Abstract
OBJECTIVE:
Humanitarian crisis in the Middle East geography has brought refugees into being. The aim of this study is to investigate the relationship between refugees’ tuberculosis diagnosis process and air pollution parameters and environmental exposures.
Methods:
A total of 229 patients with tuberculosis registered at Şanlıurfa Tuberculosis Dispensary during 2012-2018 were included. In this cross-sectional study, education levels, smoking status, warm-up style, and exposure to biomass, pesticides, dust storm, PM10, and sulfur dioxide were evaluated. Air parameters were received from https://www.havaizleme.gov.tr/. Bacteriological diagnosis was classified as smear-positive lung tuberculosis, smear-negative culture-positive lung tuberculosis, and other diagnostic methods. This study was approved by the Harran University Ethical Committee (10.12.2018; session: 12; decision no: 36).
Results:
Of the 229 patients diagnosed with tuberculosis, 53.3% were males and 46.7% were females. The average age was 31.15 ± 15.16. About 24.5% of refugees lived in camps, while 75.5% lived outside of the camps. The rate of smear (+) lung tuberculosis was 38% and smear (−) culture (+) lung tuberculosis was 14.4%.
Smoking (P = .007) in smear (+) cases and exposure to PM10 (P = .036) and sulfur dioxide (P = .015) in culture (+) cases were significant.
Conclusion: Smoking and air pollution are associated with delayed diagnosis of tuberculosis and severe forms of tuberculosis. We think that as a result of smoking cessation and reduction of air pollution, tuberculosis incidence in refugees can be reduced.
Keywords: Air pollution, particulate matter, smoking, Syrian refugees, tuberculosis
Main Points
Examining the relationship between refugees' air pollution parameters and their environmental exposure.
Examining the relationship between smear-positive TB cases and PM10 and SO2.
Comparing tuberculosis (TB) in Turkish citizens and refugees.
Demonstrating that cigarette smoke and air pollution are risk factors for TB.
It is a study showing that TB incidence in refugees can be reduced by quitting smoking and reducing air pollution.
Introduction
Tuberculosis (TB) is still an important disease that requires timely diagnosis and treatment. Globally, in 2019, there were estimated 10.0 million TB cases and 1.4 million TB deaths.1 According to the 2019 Organization for Economic Co-Operation and Development data, 2.8% of the population was foreign-born.2 Socioeconomic parameters such as unemployment, poverty, low income, and rapid population growth are known to increase the incidence of TB.3
Air pollution is the elevation of pollutants that can be found in the atmosphere to the levels that adversely affect the health of people and living creatures and/or increase to the amounts that will cause material damage.4 Air pollution indicator is particulate matter (PM). Particulate matter is measured in terms of micrograms per cubic meter (μg/m3) and is named according to its size.5 Air pollution is associated with poverty.6 Now it is known that air pollution and other environmental factors play a role in the development of TB.
Wars and accompanying hunger, homelessness, and being a refugee cause a decline in health indicators including TB.7 The concept of the refugee was published in 1951 in the United Nations Geneva Convention with the definition of “as a person who has a rightful fear that he/she will be persecuted because of his race, religion, nationality, membership of a certain social group or political thoughts, and therefore leaves his country and does not return or want to return because of his fear.”8 Tuberculosis-causing agent is Mycobacterium tuberculosis, a complex bacilli. Among persons living in the same environment, the bacillus is transmitted to healthy persons by inhalation of the bacilli into the lungs. The most infectious patients are those with laryngeal TB and cavity pulmonary TB.9 For diagnosis, smear and staining with Ehrlich–Ziehl–Neelsen are performed. The transmission potential of patients who are smear negative is less than that of those who are smear positive.10 In this study, we examined the relationship between bacteriological case definitions in Syrian Refugees and PM10 and sulfur dioxide (SO2) from outdoor air pollution parameters in the context of TB.
Material and Methods
Study Design
This cross-sectional study included 229 refugee patients who applied to Şanlıurfa Tuberculosis Dispensary between 2012 and 2018 and were diagnosed with TB. Criteria for inclusion in the study were having been diagnosed with TB between 2012 and 2018 and being a refugee. This study was approved by the Harran University Ethical Committee (10.12.2018; session: 12; decision no: 36).
