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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 2  |  Issue : 1  |  Page : 39-45

Outdoor air pollution affects tuberculosis development based on geographical information system modeling


1 Mycobacteriology Research Center (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Department of Microbiology, College of Medicine, University of Kerbala, Karbala, Iraq
3 Department of Biotechnology, School of Advanced Technology in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Web Publication5-Mar-2018

Correspondence Address:
Dr. Parissa Farnia
Mycobacteriology Research Center (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/bbrj.bbrj_5_18

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  Abstract 


Background : Daily intake of air is 30 Ib as compared with 2-Ib of food and 4½ of water. Thereby, breathing-contaminated air is as harmful as drinking or eating contaminated water or food, respectively. Recent research has highlighted the extent of outdoor air pollution in large cities and warranted high-quality studies to clarify the magnitude of the problem. Here, we evaluated the possible association between tuberculosis (TB) development and exposure to outdoor air pollution in a metropolitan city of Tehran. Methods: Extraction and analysis of relevant data. Investigation performed on TB patients (n = 1167) that were residing in Tehran for the past 10 years. The average concentration of sulfur dioxide (SO2), nitrogen dioxide, carbon monoxide (CO), and particles with an aerodynamic diameter of ≤ 2.5μm (PM2.5) and ≤ 10.0 (PM10) was measured from Tehran Air Quality Control Corporation (TAQCC). Patient and ecological informations were analyzed using geographical information system. Results: Based on TAQCC, Tehran had an average of 180–250 polluted days per year for the last 10 years. The high incidence of pulmonary TB (18 to 31/100,000) was detected in populations which were exposed to high concentration of CO (2.7 to 5.2 parts per million, 95% confidence interval [CI]; 1.10 to 1.90) and PM2.5(35 to 42μg/m3; 95% CI 1.03 to 1.80). The level of SO2,NO, and PM10was also high but not significantly related to TB (P > 0.05). Conclusion: The long-term exposure to PM2.5 and CO was positively associated with TB development.

Keywords: Geographical information system, outdoor air pollution, tuberculosis


How to cite this article:
Rajaei E, Hadadi M, Madadi M, Aghajani J, Ahmad MM, Farnia P, Ghanavi J, Farnia P, Velayati AA. Outdoor air pollution affects tuberculosis development based on geographical information system modeling. Biomed Biotechnol Res J 2018;2:39-45

How to cite this URL:
Rajaei E, Hadadi M, Madadi M, Aghajani J, Ahmad MM, Farnia P, Ghanavi J, Farnia P, Velayati AA. Outdoor air pollution affects tuberculosis development based on geographical information system modeling. Biomed Biotechnol Res J [serial online] 2018 [cited 2023 May 30];2:39-45. Available from: https://www.bmbtrj.org/text.asp?2018/2/1/39/226577




