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on the International Union Against Tuberculosis and. Lung Disease's 1984 questionnaire was used to assess asthma and CB prevalence. Multivariate logistic ...
INT J TUBERC LUNG DIS 16(9):1270–1277 © 2012 The Union http://dx.doi.org/10.5588/ijtld.12.0005

Indian Study on Epidemiology of Asthma, Respiratory Symptoms and Chronic Bronchitis in adults (INSEARCH) S. K. Jindal,* A. N. Aggarwal,* D. Gupta,* R. Agarwal,* R. Kumar,† T. Kaur,‡ K. Chaudhry,‡ B. Shah‡ * Department of Pulmonary Medicine, and † School of Public Health, Postgraduate Institute of Medical Education and Research, Chandigarh, ‡ Division of Non-Communicable Diseases, Indian Council of Medical Research, Ansari Nagar, New Delhi, India SUMMARY

Field sites in 12 districts in different parts of

O B J E C T I V E : To determine the nationwide population prevalence of and risk factors for asthma and chronic bronchitis (CB) in adults. D E S I G N : A standardised validated questionnaire based on the International Union Against Tuberculosis and Lung Disease’s 1984 questionnaire was used to assess asthma and CB prevalence. Multivariate logistic regression analyses were performed to determine the risk factor associations. Estimates standardised to the 2011 population projection estimates for India were used to calculate the national disease burden. R E S U LT S : A total of 85 105 men and 84 470 women from 12 urban and 11 rural sites were interviewed. One

or more respiratory symptoms were present in 8.5% of individuals. The overall prevalence of asthma and CB was respectively 2.05% (adults aged ⩾15 years) and 3.49% (adults aged ⩾35 years). Advancing age, smoking, household environmental tobacco smoke exposure, asthma in a first-degree relative, and use of unclean cooking fuels were associated with increased odds of asthma and CB. The national burden of asthma and CB was estimated at respectively 17.23 and 14.84 million. C O N C L U S I O N : Asthma and CB in adults pose an enormous health care burden in India. Most of the associated risk factors are preventable. K E Y W O R D S : asthma; chronic bronchitis; tobacco smoking; solid fuel combustion; environmental tobacco smoke

CHRONIC RESPIRATORY DISEASES (CRD), primarily bronchial asthma and chronic obstructive pulmonary disease (COPD), together account for a global burden of more than 400 million patients.1–3 In India, CRDs account for 7% of deaths and a 3% loss of disability adjusted life years (DALYs).4 Data on nationwide prevalence are, however, lacking. Most of the available studies have employed different definitions and methodologies, eluding uniformity. A review of the published reports on chronic bronchitis (CB) in the last 30 years revealed prevalence varying from 1.9% to 9%.5 However, it has been difficult to extrapolate these results for the whole of India. In an earlier study conducted at four centres, we estimated the overall prevalence as 4.1%.6 A number of reports are available on the prevalence of asthma among children in India.7–11 The multicentric International Study on Asthma and Allergies in Childhood (ISAAC) provides fairly comprehensive prevalence data from different parts of the country.8,9,12 However, only a few studies have been published on the prevalence of asthma among adults.13–15 The large European Community Respiratory Health (ECRH)

survey from Mumbai, reporting the prevalence of physician-diagnosed asthma as 3.5%, was limited to only a single centre.15 These data cannot be used for the whole country due to enormous epidemiological diversity. Two earlier studies from this centre report prevalence of respectively 2.8% and 2.4% among adults.13,14 A nationwide study for the assessment of CRD burden due to asthma and COPD in India was therefore clearly necessary. The multicentric Indian Study on Epidemiology of Asthma, Respiratory Symptoms and Chronic Bronchitis (INSEARCH), employing a uniform methodology, was undertaken under the auspices of the Indian Council of Medical Research (ICMR). For this study, we used the Bronchial Symptom Questionnaire (1984) of the International Union Against Tuberculosis and Lung Disease (The Union), which we had validated earlier for the diagnosis of asthma.16 The Union questionnaire was chosen for its ease of administration in the field setting. It was not feasible to include objective tests of diagnosis due to the practical difficulties of application and standardisation.

SETTING:

India.

