used was recorded. A history of upper respiratory infection in mother, father, sibs or grand parents in preceding two weeks and a history of pneumonia/bronchitis in any family member was elicited. Information on the type of house (thatched or cemented) was recorded.

History of breastfeeding and the age of introduction of supplementary feeding was elicited. Caloric intake of the child was calculated by recording the food items given to the child regularly prior to the current illness by recall. Child was examined for pallor and graded as suffering from severe anemia if the color of palmer creases was similar to the rest of the palm(18). Length of the child was measured on an infantometer to the nearest centimeter till the age of two years and thereafter height on a stadiometer. Weight of the child was recorded on beam type of weighing scale to the nearest 100 g. For assessment of severity of malnutrition an age independent criteria in form of ratio of weight in kilograms multiplied by 100 and length or height in cm2 was calculated. The ratio of more than 0.14 was considered as normal or mild malnutrition while a ratio of less than or equal to 0.14 was considered as severe malnutrition(19).

Data was recorded on a pre-designed proforma and managed on Excel spread sheet. All the entries were double checked for any possible key-board error. Association of each of the categorical variable with severe acute lower respiratory tract infection (outcome variables) was assessed with chi-square test and the strength of their association was computed by unadjusted odds ratio (95% confidence interval). Variables showing statistically significant association with the outcome variables upto p = 0.2 were consi-dered as potential risk factors of severe acute lower respiratory tract infection. Subse-quently, these variables were simultaneously subjected to stepwise multiple logistic regression model to determine the significant independent risk factor of severe ALRTI. Data analysis was performed using STATA 6.0 Intercooled version (STATA Corp. Houston, Texas, USA). In this study p value less than 0.05 was considered as statistically significant.

In this study majority of children (62.5% in cases and 66.9% in controls) were infants with their age distribution comparable. There were significantly more boys in cases (73.1%) as compared to controls (64.0%)(p = 0.03). Both mothers’ and fathers’ level of education was negatively associated with occurrence of severe acute lower respiratory tract infection. There were significantly higher numbers of illiterate mothers (34.8%) in ALRTI group as compared to controls (19.6%) (p <0.000). Similarly, significantly more fathers were illiterate in ALRTI group (17.4%) as com-pared to control group (6.1%). Inappropriate immunization for age was significantly positively associated with ALRTI (ALRTI: 70.2% vs control: 49.2%). URTI in both mother and siblings were significantly positively associated with ALRTI (p = 0.000). Similarly, the families having history of LRTI; and having more than two children at home, were significantly positively associated with ALRTi (Table I). Amongst the four nutritional variables considered in this study, lack of breastfeeding, malnutrition, and inadequate caloric intake were significantly associated with ALRTI (Table II). Both the environmental variables (cooking fuel used and type of home) were strongly associated with ALRTI (Table III).

When the variables showing significant association at p <0.2 were simultaneously considered in stepwise logistic regression model with ALRTI as a binary outcome it was observed that children not exclusively breast-fed for the first four months of life were 1.6 times more at risk of developing ALRTI (OR 1.6; 95% CI 1.23-2.17). The risk of ALRTI increased by six and half times (OR 6.5; 95% CI 2.73-15.61) when the mother had URTI in preceding 2 weeks and as much as 24 times (OR: 24; 95% CI 7.8-74.4) when the sib of the child had URTI in preceding 2 weeks. Children with severe malnutrition were at a 1.85 times (OR 1.85; 95% CI 1.14-3.0) greater risk of developing ALRTI as compared to children with mild malnutrition or with normal nutritional status. Use of cooking fuel other than LPG was associated with 2.5 times greater risk (OR 2.5; 95% CI 1.51-4.16) of ALRTI. Incomplete immunization for age was associated with 2.85 times increased risk (OR 2.85; 95% CI 1.59-5.0) of ALRTI and history of LRTI in other members of family was associated with 5.1 times (OR 5.1; 95% CI 3.0-8.8) greater risk for ALRTI (Table IV).

Use of cooking fuel other than LPG, URTI in mother or sibling in preceding two weeks, family history of LRTI, lack of breastfeeding, severe malnutrition and inadequate immu-nization emerged as independent significant risk factors for severe ALRTI in the present study.