  Introduction Top


Air pollution is affecting everyone in developed and developing countries and continues to pose a major threat to human health, worldwide.[1] According to World Health Organization (WHO), more than 2 million premature deaths each year are attributed to the effects of air pollution, of which the outdoor air pollution was associated with reduced lung function and increased respiratory mortality.[1],[2] In general, the source of air pollution is either atmospheric (outdoors), domestic (indoor), or occupational.[1],[2],[3],[4] Outdoor (ambient) air pollution is largely produced as a consequence of the inefficient combustion of fuels for transport and power generation whereas the indoor air pollution is formed by burning and heating of solid fuels (agricultural residues, dung, straw, and wood) or coals.[1],[2],[3],[4],[5] It has been shown that people living in air-polluted countries will disproportionately experience diseases such as cardiovascular and chronic respiratory symptoms such as lung cancer and chronic obstructive pulmonary disease.[5],[6],[7],[8],[9],[10],[11] Other than these well-documented health effects, an increasing number of studies highlighted the potential role of indoor and occupational air pollutions on incidence of tuberculosis (TB).[11],[12],[13],[14],[15],[16],[17] In this context, Tremblay in 1858 was the first to realize an inverse association between TB mortality and number of windows per household.[13] Since then, investigators reported the importance of indoor air pollution and TB although in most of studies, the risk of exposure was poorly assessed.[11],[12] Lin et al. in a systematic review and meta-analysis showed the relative increases in risk public relation (PR) of pulmonary TB, and indoor air pollution was to be 1.95%.[11] Likewise, occupational air pollution (i.e., silicosis) was showed to be associated with the elevated risk of TB.[14],[15] By contrast, limited studies could demonstrate the impact of outdoor air pollution on TB infection and/or progression of diseases.[16],[17] In one study, Hwang et al. have associated the long-term exposure to ambient sulfur dioxide [SO2] with high risk of TB in Korean males.[16] In another study, Smith et al. reported a positive association of pulmonary TB with ambient CO and nitrogen dioxide (NO2).[17] As such, the host immune system most often contains TB infection; however, in weekend immunity like in people who have compromised immune systems, people with malnutrition or diabetes, and/or people who smoke, diseases progress from inactive to activation forms.[18],[19],[20],[21],[22] Based on WHO estimation, 95% of TB death occurs in low- and middle-income countries, where the people breathe smoggy air over long of period time. Although there is no confirmation if the outdoor air pollution in these countries has impact on TB, and if it does then the attributed burden would become greater in near future. Here, we aimed to find out the effect of outdoor air pollution on TB in metropolitan city of Tehran. To perform the study, the geographic information system (GIS) was used to assess and analyze the collected information.[23],[24],[25],[26] The trend of outdoor air pollution (i.e., SO2, carbon monoxide (CO), nitrogen oxides, and particulates substances) was analyzed for the past 10 years. Then, the distribution of TB patients that were residing in one of 22 municipal areas of Tehran (for the same period) and were referred to hospital for diagnosis and treatment (2010–2016) were evaluated. The effect of other environment risk factors such as population, area, and climatic changes were also investigated.


  Methods Top


Data on tuberculosis patients

In this retrospective study, the information from confirmed TB cases (based on laboratory and radiological findings) that were registered (2010–2016) at National Research Institute of TB and Lung Diseases (NRITLD) was gathered. Patients that were residing in one of the 22 municipal regions of Tehran (at least 10 years) were included in this study. As the institute is the referral center for multidrug-resistant TB (MDR-TB) treatment and has the national TB laboratory of country, thereof, most of suspected TB patients in Tehran and nearby provinces are sent to this hospital for diagnosis and treatment. Data for patients include gender, family history, full postal address, age, ethnicity and nationality, duration of stay in Tehran.

Location of the study using geographic information system applications

Tehran is located in a mountainous area with elevation range from 1200 m to 1980 m (Lethbridge elevation 910 m). Tehran is the 19th largest metropolitan area in the world with population around 9 million in 2015. In Tehran, there are 22 municipal districts (MDs) (each with its own administrative center). Twenty of the 22 MDs are located in Tehran County's Central District, while the districts 1 and 20 are, respectively, located in Shemiranat and Ray counties. The GIS maps of Tehran with scale of 1:1000000 include municipal areas with climate conditions (average of rainfall, humidity, and dryness in the last 10 years) were elicited from the Forest, Rangeland, and Watershed Management Organization of Iran [Figure 1]. The map of 10-year pollution and populations' average were also collected from Tehran Municipal administration office. Substances that are estimated for air pollution are SO2, CO, nitrogen oxides, and particulates (≤2.5μm [PM2.5] and ≤ 10.0 [PM10]). These substances were measured from Tehran Air Quality Control Corporation (TAQCC) using one or more monitoring stations in each MDs [23],[24] (two municipal regions, i.e., D-12 and D-17 had no monitoring stations; therefore, no data enter for these regions). The obtained pollutant concentrations were more than 70% completeness in each year. To assess individual level of air pollution exposure, geocoded patient home and office address (for past 10 years) were assigned the pollutant concentration of the closet monitoring station in each MDs. The concentration measured is representative of the average exposure of the people.
Figure 1: Map of the study area (22 regions of Tehran city)