Data Collection
Age, gender, education level, place of residence, smoking status, way of heating, exposure to biomass, pesticide, and dust storm, year of diagnosis, bacteriological diagnosis, treatment status, and organ involvement of patients were recorded. According to the organ involvement, TB classification was performed as lung TB, extrapulmonary TB, and both lung and extrapulmonary TB. Classification according to the treatment status included treatment, treatment completion, treatment lost to follow-up, transfer to another center, death, and ongoing treatment. Bacteriological diagnosis was classified as smear-positive lung TB, smear-negative culture-positive lung TB, and other diagnostic methods. Other diagnostic methods included adenosine deaminase enzyme level, TB polymerase chain reaction, smear-negative pulmonary TB, and so on.
Organ involvement, bacteriological diagnosis type, treatment results, and home addresses of the patients were listed. The patients were visited at their homes, and questions on smoking status, ways of heating, and exposure to pesticides, biomass, and dust storm were asked to those who volunteered to participate, and their answers were recorded. Interviews with Syrian refugees were conducted in the presence of a certified translator. Each visit lasted for an average of 25-30 minutes.
The average annual PM10 and SO2levels in Şanlıurfa between 01.01.2012 and 31.12.2018, where patients were diagnosed, were retrieved from https://www.havaizleme.gov.tr/.
Results
Of the 229 patients diagnosed with TB, 53.3% were males and 46.7% were females. The mean age was 31.15 ± 15.16. About 24.5% of the participants lived in camps, while 75.5% lived outside of the camps. While the number of diagnosed cases was 0.9% in 2012, it was 12.7% in 2018, and the highest rate was 27.1% in 2015 (Table 1).
Table 1.
Distrubution of Demographic Characteristics and Diagnosis Year of Patients With Tuberculosis
| Features (n = 229) | n (%) |
|---|---|
| Age min-max=1-72 Mean ± SD, 31.15 ± 15.16 | |
| Gender | |
| Female | 122 (53.3) |
| Male | 107 (46.7) |
| Residence | |
| City center | 173 (75.5) |
| Camp | 56 (24.5) |
| Diagnosis year | |
| 2012 | 2 (0.9) |
| 2013 | 15 (6.6) |
| 2014 | 29 (12.7) |
| 2015 | 62 (27.1) |
| 2016 | 43 (18.8) |
| 2017 | 49 (21.4) |
| 2018 | 29 (12.7) |
In total, 56.3% of the individuals in the study group declared that they smoke, 30.1% of the participants had pesticide exposure, 24.0% had biomass exposure, and 91.3% had dust storm exposure. The most common form of heating was coal with 39.3% (Table 2).
Table 2.
Distribution of Exposure of Patients with Tuberculosis to Some Environmental Substances
| n(%) | |
|---|---|
| Smoking | |
| Yes | 129 (56.3) |
| No | 94 (41.0) |
| Passive smoker | 4 (1.7) |
| Ex-smoker | 2 (0.9) |
| Pesticide exposure | |
| Yes | 69 (30.1) |
| No | 160 (69.9) |
| Biomass exposure | |
| Yes | 55 (24.0) |
| No | 177 (76.0) |
| Dust storm exposure | |
| Yes | 209 (91.3) |
| No | 20 (8.7) |
| Heating type | |
| Wood | 58 (25.3) |
| Coal | 90 (39.3) |
| Wood and coal | 8 (3.5) |
| Electric | 69 (30.1) |
| Natural gas | 2 (0.9) |
| Central heating | 2 (0.9) |
Pulmonary TB shows the most common organ involvement, with 71.2%. When TB treatment was examined, the results showed 42.4% treatment completion and a cure rate of 18.8%. The rate of death in TB follow-ups is 4.8%. Bacteriologically, smear (+) lung TB is 48.9% and smear (−) culture (+) lung TB is 34.9% (Table 3).
Table 3.
Distribution of Patients with Tuberculosis to Clinical Characteristics
| n (%) | |
|---|---|
| Location of TB | |
| Lung TB | 163 (71.2) |
| Extrapulmonary TB | 57 (24.9) |
| Both lung TB and extrapulmonary TB | 9 (3.9) |
| Treatment outcome | |
| Cure | 43 (18.8) |
| Completed treatment | 97 (42.4) |
| Death | 11 (4.8) |
| Treatment lost to follow-up | 36 (15.7) |
| Transfer | 16 (7.0) |
| Treatment is still continuing | 26 (11.4) |
| Bacteriological diagnosis | |
| Smear (+) lung TB | 112 (48.9) |
| Smear (−) culture (+) lung TB | 80 (34.9) |
| Other diagnosis type | 37 (16.2) |
In one-way analysis, it was seen that there were no effects of pesticide exposure (F = 1.458, P = .235), heating (F = 0.084, P = .919), biomass exposure (F = 1.731, P = .179), and dust storm exposure (F = 1.615, P = .201) on bacteriological diagnosis. In smear (+) cases smoking (P = .007) , in culture (+) cases exposure to PM10 (P = .036) and SO2 (P = .015) were significant. With bacteriological diagnosis, the average values of parameters related to air pollution are presented in Table 4.