Correspondence to: S K Jindal, Department of Pulmonary Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India. Tel: (+91) 172 275 6821. Fax: (+91) 172 274 5959. e-mail: [email protected] Article submitted 6 January 2012. Final version accepted 4 April 2012.

Asthma and chronic bronchitis in India

Figure 1 Geographic location of the 12 participating centres and the coordinating centre (Chandigarh).

METHODS Study design A cross-sectional study was performed simultaneously (2007–2009) at 12 centres located across India (Figure 1). Ethical approval was obtained from the Institutional Ethics Committees of the coordinating centre (Chandigarh) and the other participating centres. Informed consent was obtained from each respondent at the time of the interview. We used a two-stage, stratified sampling design at each centre, considering the district as a unit. The villages/urban areas formed the first stage and the households the second stage unit in the two-stage stratification. A sample of 12 421 subjects was estimated to obtain a 95% confidence interval (CI) of ±0.3% around a prevalence estimate of 3%. Generally, 30–40 clusters were studied at each centre, with about 100 households targeted in each cluster. All individuals aged ⩾15 years residing at each selected household were interviewed. At least two additional attempts were made to contact an individual in case of non-availability on the first visit. The study questionnaire was administered by field staff, all of whom underwent structured training conducted by the coordinating centre. It generally took about a year to complete the study sample at each site. Internal quality assurance was ensured by each study site supervisor through a random repeat survey of 10% of the surveyed households. External quality assurance was carried out during periodic monitoring visits by investigators from the coordinating centre. Study questionnaire and definitions We had previously developed the study instrument by translating the Union’s English questionnaire (1984) into Hindi, testing its reliability, and validating it against physician-diagnosed asthma using a specific set of questions.13,14,16,17 The study questionnaire included the translated Union questionnaire along with items on demographic and environmental exposure

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factors (tobacco smoking, exposure to household environmental tobacco smoke [ETS], and cooking habits) likely to influence the prevalence of asthma and CB, and captured the respiratory symptoms of the 12-month period preceding the interview. The questionnaire was also translated into the regional language of each study site. The reliability of each language version was established by using test-retest and split-half method. All three (English, Hindi and regional language) versions of the questionnaire were used at each centre, depending on the language preference of the interviewee. The questionnaire diagnosis of asthma was established by affirmative responses to the validated set of questions, which consisted of at least one of the two questions on wheezing and tightness of the chest, plus one of the three questions on history of previous diagnosis of asthma, an attack of asthma and use of medication for asthma, in the past 12 months.13,14 CB was diagnosed based on a separate set of questions from the same questionnaire and on presence of cough with expectoration for ⩾3 months in a year for 2 or more consecutive years.6,18 Physician evaluation was not used to establish the diagnoses. Statistical analysis Responses to the questionnaires were stored using a customised EpiData database (http://www.epidata.dk), and analyses were carried out at the coordinating centre. Prevalence of asthma and CB were computed, and estimates standardised to the age distribution of the population as per the 2011 population estimates for India (http://nrhm-mis.nic.in/) were calculated. Group comparisons were performed using the χ2 test (for categorical variables) or Student’s t-test (for scalar variables). Univariate and multivariate logistic regression analyses were conducted to calculate odds ratios (OR) and 95%CIs to determine the relationships between potential risk factors and the presence of asthma or CB. These analyses were conducted for each centre individually as well as for the entire study population. Prevalence estimates were not analysed by language of survey. To calculate the national burden, the standardised prevalence estimates for men and women across different age groups were summated and multiplied by the projected number of individuals in each stratum. For asthma, the census data for adults aged ⩾15 years were considered. For CB, burden estimates were calculated for persons aged ⩾35 years.

RESULTS A total of 169 575 individuals were surveyed at 23 sites across 12 centres (Figure 1). These included 60 764 and 108 811 persons residing in respectively 12 urban and 11 rural locations at the time of interview. There was a high participation rate, of