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Drawing of tuberculosis-related Maps

The 5 years' cumulative incidence rates of TB and TB-MDR were calculated according to 2016 population survey. These data were added to descriptive tables of GIS map, and distribution of TB forms was drawn. Each of population density, climate, average of rainfall maps, and air pollution (i.e., SO2, CO, nitrogen oxides, and particulate substances) was added to the distribution maps of incidence of TB forms, as a new layer by Arc GIS ver. 10.3, ESRI (Environmental Systems Research Institute, Inc.; Dublin, Ireland). To better display the relationships between TB and environmental parameters and/or population density, environmental parameters were divided into 3 subgroups: dry, dry and semidry, and humid-mediterranean. Air pollution was also grouped based on size and kind of substances into 4 groups: SO2, CO, nitrogen oxides, and particulates. Population was divided into 4 groups: 20000–100000; 100000–200000; 2000000–300000; and 300000–400000 .

Data analysis

To perform data analyses, SPSS version 15 (Chicago, IL, USA) was used. Relationships between TB incidence rates in different municipal areas and environmental parameters and population density were determined by means plot, independent t-test, and Pearson correlation coefficient. In addition, Structural Equation Modeling by Analysis of Moment Structure-20 was performed.[27]


  Results Top


Incidence of tuberculosis in 22 regional districts of Tehran using geographic information system mapping

During the study period, 5630 patients were referred to NRITLD, Tehran, Iran. Out of which, 1167 (20.3%) were residing in Tehran and the remaining (79.2%) were from other provinces. The male to female ratio was 1.1 and the average age was 47 for female and 50 for males. Four hundred and twenty (420/1167; 35.9%) patients were new smear positive and had no previous history of TB treatment, whereas the remaining 747 (64%) had previous history of TB. Out of which, 466/747 (60%) had been already registered in other public or private health center in Tehran, and only after treatment failure, they referred to this center for diagnosis and treatment. In overall, 333/1167 were reported to be MDR-TB (28.5%). The spatial aspects of TB distribution in 22 MDs of Tehran showed a hot- and cold-spot areas; the high prevalence was in districts D-1 (31.8/100,000), D-4 (20.9/100,000), D-20 (19.8/100,000), and D-7 (18.7/100,000), and low prevalence regions were districts D-21 (3.1/100,000) and D-22 (5/100,000) [Figure 2]. Classical investigation revealed that 39.0% of new smear-positive patients (164/420) were located in D-1 (49/164; 29.8%), D-2 (24/164; 14.6%), D-20 (51/.164; 31.0%), and D-7 (40/164; 24.4%). Likewise, the frequency of MDR-TB in the areas was shown to be D-2 (37/33; 11.1%) and D-4 (36/333; 10.8%). The MD of D-1, D-2, and D-4 are in Northern of Tehran and they are cross-boarding with each other [Figure 2] whereas the D-7 is in East and D-20 is in South of Tehran. The lowest incidence rates (5–7/100,000) are detected in west of Tehran in districts 21 and 22. In most of the instances, municipal areas with similar incidences are seen to be located close to each other's on the map, such as areas 7, 10, 11, and 12, and so on [Figure 2]. Based on this study, the total number of TB patients were 1167 cases among the total studied population (8,312,795 person) of the twenty two administrative areas of Tehran/IRI which accounts for a mean incidence rate of 13.23 case/100,000 population. While the total multidrug-resistant TB cases were 333 case which accounts for a mean incidence rate of 4 case per 100,000 population. The total surface area (Km 2) is ranging from lowest of 8.2 Km (D-17and D-10) to largest of 64.0 Km 2 (D-1and D-2). Five districts had larger Km 2 of areas (D-1, D-2, D-4, D-5, D-22, and D-21), of which two (D-21 and D-22) had lowest population density (2817.15/Km 2) with low TB incidence rate (average of 4/100,000). In contrast, the other larger area with higher population of density (10405.36/Km 2) had higher TB incidence rate (average of 22.8/100,000). Therefore, our results showed a positive association between TB incidence and population density (P < 0.05). Accordingly, weather conditions in municipal areas of Tehran are classified into 3 groups: humid and mediterranean (which seen in Northern of Tehran), districts 2–8 had dry to semidry, and districts 9–22 had dry conditions. The TB incidence rate (31.8/100,000) was highest in regions with humid and mediterranean climate. By combination of variable risk factors such as total area, air pollution index, and population density in “Analysis of Moment Structure,” we found a significant role of these variables in development of TB [Figure 3].
Figure 2: The geographic information system map of Tehran with scale of 1:1,000,000 includes 22 municipal areas. The spatial aspects of tuberculosis distribution in these districts (municipal districts) of Tehran, showed a hot- and cold-spot areas; the high prevalence was in districts D-1, D-4, D-20, and D-7 and low prevalence regions was in districts D-21 and D-22