Table 4.
Comparison of Bacteriological Diagnosis and Air Pollution Parameters
| Smear (+), n = 112 | Smear (−) Culture (+), n = 80 | Other Case Diagnosis Type, n = 37 | F/P | |
|---|---|---|---|---|
| Smoking | 0.76 ± 0.557 | 0.53 ± 0.656 | 0.49 ± 0.507 | 5.096/.007 * |
| Pesticide exposure | 0.25 ± 0.435 | 0.36 ± 0.484 | 0.32 ± 0.475 | 1.458/.235 |
| Heating type | 2.39 ± 1.276 | 2.46 ± 1.222 | 2.46 ± 1.325 | 0.084/.919 |
| Biomass exposure | 0.19 ± 0.392 | 0.30 ± 0.461 | 0.27 ± 0.450 | 1.731/.179 |
| Dust storm exposure | 0.95 ± 0.226 | 0.88 ± 0.333 | 0.89 ± 0.315 | 1.615/.201 |
| PM10 | 52.45 ± 11.497 | 55.99 ± 12.455 | 50.16 ± 14.200 | 3.384/.036 * |
| SO2 | 14.04 ± 7.068 | 17.07 ± 9.975 | 13.62 ± 3.530 | 4.248/.015 * |
*Post hoc least significant difference.
Discussion
Our study evaluates refugees diagnosed with TB, certain sociodemographic characteristics, diagnostic processes, and exposures in their environment, and the relationship between PM10 and SO2 and bacteriological diagnosis. With this aspect, this is a noteworthy study in the literature. We found the means of smoking in bacteriological smear (+) cases (P = .007) and of exposure to PM10 (P = .036) and to SO2 (P = .015) in smear (−) culture (+) cases to be significantly higher .
Smoking causes severe TB and/or deaths worldwide. Previous studies have shown that the smoke caused by smoking, which is one of the causes of indoor air pollution, has damaged alveolar macrophages, and as a result, the anterior defense system of the lungs has weakened.11 In a meta-analysis conducted by Wang et al.12 in 2020, contrary to our findings, they reported that smoking caused smear and culture negative in bacteriological diagnosis and delay in TB diagnosis.12 In countries with high TB incidence and prevalence, there are studies reporting that TB outbreak can be controlled by smoking cessation.13 There are similar studies in Turkey on the effects of effective control of smoking and indoor air quality to help prevent the risk of developing TB control.14 In this study, 56.3% of patients had smoking habit, similar to the numbers reported in the literature. We found that there was a significant relationship between smoking and TB in patients with bacteriological smear (+) cases (P = .007).
PM10, one of the air pollution parameters, is suspended in the atmosphere. It reaches the lungs through the respiratory tract and plays a role in the etiopathogenesis of various diseases.15 Another air pollutant is SO 2 . Popovic et al.16 reported that limited evidence of associations exists for PM10, SO 2 with TB.16 Short-term exposure to low SO 2 in the environment, according to a different opinion on SO2, is thought to have an acute protective effect against lung infections.17 This view was suggested for patients who were followed up on in the TB outpatient clinic. In another study, Zhu et al.18 found a significant relationship between exposure to PM10 and SO2 and the frequency of lung TB.18 In our study, we found a significant relationship between air pollution parameters and bacteriological diagnosis, in parallel with the literature. In smear (−) culture (+) cases, PM10 (P = .036) and SO 2 (P = .015) averages were significantly higher.
Pesticides show toxic effects in humans and weaken the immune system. Pesticide application causes respiratory diseases in acute and chronic periods.19 As a result of exposure to pesticides, TB sensitivity increases.20 In our study, 30.1% of the participants had pesticide exposure. There were no significant differences smear (+), smear (−) culture (+) and other case diagnosis type (Table 4).
In recent years, relatively many studies have linked biomass fuel fume exposure to various aspects of TB. It has been reported that there is a relationship between TB and exposure to biomass fuel fumes compared to fumes from other cleaner forms of fuel.21 Another study reported that biomass fuel is a risk factor for lung TB and emphasized the importance of reducing biomass fuel.22 In this study, we found biomass exposure to be 24.0%. However, no statistically significant differences were found Smear (+), smear (−) culture(+) and other case diagnosis type (Table 4).
