Effects of indoor air pollution on respiratory symptoms of non-smoking women in Niš, Serbia
© Novamedia srl 2011
Received: 17 February 2011
Accepted: 30 August 2011
Published: 10 December 2011
The aim of this study was to determine the effects of indoor air pollution exposure on respiratory symptoms and illnesses in non-smoking women in Niš, Serbia.
Materials and methods
The study was carried out in 1,082 never-smoking females, aged 20-40 years, who were not occupationally exposed to indoor air pollution. The prevalence of respiratory symptoms and illnesses was assessed using the American Thoracic Society questionnaires. Multivariate methods were used in the analysis.
A strong association was found between respiratory symptoms and indoor air pollution. The associations between home dampness and sinusitis and bronchitis were also found to be statistically significant.
Indoor air pollution exposure is an important risk factor for respiratory symptoms and illnesses in non-smoking women in Niš, Serbia.
KeywordsIndoor air pollution non-smoking women respiratory symptoms
Effetti dell'inquinamento nell’aria di ambienti confinati sui sintomi respiratori di donne non fumatrici residenti a Niš, Serbia
Scopo di questo studio era determinare gli effetti dell'esposizione ad inquinamento nell'aria di ambienti confinati sui sintomi respiratori e in termini patologici nelle donne non fumatrici di Niš, Serbia.
Materiali e metodi
Lo studio è stato condotto su 1.082 donne che non hanno mai fumato, di 20-40 anni di età, non esposte sul luogo di lavoro ad inquinamento aereo indoor. La prevalenza di sintomi respiratori e di patologie è stata valutata con i questionari dell’American Thoracic Society. Per l'analisi si è ricorsi a metodiche multivariate.
È stata riscontrata una forte associazione tra sintomi respiratori ed inquinamento ambientale indoor. L'associazione tra umidità domestica, sinusiti e bronchiti è stata a sua volta individuata come statisticamente significativa.
L'esposizione ad inquinamento ambientale in ambienti confinati è un fattore di rischio rilevante per disturbi respiratori e per patologie nelle donne non fumatrici di Niš, Serbia.
KeywordsIndoor air pollution non-smoking women respiratory symptoms
Parole chiaveDonne non fumatrici inquinamento aereo indoor sintomi respiratori
Sources of indoor air pollution can exist in any home, with constant or periodical emission of pollutants. The pollutants that are emitted are different from outdoor pollutants in terms of their concentration, which can be sometimes significantly higher . There are many different types of pollutants which may given rise to combined effects. The main factors related to indoor air pollution are chemicals for intended use or unintentional emissions from different sources, particles, microbes, pets, humidity, ventilation, temperature.
The presence of indoor pollutants, even at low concentrations, may have an important biological impact on account of long exposure periods . In developing countries, it is typical for individuals to be exposed to very high levels of pollution for 3-7 hours each day over many years .
Exposure to hazardous pollutants may have an immediate or a long-term effect, which may not become manifest for many years. The significance of the exposure depends upon the source, how much is emitted from the source, how harmful the pollutant is, and how much has accumulated within the home .
The respiratory system is the primary target of indoor air pollutants' effects because most frequently they enter the human organism through inhalation. Air pollution-related diseases are the most important cause of respiratory morbidity and mortality in adults. There are also indications that these effects are higher for sensitive groups of the population, such as children, women and persons with chronic diseases . Respiratory health effects, such as infections and asthma, are the illnesses most closely associated with increased absenteeism from work.
Several studies have investigated the effects of indoor air pollution on the health of infants and children [6–8]. In this study, we examined the effects of indoor air pollutants on the prevalence of respiratory symptoms and illnesses in non-smoking women.
Materials and methods
The study was conducted in the city of Niš, situated in the South of Serbia. In 2008 Niš had a population of 381,757 inhabitants in an area of 596,71 km2.
We evaluated data from a sample of 1,082 never-smoking women, aged 20-40 years, living in a part of the town with low concentrations of outdoor air pollutants and who were not professionally exposed to air pollution. They had lived for at least five years in this location, at a distance of 15 km from the sampling site. The participants of this study were recruited during a medical check up at the Health Care Center of Niš.