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Figure 3: Structural equation modeling of tuberculosis incidence and the predictor variables: total area, air pollution index, and population density are positively associated with tuberculosis development

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Tehran air pollution

The concentration of air pollutant data represents the average pollutions of years 2006–2016. All the studied substances, i.e., SO2, NO2, CO, particles of PM2.5 and PM10 had higher annual average than WHO air quality guidelines.[1] The concentration of PM2.5 was highest in municipal regions D-1 (36.4 μg/m3), D-3 (42 μg/m3), D-4 (37.7 μg/m3),

D-7 (35.45 μg/m3), and D-20 (40.8 μg/m3). All these regions had either level of TB or MDR-TB patients. The average concentration of PM2.5 was 32.4 μg/m3 ranging from 22 to 42μg/m3( 95% confidence interval [CI]). Similarly, the average level of PM10 was 84.92 4 μg/m3 ranging from 50 to 116 μg/m3. The level was high in all municipal regions, but the concentrations were extremely high in southwest and southeast of Tehran, i.e., D-9 (116.5 μg/m3), D-14 (113.9 μg/m3), D-15 (89.24 μg/m3), D-18 (116.9 μg/m3), and D-21 (109 μg/m3). The incidence of TB was low in these regions; thereby, the high level of PM10 was not associated with TB [Figure 4]. Our results also showed high level of CO (2.7 to 5.2 parts per million [ppm], 95% CI; 1.10 to 1.90) in districts (D-1, D-3, D-4) where the incidence of TB was high. The low concentrations (1.4 to 2.4 ppm) were detected in west (D-9; D-21, D-22, D-18), east (D-13; D-14), and south ((D-15) where the incidence of TB was low [Figure 5]. Based on WHO standard value/annual mean, the estimated surface of NO2 concentration is 40 ppb.[1],[2] The average concentration of NO2 is 49.82 ppb ranging from 21.1 to 99.0 ppb. We found one district (D-4) with 84.15 ppb had 20.9 per 100,000 TB incidence; in contrast, another district (D-10) with 99.0 ppb had 9.6 per 100,000 TB incidence. Hence, NO2 may not directly affect the TB development. Likewise, the SO2 concentration was variable, and we could not confirm direct association between SO2 and TB. The average was 20.7 ppb ranging from 13.6 to 31 ppb. Overall, the regions with high incidence of TB (D-1, D-4, D-7, D-20) had higher concentration of ambient air pollution, during study period (95% CI).
Figure 4: The geographical scales in Tehran demonstrate the highest tuberculosis and/or multidrug-resistant tuberculosis patients in areas with highest level of PM2.5 concentration. These areas had D-1; D-3, D-7; D-20 even higher than IT-1 level (35 to 42.8 μg/m3)