The southeastern region of Turkey is often affected by dust storms coming from the Middle East due to its geographical location. Cellular growth is impaired as a result of exposure to dust particles contained in dust storms. Dust storm exposure causes respiratory complaints and diseases in the acute and/or chronic period.23 According to a study, young men coming from outside regions to geographical locations with dust storms were found to be at more risk of death than the local population.24 Refugees have been exposed to periodic dust storms originating from the desert in Syria where they used to live and to dust stroms in Turkey where they migrated as these countries are in the same geography. In our study, 91.3% dust storm exposure was detected. However, there was no significant difference between the groups for TB bacteriological diagnosis. Patients were warned not to go out during dust storms and/or to wear a respiratory mask.
In conclusion, in our study in which we investigated the relationship between air pollution parameters and environmental exposures of refugees in the context of TB, that is, smear-positive TB cases, and air pollution parameters PM10 and SO 2 , we observed that smear negative-culture positive more TB-positive cases. The main result of our study is that cigarette smoke and air pollution are risk factors for TB. Smoking and air pollution are associated with delayed diagnosis of TB and severe forms of TB. We think that as a result of smoking cessation and reduction of air pollution, TB incidence in refugees can be reduced.
Limitations
This study has several limitations. The scope of our study, which examines the relationship between the factors related to TB frequency, is refugees. One out of every four refugees is staying in camps. The living space conditions of refugees who stay in camps and outside of the camps differ. In addition, air pollution parameters are measured on a national air quality monitoring network, not on a home basis, and other pollutants such as PM2.5 and ozone are not measured in our region.
Funding Statement
The authors declared that this study has received no financial support.
Footnotes
Ethics Committee Approval: This study was approved by the Harran University Ethical Committee (10.12.2018; session: 12; decision no: 36).
Informed Consent: Verbal informed consent was obtained from the patients who agreed to take part in the study.
Peer Review: Externally peer-reviewed.
Author Contributions: Concept - Ş.K., R.C.; Design - Ş.K., R.C.; Supervision - Ş.K., R.C.; Resources - Ş.K., R.C.; Materials - Ş.K.; Data Collection and/or Processing - Ş.K., R.C.; Analysis and/or interpretation - Ş.K., R.C.; Literature Review - Ş.K., R.C.; Writer - Ş.K., R.C.; Critical Review - Ş.K., R.C.
Acknowledgments: The authors sincerely thankful to Professors Peri Meram Arbak and Associate Professor Dr. Zafer Hasan Ali Sak for their invaluable support.
Conflict of Interest: The authors have no conflict of interest to declare.
References
- 1. World Health Organization (WHO). Global tuberculosis report 2020. Available at: https://apps.who.int/iris/bitstream/handle/10665/336069/9789240013131-eng.pdf. [Google Scholar]
- 2. Organization for Economic Co-Operation and Development (OECD). Foreign-born population (indicator). 2021. 10.1787/5a368e1b-en) [DOI] [Google Scholar]
- 3. Trauer JM, Dodd PJ, Gomes MGM, et al. The importance of heterogeneity to the epidemiology of tuberculosis. Clin Infect Dis. 2019;69(1):159–166.. 10.1093/cid/ciy938) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. HEAL. Linyit kömürü: sağlık etkileri ve sağlık sektöründen tavsiyeler. 2018. Available at: https://www.env-health.org/wp-content/uploads/2018/12/HEAL-Lignite-Briefing-TRweb.pdf. [Google Scholar]
- 5. World Health Organization (WHO). Ambient (Outdoor) Air Quality and Health. Accessed August 2, 2016. [Google Scholar]
- 6. Viegi G, Simoni M, Scognamiglio A, et al. Indoor air pollution and airway disease. Int J Tuberc Lung Dis. 2004;8(12):1401–1415.. [PubMed] [Google Scholar]