Respiratory symptoms and illnesses
The study was carried out between March and September 2008. Details of the women's prevalence of respiratory symptoms (cough, phlegm, blocked/runny nose, wheezing and shortness of breath) in the last 12-month period and of the lifetime prevalence of respiratory illnesses (e.g. asthma, allergic rhinitis, sinusitis, pneumonia and bronchitis, as diagnosed by their doctors) were obtained through questionnaires. Trained physicians filled out the questionnaires during an interview with the women. The questionnaire was adapted from the American Thoracic Society questionnaires validated for Serbian language . Respiratory symptoms were defined based on yes/no responses to the symptoms questions in the questionnaire. The questions about respiratory symptoms were as follows: Have you had daily coughs for > 3 weeks in the last 12 months? Have you had phlegm in your nose or throat in the last 12 months when you did not have flu? Have you had wheezing in your chest in the last 12 months when you did not have flu? Have you ever had attacks of shortness of breath in the last 12 months? In the past 12 months, have you had a problem with a runny or a blocked nose when you did not have flu?
Our questionnaire also included items about socio-economic status, indoor environmental determinants (e.g. environmental tobacco smoke [ETS] at home, use of biomass fuels, home dampness and the keeping of pets) and family history of respiratory illnesses.
Outdoor air pollutants
Concentrations of outdoor air pollutants (sulfur dioxide and black smoke) were measured for 24 hours/day in the women's living area during the period 2004-2008. The sampling protocol was carried out by well trained personnel. Laboratory examination of sulfur dioxide (SO2) and black smoke was performed according to the Regulation of Guideline Values of Immission (Official Register Republic of Serbia 54/92). Concentrations of SO2 were analyzed by spectrophotometry, while concentrations of black smoke (BS) were analyzed by reflectometry. For all pollutants annual averages were calculated.
Multiple logistic regression analyses were performed to analyse the relationship between respiratory symptoms and disease and exposure to different sources of indoor air pollution. Potential confounding factors such as age, education, family history of respiratory illnesses and annual average of SO2 and black smoke were adjusted for. Results are presented as adjusted odds ratios (OR) with 95% confidence intervals (CI).
Description of the study population, all women (N = 1,082)
N (%) of women
Shortness of breath
Doctor-diagnosed allergic rhinitis
ETS at home
Use of biomass fuels
Keeping of pets
< 12 grades
> 12 grades
Family history of respiratory illnesses
Arithmetic mean concentrations of sulfur dioxide and black smoke in women's living area, 2004-2008
Mean concentrations (μg/m3)
5-year mean concentrations (μg/m3)
Higher concentrations were found in areas with high population and traffic density such as Amsterdam and Berlin (45-50 μg/m3) and central European cities such as Budapest (57 μg/m3), and even higher concentrations occurred in southern European cities such as Pisa (61 μg/m3) and Athens (98 μg/m3) .
Multiple logistic regression analysis of associations between symptoms in non-smoking women and exposure to indoor air pollution
Shortness of breath
ETS at home
Use of biomass fuels
Keeping of pets
Multiple logistic regression analysis of associations between illnesses in non-smoking women and exposure to indoor air pollution
ETS at home
Use of biomass fuels
Keeping of pets
The available evidence on toxicity, indoor concentrations and number of people exposed suggests that some indoor air pollutants may constitute a significant public health problem, in particular a high prevalence of respiratory symptoms and illnesses. The respiratory system has various defense mechanisms which may alleviate air pollutants' effects, since the respiratory system is the primary place where the negative influence of air pollutants is most clearly seen.
In carrying out this study on the influence of indoor air pollution on the appearance of respiratory symptoms and diseases, we focused on the research of the five most important factors of indoor air pollution - ETS at home, use of biomass fuels, home dampness, home heating and keeping of pets. Gender differences in the effects of environmental factors may be related to personal habits, the occupational environment and the home environment. Women have been found to be more susceptible than men to environmental factors [11–13].
The results of this investigation show that exposure to ETS at home, use of biomass fuels, and home dampness represent increasing factors for the prevalence of respiratory symptoms and illnesses.