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The International Journal of Tuberculosis and Lung Disease

respectively 93.5% and 98.2% for urban and rural households. Of those eligible in the surveyed households, 98.6% of urban and 97.6% of rural subjects were finally interviewed. The overall rural to urban ratio was 1.79 (range, 1.46– 4.28; Table 1). In all, 85 105 men and 84 470 women were interviewed; nearly half the study population was aged 35 years, as its presence in the younger age groups was considered as epidemiologically insignificant and as having a greater likelihood of confounding from respiratory infections. Risk factors and limitations There were higher odds of advancing age, tobacco smoking and ETS exposure for both asthma and CB. The age relationship for asthma is partly attributable to a ‘cumulative effect’ in older age groups with previously diagnosed as well as late onset asthma, when the definition of ‘ever asthma’ is considered. An overlap from cases of CB in older age cannot be altogether denied; however, this is less likely, as we used separate sets of questions for the two conditions. The higher OR with exposure to household ETS and combustion of solid fuels points to a significant role of indoor air pollutants,30,31 particularly as the widespread use of biomass fuels for domestic combustion is an important cause of chronic respiratory disease, especially among women in developing countries.31,32 An increased prevalence of chronic bronchitis and respiratory symptoms in women exposed to solid fuel combustion has been shown in earlier studies.32–34 There are some obvious limitations of the symptombased diagnosis of asthma as well as of the physician’s perception of asthma symptoms, even if a validated questionnaire is used. As an example, the percentage of responses to single questions on the reported symptoms of wheezing, use of inhalers and physician diagnosis of asthma, was higher in this study than the finding of prevalence of asthma. There are several possible reasons: 1) there are no specific terms for asthma in Indian vernacular languages (‘Dama’ is used for both asthma and COPD in Hindi and many other Indian languages); 2) general practitioners practising in small places in the peripheral regions do

not often differentiate between asthma and COPD; and 3) inhalers and bronchodilators are sometimes used/abused for non-specific symptoms of cough. It has been previously shown, in a cross-cultural international study, that definitions including questions with the term ‘asthma’ should also include other questions due to the way this term is perceived in other languages.35 We tried to minimise this difficulty by using a set of questions validated for diagnosis in our setting. Presence of confounding by a small number of patients with other respiratory morbidities, such as bronchiectasis or tuberculosis, cannot be altogether excluded. This is unlikely to influence the overall prevalence in a large sample with the different sets of questions we have chosen.

CONCLUSIONS The total population prevalence estimate of asthma and CB in adults amounted to over 32 million patients for the projected 2011 population of around 415 million. Tobacco smoking, ETS exposure and indoor air pollution due to solid fuel combustion are important risk factors, all of which are important public health concerns and are potentially preventable. Acknowledgement This study was funded by a research grant from the Indian Council of Medical Research, New Delhi, India. INSEARCH study group participating centres and investigators: R Solanki, D Patel, P K Chhaya (Ahmedabad); N Misra, M C Dash (Berhampur); V K Jain, B B Mathur, M C Gujrani, R Acharya (Bikaner); V Thanasekaraan, B W C Sathiasekaran, G Palani (Chennai); P Baruwa, C Phukan (Guwahati); D Ganguly (Kolkata); R Chowgule, V Shetye (Mumbai); B S Jayaraj, P A Mahesh (Mysore); R M Sarnaik (Nagpur); R Vijaikumar, A Sahar (Secunderabad); S K Kashyap, M Sarkar, R S Negi (Shimla); C S Ghosh, Dineshaprabhu, S Remadevi (Trivandrum).