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Figure 5: Based on Tehran Air Quality Control Corporation report, the level of CO (2.7 to 5.2 parts per million, 95% confidence interval; 1.10 to 1.90) was positively correlated with tuberculosis development

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  Discussion Top


Tehran air was unhealthy or worse for 180–250 days, according to TAQCC. The number of polluted days was raised to average of 220–250 per year from 2010 to 2016. The level of pollutants substances, i.e., SO2, NO2, CO, and particles (PM2.5 and PM10) was significantly higher than recommended interim targets.[1],[2] This low quality of air is not only attributed to the presence of million cars that are old and not provided with catalysts convertors but also related to Tehran geographical location and its altitude.[23],[24],[28],[29] The city is surrounded by mountain in the north, northwest, east, and southeast with no perennial winds. As a result, in most of the times, there is no flow to carry out the polluted air from city.[28],[29] In the present investigation, we found that the TB incidence rate is more than 10-fold in area with higher concentration of PM2.5. In general, the fine particulate matter measuring less than 2.5 μm enters the respiratory tract and is considered to contribute to the health effects observed in urban environments.[5],[6],[30],[31] Differences between proportions of two PMs (less than 10 and 2.5 μm) in municipal regions of Tehran indicate variable sources for particulate air pollution. The PM10 is primarily produced by mechanical processes such as construction activities, road dust re-suspension, and wind, whereas the PM2.5 is usually originated from combustion sources.[1],[2],[30] Based on WHO air quality guidelines, there are three level of interim targets (IT) for PM2.5.[1],[2] The highest mean concentrations of PM2.5 is about 35μg/m3 that was selected as theIT-1 level, followed by IT-2 (25μg/m3) and IT-3 (15μg/m3). The mean concentration of PM2.5 in Tehran was 32.4 μg/m3, and in 4 areas (D-1, D-3, D-7, D-20), the level was even higher (35 to 42.8 μg/m3) than IT-1 level. This level of PM2.5 is very alarming and needs an urgent attention. Recently, Sarkar et al. (2011) showed diesel exhaust particles (DEP) “as a major component of urban fine particulate matter.”[31] He showed this particulate would induce “dysregulation of host immunity” that may result in increased susceptibility to M. tuberculosis infection and/or facilitate reactivation of latent M. tuberculosis infection and increased incidence of TB.[31] The geographical scales in Tehran demonstrate the highest TB patients in areas with highest level of PM2.5 concentration (35 to 42μg/m3; 95% CI 1.03 to 1.80). Based on available literature, the fine particulate with less than 2.5 μm remains airborne for prolonged time periods and can easily deposit in the lungs on inhalation. Likewise, Tubercle bacilli is inhaled and can remain in infected TB patients. Therefore, in real-life conditions, the concurrent of respiratory exposure to PM2.5 and Tubercle bacilli are expected to occur although morein vitro experiments are needed to confirm its direct effect on host immune system. The average concentration of PM10 was 84.92 μg/m3 (ranging from 50 to 116 μg/m3) during the study period. Although no differences was observed in level of PM10 in areas with high and low incidence of TB, PM10 includes both the coarse (particle size between 2.5 and 10 μm) and fine particles (<2.5 μm). These particles are usually associated with increased mortality in both developed and developing countries.[1],[5],[6],[31] Naddafi et al. in 2012 reported excess of mortality in short-term exposure to PM10 in Tehran.[24] In similar context, Tominz et al. showed the impact of PM on 24,000 inhabitants was excess of 8 out of 177 mortality in a year in two small towns in Northern Italy.[32] In another study, the number of excess cases attributed to air particulate (PM10) was 677 for total mortality.[33] Based on these observational studies, it has become clear that PM10 particulate poses a greatest respiratory health effects, which might indirectly affect the TB development also.