Environmental tobacco smoke (ETS) is a major source of indoor air contaminants. We did not find that ETS exposure was a significant risk factor for the presence of asthma in non-smoking women (OR 0). One reason for this may be the underestimation of diagnosis of asthma by doctors. Most studies carried out around the world have demonstrated a connection between ETS exposure and the appearance of asthma [14–17]. Climatic changes and exposure to urban air pollution can affect the appearance of asthma, too [18, 19]. However, there are studies that did not show such a connection [20, 21]. One study from Singapore  confirmed the risk of asthma among non-smoking adult women residing with heavy smokers (OR 1.6; 95% CI 0.69-3.79). We also studied respiratory symptoms in relation to ETS exposure and found a significantly higher prevalence of common respiratory symptoms like breathlessness and cough among the ETS exposed individuals. Increased prevalence of respiratory symptoms has been reported in several recent studies among non-smoking women adults [23–25]. Smoke from household solid fuels is a complex mixture which contains many potentially relevant components from a toxicological point of view. According to our results, exposure to the smoke which is released by the combustion of wood and coal affects the appearance of cough and breathlessness. Air pollution due to the use of biomass fuel has been shown to be associated with chronic obstructive lung disease (COPD), especially in females [26–29]. Ekici et al.  compared the presence of chronic airway diseases (CAD) in two groups of nonsmoking women older than 40 years with (exposed group) and without (control group) a history of exposure to biomass cooking. The prevalence of CAD in the exposed group was found to be higher than that in the control group [28.5% vs. 13.6%, crude ORs 2.5 (1.5-4.0), p = 0.0001]. Kiraz et al.  found that rural women exposed to biomass fumes are more likely to suffer from chronic bronchitis (CB) and COPD than urban women even though the prevalence of smoking is higher among the latter group. In a cross-sectional study in Mid-Anatolia , pulmonary function measurements of 112 cow-dung users and 153 modern energy source users, all non-smokers, were assessed and compared. For all pulmonary function test parameters [forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC), FEV1/FVC, and forced expiratory flow (FEF(25-75))] a highly significant (p < 0.0001) reduction of the values was observed in biomass users.
Biological agents in indoor air are known to cause three types of human diseases: infections, hypersensitivity diseases and toxic diseases. In addition, exposure to conditions conducive to biological contamination (e.g. dampness) has been related to upper and lower respiratory symptoms. Several studies have shown that home dampness is a significant predictor of respiratory symptoms [33–35]. Fisk et al.  reported the results of a quantitative meta-analysis of the studies reviewed in the US Institute of Medicine (IOM) report plus other related studies. The resulting summary estimates of ORs from random effects models based on all studies ranged from 1.38 to 1.50, with 95% CIs excluding the null in all cases. Based on the results of this meta-analysis, building dampness and mold are associated with approximately 30-50% increases in a variety of respiratory and asthma-related health outcomes. The effects of pet-keeping on life varied according to pet type, allergic sensitivity of an individual and greater environmental exposure to allergen. Biological agents in pets did not have any impact on non-smoking women's health in our investigation. Results of other studies show that dogs and cats have the strongest impact on health. In our case most of the women kept birds. It was probably the reason for the discrepancy in results.
There is a clear need for more studies on indoor pollution and health in adults, and especially in women. Future studies should address both short-term and long-term health effects related to indoor air pollutants. In conclusion, the current results in non smoking women emphasize the importance of good indoor air quality for the maintenance of health.
Conflict of interest statement