Use of biomass fuels (wood, crop-residues, animal dung), coal and other media (kerosene) are predominant contributors to indoor air pollution. Nearly half the world’s households, more so in developing countries and the countryside (90%), use these fuels for cooking. These are burnt in simple stoves with very incomplete combustion generating a lot of toxic products that adversely affect specific and non specific local defenses of the respiratory tract(14,15). The risk is highest for mothers and young children due to longer stay indoors and close proximity during cooking. A recent review that systematically analyzed all published studies pertaining to indoor air pollution from biomass fuels concluded that there is a strong consistent increase in ALRTI in young children even after adjusting for confounders such as poverty. Provision of clean fuels, householder’s education and modification of stoves are potential measures to decrease this risk(14,15).

Environmental tobacco smoke (ETS) is another indoor pollutant that reduces local defense mechanisms and predisposes children to invasive infection(20,21). In the present study smoking by the mother, father or grand parents did not emerge as a significant risk factor in bivariate analysis. The number of mothers and grandparents who were smokers was low. The number of fathers who smoked was relatively greater in the cases as compared to controls, but the difference did not reach statistical significance. The exposure of children due to smoking by fathers may be limited because of relatively greater time spent by fathers outside the home.

History of LRTI in family was an independent risk factor for severe penumonia. We believe that this probably results from family members sharing common environ-ment that predisposed them for LRTI. The possibility of asthma/chronic bronchitis in the family members identified as LRTI cannot be ruled out as the diagnosis was based on the history. History of URTI in the mother or siblings was associated with higher risk of ALRTI in cases. Most of URTI are caused by viral infections that are highly contagious and likely to occur in many members of the family. Viral URTI may predispose a child to ALRTI(22).

Lack of exclusive breastfeeding for first four months and severe malnutrition were independent risk factors for ALRTI. Both these factors can be prevented by proper health education of mothers. Inadequate caloric intake was found to be significant factor associated with ALRTI in bivariate analysis but it was not a significant factor on multivariate analysis. Caloric intake goes down in all acute illnesses temporarily but longer duration of inadequate intake results in malnutrition. For effect of exclusive breast feeding on ALRTI, children below 4 months of age were counted with the group of children breastfed for less than 4 months even though they may be exclusively breastfed. To see the true protective effect of exclusive breast-feeding up to four months we did the entire calculations again after excluding children below 4 months of age (data not shown). The final results were not altered. It is important to note that exclusive breastfeeding for first 4 months of life not only protect against severe ALRTI but also protects from development of asthma and other allergic disorders(23,24).

For assessment of malnutrition we used weight/length2 as pediatricians are familiar with it. We also calculated weight for height ‘z’ scores for cases and controls. The result of this analysis also showed malnutrition as a significant risk factor (OR 2.6; 95% CI 1.25-5.4; p = 0.008) for ALRTI in children below 5 years of age.

We observed that children who were immunized for age were less likely to suffer from ALRTI as compared to those incom-pletely immunized. This was independent of maternal age or education. It suggests that mothers utilizing immunization services are better aware of health care facilities and probably seek early consultation for illness of their children. Awareness of mothers leading to early identification of illness probably avoids severe illness.

We conclude that indoor environmental pollution (use of cooking-fuel other than LPG) and nutritional factors (lack of breast-feeding, severe malnutrition) are modifiable major risk factors for severe pneumonia. Appropriate measures to reduce exposure of children to indoor environmental pollutants like smokes produced due to use of biomass may help to reduce severe ALRTI. Promotion of exclusive breastfeeding in first four months and appropriate nutritional supplements thereafter may help in decreasing the incidence of severe ALRTI.

Contributors: SKK was involved in designing the study, collection of data and preparation of manuscript. He will act as a guarantor of the study. SB was involved in design and writing of the manuscript. MG was involved in data collection. RMP was involved in statistical analysis and manuscript writing. RL, TS and RSM helped in drafting the manuscript.

Funding: Department of Biotechnology, Government of India.

Competing interests: None stated.

1. 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: 807-826.

2. Behrman S. Epidemiology of acute respiratory infection in children of developing countries. Rev Infect Dis 1991; (Suppl 6): S454-S462.