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7 Chhabra S K, Gupta C K, Chhabra P, Rajpal S. Prevalence of bronchial asthma in school children in Delhi. J Asthma 1998; 35: 291–296. 8 Shah J R, Amdekar Y K, Mathur R S. Nationwide variation in prevalence of bronchial asthma. (Part of the International Study of Asthma and Allergies in Childhood—ISAAC). Indian J Med Sci 2000; 6: 213–220. 9 Pakhale S, Wooldrage K, Manfreda J, Anthonisen N. Prevalence of asthma symptoms in 7th and 8th-grade school children in a rural region in India. J Asthma 2008; 45: 117–122. 10 Jain A, Bhat V H, Acharya D. Prevalence of bronchial asthma in rural Indian children: a cross-sectional study from South India. Indian J Pediatr 2010; 77: 31–35. 11 Behl R K, Kashyap S, Sarkar M. Prevalence of bronchial asthma in school children of 6–13 years of age in Shimla City. Indian J Chest Dis Allied Sci 2010; 52: 145–148. 12 Lai C K, Beasley R, Crane J, Foliaki S, Shah J, Weiland S. Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 2009; 64: 476–483. 13 Jindal S K, Gupta D, Aggarwal A N, Jindal R C, Singh V. Study of the prevalence of asthma in adults in North India using a standardized field questionnaire. J Asthma 2000; 37: 345– 351. 14 Aggarwal A N, Chaudhry K, Chhabra S K, et al. Prevalence and risk factors for bronchial asthma in Indian adults: a multicentre study. Indian J Chest Dis Allied Sci 2006; 48: 13–22. 15 Chowgule R V, Shetye V M, Parmar J R, et al. Prevalence of respiratory symptoms, bronchial hyperreactivity, and asthma in a megacity. Results of the European Community Respiratory Health Survey in Mumbai (Bombay). Am J Respir Crit Care Med 1998; 158: 547–554. 16 Burney P G, Laitinen L A, Perdrizet S, et al. Validity and repeatability of the IUATLD (1984) Bronchial Symptoms Questionnaire: an international comparison. Eur Respir J 1989; 2: 940– 945. 17 Burney P, Chinn S. Developing a new questionnaire for measuring the prevalence and distribution of asthma. Chest 1987; 91(Suppl): 79S–83S. 18 Definition and classification of chronic bronchitis for clinical and epidemiological purposes. A report to the Medical Research Council by their Committee on the Aetiology of Chronic Bronchitis. Lancet 1965; 1: 775–779. 19 Buist A S, Vollmer W M, McBurnie M A. Worldwide burden of COPD in high- and low-income countries. Part I. The Burden of Obstructive Lung Disease (BOLD) Initiative. Int J Tuberc Lung Dis 2008; 12: 703–708. 20 Menezes A M, Perez-Padilla R, Jardim J R, et al. Chronic obstructive pulmonary disease in five Latin American cities (the PLATINO study): a prevalence study. Lancet 2005; 366: 1875– 1881. 21 The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Worldwide variation in preva-

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lence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. Lancet 1998; 351: 1225–1232. European Community Respiratory Health Survey. Variations in the prevalence of respiratory symptoms, self-reported asthma attacks, and use of asthma medication in the European Community Respiratory Health Survey (ECRHS). Eur Respir J 1996; 9: 687–695. Toren K, Brisman J, Jarvholm B. Asthma and asthma-like symptoms in adults assessed by questionnaires—a literature review. Chest 1993; 104: 600–608. Bai J, Peat J K, Berry G, Marks G B, Woolcock A J. Questionnaire items that predict asthma and other respiratory conditions in adults. Chest 1998; 114: 1343–1348. Parasuramalu B G, Huliraj N, Rudraprasad B M, Prashanth Kumar S P, Gangaboraiah, Ramesh Masthi N R. Prevalence of bronchial asthma and its association with smoking habits among adult population in rural area. Indian J Public Health 2010; 54: 165–168. de Marco R, Accordini S, Cerveri I, et al. Incidence of chronic obstructive pulmonary disease in a cohort of young adults according to the presence of chronic cough and phlegm. Am J Respir Crit Care Med 2007; 175: 32–39. Halbert R J, Natoli J L, Gano A, Badamgarav E, Buist A S, Mannino D M. Global burden of COPD: systematic review and meta-analysis. Eur Respir J 2006; 28: 523–532. Ko F W S, Hui D S C, Lai C K W. Worldwide burden of COPD in high- and low-income countries. Part III. Asia-Pacific studies. Int J Tuberc Lung Dis 2008; 12: 713–717. Johnson P, Balakrishnan K, Ramaswamy P, et al. Prevalence of chronic obstructive pulmonary disease in rural women of Tamilnadu: implications for refining disease burden assessments attributable to household biomass combustion. Glob Health Action 2011; 4: 7226. Baena-Cagnani C E, Gomez R M, Baena-Cagnani R, Canonica G W. Impact of environmental tobacco smoke and active tobacco smoking on the development and outcomes of asthma and rhinitis. Curr Opin Allergy Clin Immunol 2009; 9: 136– 140. Fullerton D G, Bruce N, Gordon S B. Indoor air pollution from biomass fuel smoke is a major health concern in the developing world. Trans R Soc Trop Med Hyg 2008; 102: 843–851. Liu S, Zhou Y, Wang X, Wang D, Lu J, Zheng J, Zhong N, Ran P. Biomass fuels are the probable risk factor for chronic obstructive pulmonary disease in rural South China. Thorax 2007; 62: 889–897. Viegi G, Simoni M, Scognamiglio A, et al. Indoor air pollution and airway disease. Int J Tuberc Lung Dis 2004; 8: 1401– 1415. Salvi S S, Barnes P J. Chronic obstructive pulmonary disease in non-smokers. Lancet 2009; 374: 733–743. Sunyer J, Basagana X, Burney P, Anto J M. International assessment of the internal consistency of respiratory symptoms. Am J Respir Crit Care Med 2000; 162: 930–935.