None of the authors has any conflict of interest to declare in relation to the subject matter of this manuscript.
This study was published thanks to the Ministry of Science and Technological Development of the Republic of Serbia (Project no. 42008 and project no. 43014).
- Brooks BO, Utter GM, DeBroy JA, Schimke RD: Indoor air pollution: an edifice complex. J Toxicol Clin Toxicol. 1991, 29: 315-374. 10.3109/15563659109000363.View ArticlePubMedGoogle Scholar
- Simoni M, Biavati P, Carrozzi L, Viegi G, Paoletti P, Matteucci G, Ziliani GL, Ioannilli E, Sapigni T: The Po river delta (North Italy) indoor epidemiological study: home characteristics, indoor pollutants, and subjects' daily activity pattern. Indoor Air. 1998, 8: 70-79. 10.1111/j.1600-0668.1998.t01-2-00002.x.View ArticleGoogle Scholar
- Bruce N, Perez-Padilla R, Albalak R: Indoor air pollution in developing countries: a major environmental and public health challenge. Bull World Health Organ. 2000, 78: 1078-1092.PubMed CentralPubMedGoogle Scholar
- WHO: Assessment of exposure to indoor air pollutants. Edited by: Jantunen M, Jaakkola JJK, Krzyzanowski M. 1997, WHO Regional Publications, European Series, No. 78Google Scholar
- IPCS 1993: Principles for evaluating chemical effects on the aged population. Environmental Health Criteria 144. 1993, WHO, GenevaGoogle Scholar
- Ahluwalia SK, Matsui EC: The indoor environment and its effects on childhood asthma. Curr Opin Allergy Clin Immunol. 2011, 11: 137-143. 10.1097/ACI.0b013e3283445921.View ArticlePubMedGoogle Scholar
- Heinrich J: Influence of indoor factors in dwellings on the development of childhood asthma. Int J Hyg Environ Health. 2011, 214: 1-25. 10.1016/j.ijheh.2010.08.009.View ArticlePubMedGoogle Scholar
- Jaakkola JJ, Jaakkola MS: Effects of environmental tobacco smoke on the respiratory health of children. Scand J Work Environ Health. 2002, 28 (Suppl 2): 71-83.PubMedGoogle Scholar
- Ferris BG: Epidemiology Standardization Project (American Thoracic Society). Am Rev Respir Dis. 1978, 118: 1-120.PubMedGoogle Scholar
- WHO: Air quality guidelines for particulate matter, ozone, nitrogen dioxide and sulfur dioxide - Global update. Summary of risk assessment. 2005Google Scholar
- Curtis L, Rea W, Smith-Willis P, Fenyves E, Pan Y: Adverse health effects of outdoor air pollutants. Environ Int. 2006, 32: 815-830. 10.1016/j.envint.2006.03.012.View ArticlePubMedGoogle Scholar
- Cohen AJ, Ross Anderson H, Ostro B, Pandey KD, Krzyzanowski M, Künzli N, Gutschmidt K, Pope A, Romieu I, Samet JM, Smith K: The global burden of disease due to outdoor air pollution. J Toxicol Environ Health. 2005, 68: 1301-1307. 10.1080/15287390590936166.View ArticleGoogle Scholar
- Bernstein JA, Alexis N, Barnes C, Bernstein IL, Bernstein JA, Nel A, Peden D, Diaz-Sanchez D, Tarlo SM, Williams PB: Health effects of air pollution. J Allergy Clin Immunol. 2004, 114: 1116-1123. 10.1016/j.jaci.2004.08.030.View ArticlePubMedGoogle Scholar
- Jaakkola MS, Jaakkola JJK: Effects of environmental tobacco smoke on the respiratory health of adults. Scand J Work Environ Health. 2002, 28 (Suppl 2): 52-70.PubMedGoogle Scholar
- Jaakkola MS, Piipari R, Jaakkola N, Jaakkola JJ: Environmental tobacco smoke and adult-onset asthma: a population-based incident case-control study. Am J Public Health. 2003, 93: 2055-2060. 10.2105/AJPH.93.12.2055.PubMed CentralView ArticlePubMedGoogle Scholar
- Jaakkola N, Jaakkola MS, Gissler M, Jaakkola JJ: Smoking during pregnancy in Finland: determinants and trends, 1987-1997. Am J Public Health. 2001, 91: 284-286.PubMed CentralView ArticlePubMedGoogle Scholar
- Barış SA, Yıldız F, Başyiğit I, Boyacı H, Ilgazlı A: Prevalence of smoking and chronic obstructive pulmonary disease amongst teachers working in Kocaeli, Turkey. Multidiscip Resp Med. 2011, 6: 92-96.View ArticleGoogle Scholar
- Annesi-Maesano I: Does urban asthma exist? How climatic changes and urban air pollution intervene on asthma and respiratory allergy. Multidiscip Resp Med. 2011, 6: 10-13.View ArticleGoogle Scholar
- D'Amato G: Effects of climatic changes and urban air pollution on the rising trends of respiratory allergy and asthma. Multidiscip Resp Med. 2011, 6: 28-37.View ArticleGoogle Scholar
- Kronqvist M, Johansson E, Pershagen G, Johansson SG, van Hage-Hamsten M: Risk factors associated with asthma and rhinoconjunctivitis among Swedish farmers. Allergy. 1999, 54: 1142-1149. 10.1034/j.1398-9995.1999.00115.x.View ArticlePubMedGoogle Scholar