3. Hussey GD, Apolles P, Arendse Z, Yeates J, Robertson A, Swingler G et al. Respiratory syncytial virus infection in children hospitalized with acute lower respiratory tract infection. S Afr Med J 2000; 90: 509-512.

4. Banajeh SM. Outcome for children under 5 years hospitalized with severe acute lower respiratory tract infection in Yemen: A 5-year experience. J Trop Pediatr 1998; 44: 342-346.

5. Hamid M, Qazi SA, Khan MA. Clinical, nutritional and radiological features of pneumonia. J Pak Med Assoc 1996; 46: 95-99.

6. Shah N, Ramankutty V, Premila PG, Sathy N. Risk factors for severe pneumonia in children in south Kerala, a hospital based case control study. J Trop Pediatr 1994; 40: 201-206.

7. Suwanjuth S, Ruangkanchanasetr S, Chantarojanasiri T, Hotrakitya S. Risk factors associated with morbidity and mortality of pneumonia in Thai children under 5 years. Southeast Asian J Trop Med Public Health 1994; 25: 60-66.

8. Murtagh P, Cerqueiro C, Halac A, Avita M, Salomon H, Weissenbacher M. Acute lower respiratory infection in Argentanian children - A 40 month clinical and epidemiological study. Pediatr Pulmonology 1993; 16: 1-8.

9. Campbell H, Armstrong JR, Byass P. Indoor air pollution in developing countries and acute respiratory infection in children. Lancet 1989; 1: 1012.

10. Collings DA, Sithole SD, Martin KS. Indoor wood smoke pollution causing lower respira-tory disease in children. Trop Doctor 1990; 20: 151-155.

11. Deb SK. Acute respiratory disease survey in Tripura in case of children below five years of age. J Indian Med Assoc 1998; 96: 111-116.

12. Sharma S, Sethi GR, Rohtagi A, Chaudhary A, Shankar R, Bapna JS, et al. Indoor air quality and acute lower respiratory infection in Indian urban slums. Environ Health Perspect 1998; 106: 291-297.

13. Agrawal PB, Shendurnikar N, Shastri NJ. Host factors and pneumonia in hospitalized children. J Indian Med Assoc 1995; 93: 271-272.

14. Bruce N, Perez-Padilla R, Albalak R. Indoor air pollution in developing countries: A major environmental and public health challenge. Bull WHO 2000; 78: 1078-1092.

15. Smith KR, Sarnet JM, Romieu I, Bruce N. Indoor air pollution in developing countries and acute lower respiratory infection in children. Thorax 2000; 55: 518-532.

16. Technical Basis for WHO Recommendations on the Management of Pneumonia in Children at First Level Health Facilities. WHO/ARI/91.20 Geneva, World Health Organization, 1991.

17. Park K. Immunization schedule. Principles of epidemiology and epidemologic methods. In: Textbook of Preventive and Social Medicine. 14th edn. Ed. Park K, Jabalpur, Banarasidas Bhanot Publishers, 1991; pp 125-128.

18. Bun HF, Anemia. In: Harrisons Principles of Internal Medicine, 11th edn. Eds. Brounwald E, Isselbacher KJ, Petersdorf RG, Wilson JD, Maston JB, Fauci AS, New York, McGraw Hill Book Company, 1987; pp 262-266.

19. Rao KV, Singh D. An evaluation of the relationship between nutritional status and anthropometric measurements. Am J Clin Nutr 1970; 23: 83-93.

20. Morrow PW. Toxicological data on NO: An overview. J Toxicol Environ Health 1984; 13: 205-227.

21. Lippmann M. Effects of respiratory function and structure. Ann Rev Public Health 1989; 10: 49-67.

22. O’Brian KL, Valters ML, Selbnan J, Quinlisk H, Schwartz B, Dovell SF. Severe pneumococcal pneumonia in previously healthy children: Role of preceding influenza infection. Clin Infect Dis 2000; 30: 784-789.

23. Ratageri VH, Kabra SK, Dwivedi SN, Seth V. Factors associated with severe asthma. Indian Pediatr 2000; 37: 1072-1082.

24. Wright AL, Holberg CJ, Martinez FD, Morgan WJ, Taussing LM, Group health medical associates. Breastfeeding and lower respira-tory tract illnesses in first year of life. Br Med J 1989; 299: 946.