As shown in [Figure 4], the concentration of CO had significantly (2.7 to 5.2 ppm, 95% CI; 1.10 to 1.90) correlated with TB. The main sources of CO production are incomplete combustion of carbon-containing fuels, such as gasoline, natural gas, and oil, thereby we suggest old vehicles as a largest anthropogenic source of CO in Tehran.[24],[28],[29] The toxicity of CO on bacterial and mammalian cells has been demonstrated; but in contrast, there is no strong evidence to show that CO inhibits Mycobacterium tuberculosis (MTB) growth.[34],[35] Already in experiments performed by Park et al., Mycobacterium species were able to grow on CO, a bit more slowly.[36] Furthermore, it has been shown that MTB can utilize CO at <1–5 ppm, which is relevant range since CO in the atmosphere and lungs measure at approximately 0.1 to 0.5 ppm and < 3ppm, respectively.[34],[35],[36],[37] Usually, the inhaled CO gets rapidly crossed the alveolar epithelium to reach the blood, where it binds to hemoglobin to form carboxyhemoglobin (COHB).[35],[36],[37] The COHB inhibiting the release of O2 from hemoglobin to body tissues.[35] Thereby, since the CO has greater affinity for hemoglobin than O2, the presence of CO in lung will displace O2 from hemoglobin.[1],[2],[36],[37] Hence, if there will more CO in the atmosphere, the concentration of CO in lungs also will increase, and this increase is not inhibiting the growth of Mycobacterium tuberculosis, because the bacilli have mechanism to bypass CO toxicity.[36],[37] However, the low O2 in lungs may draw a Mycobacterium tuberculosis to change their lifecycle into more restricted forms [18] although this needs to be investigated in long-term exposures. The NO2 is an important fraction of the ambient air PM2.5 mass and in presence of hydrocarbons and ultraviolet light is the main source of tropospheric ozone and nitrate aerosols.[1],[38] The current accepted value for NO2 is 40 μg/m3 (annual mean);[1],[2] the average concentration of NO2 in this study was 49.82 ppb (21.1 to 99.0 ppb) throughout the year. Likewise, the concentration of SO2 in municipal regions of Tehran was high, but the level of these two substances was also high in area with low TB incidence rate. The SO2 has high water solubility and can easily reach the upper airways.[16],[39] Where they get dissolve and dissociate into bisulfite and sulfite ions, which can be transferred into systemic circulation.[16],[39] The SO2 can affect pulmonary defense, including macrophage function, mucociliary transport, and alveolar clearance.[39] Moreover, the SO2 can affect the cytokine release like tumor necrosis factor and interleukins-1.[40] Hence, more investigation might be needed to evaluate the effect of SO2 on progression or activation of TB diseases. Finally, our results showed that majority of new smear patients (164/420; 39%) are residing in areas which had higher level of outdoor air pollution. Classical investigation revealed interlinking of 6% of patients only (n = 10). The remaining 154/164 (95.1%) developed TB without any previous contact. Basically, Tubercle bacilli can remain dormant for long times in host immune system; breathing these toxic molecules can make lung defense system week or engaged; as a result, the bacilli might get better chance to become active. Thereby, the outdoor air pollution in long terms may have effect on TB progression.

In this study, the other environmental risk factors such as population and area were found to be positively associated with TB using Structural Equation Modeling analysis.[25] We used GIS-technology to store and collect the information (nritld-rer.ir). Basically, GIS is a database which is used by different users to meet various information needs.[41] This technology has strong analytical performance and can help us in collecting and analyzing the data.[42] Today, with vast amount of information, the use of GIS is becoming mandatory applications for health programer and TB policymakers, even in developing countries like Iran.


  Conclusion Top


We found a significant association between PM2.5, CO, and TB. Although to find out the exact role of these substances in relation to host immune responses and TB bacilli itself, it may be crucial to perform anin vitro study. The information provided in this study will outline the urgency of measures to reduce contaminated air and protect public health within the country.

Acknowledgment

Authors also wished to thank Dr. Mohanad M. Ahmad, University of Karbala, Iraq for helping to analyze the GIS-data.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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