- Janson C, Chinn S, Jarvis D, Zock JP, Torén K, Burney P, European Community Respiratory Health Survey: Effect of passive smoking on respiratory symptoms, bronchial responsiveness, lung function, and total serum IgE in the European Community Respiratory Health Survey: a cross-sectional study. Lancet. 2001, 358: 2103-2109. 10.1016/S0140-6736(01)07214-2.View ArticlePubMedGoogle Scholar
- Ng TP, Hui KP, Tan WC: Respiratory symptoms and lung function effects of domestic exposure to tobacco smoke and cooking by gas in non-smoking women in Singapore. J Epidemiol Community Health. 1993, 47: 454-458. 10.1136/jech.47.6.454.PubMed CentralView ArticlePubMedGoogle Scholar
- Larsson ML, Loit HM, Meren M, Pölluste J, Magnusson A, Larsson K, Lundbãck B: Passive smoking and respiratory symptoms in the FinEsS Study. Eur Respir J. 2003, 21: 672-676. 10.1183/09031936.03.00033702.View ArticlePubMedGoogle Scholar
- Radon K, Büsching K, Heinrich J, Wichmann HE, Jörres RA, Magnussen H, Nowak D: Passive smoking exposure: a risk factor for chronic bronchitis and asthma in adults?. Chest. 2002, 122: 1086-1090. 10.1378/chest.122.3.1086.View ArticlePubMedGoogle Scholar
- Rushton L: Health impact of environmental tobacco smoke in the home. Rev Environ Health. 2004, 19: 291-309.PubMedGoogle Scholar
- Romieu I, Riojas-Rodríguez H, Marrón-Mares AT, Schilmann A, Perez-Padilla R, Masera O: Improved biomass stove intervention in rural Mexico: impact on the respiratory health of women. Am J Respir Crit Care Med. 2009, 180: 649-656. 10.1164/rccm.200810-1556OC.View ArticlePubMedGoogle Scholar
- Naeher LP, Brauer M, Lipsett M, Zelikoff JT, Simpson CD, Koenig JQ, Smith KR: Woodsmoke health effects: a review. Inhal Toxicol. 2007, 19: 67-106.View ArticlePubMedGoogle Scholar
- Regalado J, Pérez-Padilla R, Sansores R, Páramo-Ramirez JI, Brauer M, Paré P, Vedal S: The effect of biomass burning on respiratory symptoms and lung function in rural Mexican women. Am J Respir Crit Care Med. 2006, 174: 901-905. 10.1164/rccm.200503-479OC.View ArticlePubMedGoogle Scholar
- Torres-Duque C, Maldonado D, Pérez-Padilla R, Ezzati M, Viegi G: Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure. Biomass fuels and respiratory diseases: a review of the evidence. Proc Am Thorac Soc. 2008, 5: 577-590. 10.1513/pats.200707-100RP.View ArticlePubMedGoogle Scholar
- Ekici A, Ekici M, Kurtipek E, Akin A, Arslan M, Kara T, Apaydin Z, Demir S: Obstructive airway diseases in women exposed to biomass smoke. Environ Res. 2005, 99: 93-98. 10.1016/j.envres.2005.01.004.View ArticlePubMedGoogle Scholar
- Kiraz K, Kart L, Demir R, Oymak S, Gulmez I, Unalacak M, Ozesmi M: Chronic pulmonary disease in rural women exposed to biomass fumes. Clin Invest Med. 2003, 26: 243-248.PubMedGoogle Scholar
- Sümer H, Turaçlar UT, Onarlioğlu T, Ozdemir L, Zwahlen M: The association of biomass fuel combustion on pulmonary function tests in the adult population of Mid-Anatolia. Soz Praventivmed. 2004, 49: 247-253.View ArticlePubMedGoogle Scholar
- Bornehag CG, Sundell J, Bonini S, Custovic A, Malmberg P, Skerfving S, Sigsgaard T, Verhoeff A, EUROEXPO: Dampness in buildings as a risk factor for health effects, EUROEXPO: a multidisciplinary review of the literature (1998-2000) on dampness and mite exposure in buildings and health effects. Indoor Air. 2004, 14: 243-257. 10.1111/j.1600-0668.2004.00240.x.View ArticlePubMedGoogle Scholar
- Bornehag CG, Blomquist G, Gyntelberg F, Järvholm B, Malmberg P, Nordvall L, Nielsen A, Pershagen G, Sundell J: Dampness in buildings and health. Nordic interdisciplinary review of the scientific evidence on associations between exposure to "dampness" in buildings and health effects (NORDDAMP). Indoor Air. 2001, 11: 72-86. 10.1034/j.1600-0668.2001.110202.x.View ArticlePubMedGoogle Scholar
- IOM, Institute of Medicine, National Academies of Science: Damp Indoor Spaces and Health. 2004, The National Academies Press: Washington D.C.Google Scholar
- Fisk WJ, Lei-Gomez Q, Mendell MJ: Meta-analyses of the associations of respiratory health effects with dampness and mold in homes. Indoor Air. 2007, 17: 284-296. 10.1111/j.1600-0668.2007.00475.x.View ArticlePubMedGoogle Scholar