- 7. Kurtuluş Ş, Sak ZHA, Can R. Chest diseases in refugees living in a tent camp and in Turkish citizens living in the district: Ceylanpınar experience. Turk Thorac J. 2018;19(3):117–121.. 10.5152/TurkThoracJ.2018.17070) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. BMMYK. Convention and protocol relating to the status of refugees. 1951. Available at: https://www.unhcr.org/protection/basic/3b66c2aa10/convention-protocol-relating-status-refugees.html, Accessed August 8, 2020. [Google Scholar]
- 9. World Health Organization (WHO). End TB strategy. Available at: https://www.who.int/tb/strategy/en/, Accessed August 9, 2019. [Google Scholar]
- 10. Kara F. Tüberküloz Tanı ve Tedavi Rehberi. Sağlık Bakanlığı. 2nd ed. Ankara: Medya Tanıtım Matbaa; ve The Global Plan to Stop TB: 2011-2015; Stop TB Partnership; 2010; 2019. [Google Scholar]
- 11. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002;2(5):372–377.. 10.1038/nri803) [DOI] [PubMed] [Google Scholar]
- 12. Wang EY, Arrazola RA, Mathema B, Ahluwalia IB, Mase SR. The impact of smoking on tuberculosis treatment outcomes: a meta-analysis. Int J Tuberc Lung Dis. 2020;24(2):170–175.. 10.5588/ijtld.19.0002) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Perriot J, Underner M, Peiffer G, Flaudias V. Strategy and stopping smoking interventions in smokers with tuberculosis. Rev Med Liege. 2020;75(2):100–104.. [PubMed] [Google Scholar]
- 14. Öztürk AB, Kılıçaslan Z, Işsever H. Effect of smoking and indoor air pollution on the risk of tuberculosis: smoking, indoor air pollution and tuberculosis. Tuberk Toraks. 2014;62(1):1–6.. 10.5578/tt.7013) [DOI] [PubMed] [Google Scholar]
- 15. Yıldız Gülhan P, Güleç Balbay E, Elverişli MF, Erçelik M, Arbak P. Do the levels of particulate matters less than 10 μm and seasons affect sleep? Aging Male. 2020;23(1):36–41.. 10.1080/13685538.2019.1655637) [DOI] [PubMed] [Google Scholar]
- 16. Popovic I, Soares Magalhaes RJ, Ge E, et al. A systematic literature review and critical appraisal of epidemiological studies on outdoor air pollution and tuberculosis outcomes. Environ Res. 2019;170:33–45.. 10.1016/j.envres.2018.12.011) [DOI] [PubMed] [Google Scholar]
- 17. Ge E, Fan M, Qiu H, et al. Ambient sulfur dioxide levels associated with reduced risk of initial outpatient visits for tuberculosis: a population based time series analysis. Environ Pollut. 2017;228:408–415.. 10.1016/j.envpol.2017.05.051) [DOI] [PubMed] [Google Scholar]
- 18. Zhu S, Xia L, Wu J, et al. Ambient air pollutants are associated with newly diagnosed tuberculosis: a time-series study in Chengdu, China. Sci Total Environ. 2018;631-632:47–55.. 10.1016/j.scitotenv.2018.03.017) [DOI] [PubMed] [Google Scholar]
- 19. Sak ZHA, Kurtuluş Ş, Ocaklı B, et al. Respiratory symptoms and pulmonary functions before and after pesticide application in cotton farming. Ann Agric Environ Med. 2018;25(4):701–707.. 10.26444/aaem/99561) [DOI] [PubMed] [Google Scholar]
- 20. Riaz S, Manzoor F, Mahmood N, Shahid S. Molecular detection of M. tuberculosis and M. bovis and hematological and biochemical analyses in agricultural sprayers exposed to pesticides: a cross-sectional study in Punjab, Pakistan during 2014-2016. J Expo Sci Environ Epidemiol. 2017;27(4):434–443.. 10.1038/jes.2016.88) [DOI] [PubMed] [Google Scholar]
- 21. Bishwakarma R, Kinney WH, Honda JR, et al. Epidemiologic link between tuberculosis and cigarette/biomass smoke exposure: limitations despite the vast literatüre. Respirology. 2015;20(4):556–568.. 10.1111/resp.12515) [DOI] [PubMed] [Google Scholar]
- 22. Gulhan PY, Elverisli MF, Ercelik M, et al. Relationship between diagnosis period and internal and external air quality in patients with tuberculosis. Eurasian J Med. 2020;52(1):77–80.. 10.5152/eurasianjmed.2020.19226) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Yuan Y, Alahmad B, Kang CM, et al. Dust events and indoor air quality in residential homes in Kuwait. Int J Environ Res Public Health. 2020;17(7):2433. 10.3390/ijerph17072433) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Achilleos S, Al-Ozairi E, Alahmad B, et al. Acute effects of air pollution on mortality: a 17-year analysis in Kuwait. Environ Int. 2019;126:476–483.. 10.1016/j.envint.2019.01.072) [DOI] [PMC free article] [PubMed] [Google Scholar]