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RÉSUMÉ C O N T E X T E : Sites du terrain dans 12 districts de différentes parties de l’Inde. O B J E C T I F : Déterminer la prévalence nationale de l’asthme et de la bronchite chronique (CB) chez les adultes dans la population générale ainsi que leurs facteurs de risque. S C H É M A : On a utilisé un questionnaire standardisé validé basé sur le questionnaire de 1984 de l’Union Internationale Contre la Tuberculose et les Maladies Respiratoires afin d’évaluer la prévalence de l’asthme et de la CB. Les analyses de régression logistique multivariées ont été menées pour déterminer les associations de facteurs de risque. Pour le calcul du fardeau national des maladies, on a utilisé des estimations standardisées aux estimations projetées de la population de 2011. R É S U LTAT S : On a interviewé 85 105 hommes et 84 470

femmes provenant de 12 sites urbains et de 11 sites ruraux. Un ou plusieurs symptômes respiratoires étaient présents chez 8,5% des individus. La prévalence globale de l’asthme a été de 2,05% chez les adultes âgés de ⩾15 ans et celle de la CB de 2,49% chez les adultes âgés de ⩾35 ans. Les progrès de l’âge, le tabagisme, l’exposition à la fumée environnementale de tabac au sein du ménage, l’asthme chez un parent du premier degré et l’utilisation de carburants de cuisson malpropres sont en association avec un odds accru d’asthme et de CB. Le fardeau national de l’asthme est estimé à 17,23 par million d’habitants et celui de la CB à 14,84 par million d’habitants. C O N C L U S I O N : L’asthme et la CB constituent un fardeau énorme de soins de santé en Inde. La plupart des facteurs de risque qui y sont associés sont évitables. RESUMEN

M A R C O D E R E F E R E N C I A : Los centros de atención de 12 distritos en diferentes regiones de la India. O B J E T I V O : Se buscó determinar a escala nacional la prevalencia de asma y bronquitis crónica en la población adulta y definir los factores de riesgo de padecer estas enfermedades. M É T O D O : Con el propósito de evaluar la prevalencia de asma y bronquitis crónica se utilizó un cuestionario normalizado y validado, basado en el cuestionario propuesto por la Unión Internacional Contra la Tuberculosis y las Enfermedades Respiratorias en 1984. Un análisis de regresión logística multifactorial permitió determinar las asociaciones de los factores de riesgo. Se calculó la carga de morbilidad a escala nacional, al aplicar las estimaciones ajustadas a las proyecciones de población del 2011 en la India. R E S U LTA D O S : Se entrevistaron 85 105 hombres y 84 470

mujeres en 12 centros urbanos y 11 centros rurales. Se observó que 8,5% de las personas encuestadas presentaba uno o más síntomas respiratorios. La prevalencia global de asma fue 2,05% (adultos ⩾15 años de edad) y la prevalencia de bronquitis crónica fue 3,49% (adultos ⩾35 años de edad). La edad avanzada, el tabaquismo, la exposición al humo de tabaco ambiental en el hogar, el antecedente de asma en un familiar de primer grado y el uso de combustibles de biomasa para cocinar se asociaron con una mayor probabilidad de padecer asma y bronquitis crónica. Se calculó que a escala nacional, la carga de morbilidad por asma era de 17,23 millones y por bronquitis crónica era 14,84 millones. C O N C L U S I Ó N : El asma y la bronquitis crónica del adulto representan una carga considerable de la atención sanitaria en la India. La mayoría de los factores de riesgo asociados con estas dos enfermedades es prevenible.