The present large-scale study of a representative Mongolian adult population found a significant positive association between exposure to solid fuels for heating and TB. This association was independent of potential confounding factors, such as gender, smoking, marital status, BMI, contact with an active TB case, and previous history of TB. IAP from household solid fuel combustion may be a risk factor for TB in the Mongolian population, which spends most of the time at home indoors due to the cold climate.
In 2017, household IAP contributed to 1.8 million global deaths and 60.9 million disability adjusted life years (DALYs), and infectious respiratory diseases including TB accounted for most of the respiratory burden, with 27.4 million DALYs [7]. Although TB and IAP are both pressing public health issues in Mongolia, the present study is the first to report an association between IAP due to solid fuel combustion and TB in Mongolia. Due to extreme cold and long heating season, it is common for households to keep their doors and windows closed, which reduces the air circulation indoors, concentration of the pollutants released from burning solid fuels increases the exposure to respirable pollutants on individual level. Prolonged exposure to such pollutants impairs the normal clearance of secretions on the tracheobronchial mucosal surface and thus may allow a causative organism mycobacterium TB, to escape the first level of host defenses which prevent bacilli from reaching the alveoli [5].
Given that people spend 90% of their lifetime in indoor settings, indoor air quality is a major risk factor for human health [24, 25]. Some epidemiological studies have reported an association between solid fuel smoke and TB. In a case-control study conducted in Mexico, household IAP exposure was found to facilitate the development of active TB, and exposure to smoke from biomass fuels for more than 20 years led to a 3-fold higher incidence of active TB than controls (OR: 3.3; 95% CI: 1.06–10.30) [26]. A hospital-based case-control study by Pokhrel et al. found that exposure to IAP was 3.4 times more common in TB cases than in controls [27]. A meta-analysis, which included a systematic review of 12 papers, reported a 30% higher risk of developing TB in individuals exposed to IAP (OR: 1.30; 95% CI: 1.04–1.62; p < 0.02) [19]. Another meta-analysis concluded that the risk of active TB depends on the type of fuel used, with the highest risk (43% increased risk) being associated with burning solid fuels [25]. A recent meta-analysis reported that IAP is associated with the risk of contracting TB (relative risk: 1.68; 95%, CI: 1.108–2.542; p < 0.014) [28].
The combustion of solid fuels emits many chemicals which impact human health, including PM, carbon dioxide, carbon monoxide, sulfur dioxide (SO2), sulfur trioxide, nitrogen dioxide, and nitric oxide [29]. There is increasing evidence that PM exposure weakens anti-mycobacterial host immunity [30, 31]. Chronic PM exposure accompanied by high constitutive expression of pro-inflammatory cytokines results in relative cellular unresponsiveness [31, 32]. Eighty percent of the total global exposure to airborne PM occurs indoors in developing countries [33]. PM2.5 has been reported to affect lung pathology, with smear positive TB patients being more exposed to PM2.5 than smear negative TB patients [34]. Moreover, chronic exposure to PM10 ≥ 50 μg/m3 was associated with an increase in the time required for TB positive sputum culture conversion [35]. In the present study, people exposed to IAP from household solid fuel use were more likely to have smear positive TB than bacteriologically confirmed TB, and exposure to smoke from tobacco were also associated with bacteriologically confirmed TB. The indoor PM2.5 concentration is very high in ghers and houses with stoves using semi-coke coal, with estimates of 107.0 μg/m3 in winter months average, which is higher than the permissible concentration in the WHO air quality guidelines (i.e., not exceed 10 μg/m3 annual mean or 25 μg/m3 24-h mean) [36]. SO2 is also a major pollutant from solid fuel combustion, and SO2 from coal burning is associated with persistent cough symptoms among schoolchildren in urban and suburban Mongolia [37].
In Mongolia, 45.2% of households live in traditional ghers and 29.5% live in ordinary wooden houses [8]. Over 95% of households living in ghers use solid fuels including coal for everyday cooking and heating [38]. The traditional gher is a portable circular wood framed dwelling covered in multiple layers of wool felt. Heating is provided by a stove located at the center of the gher, and a chimney directs the fuel smoke through the central roof vent. In Mongolia, TB cases show seasonality, sharply rising in the spring from March to May. UB is the coldest capital city in the world, with temperatures reaching minus 40 °C during the night in winter. People spend most of their time indoors, and thus transmissibility of TB increases, as people are exposed to solid fuel smoke at home [39, 40].
We also found that TB is more common among males than females, and that tobacco smoking is associated with TB. Compared to non-smokers, smokers have an increased risk of developing TB (OR: 1.8; 95% CI: 1.3–2.5; p < 0.01). This finding is consistent with previous studies. In addition, there was positive association between tobacco smoking and solid fuel use in the present study. Therefore, tobacco smoking may be one of potential confounding factors. According to a WHO report, the global TB incidence is higher in males than in females, with male-to-female ratios of TB ranging from 1.3 in the Eastern Mediterranean to 2.1 in the Western Pacific region [3]. This gender difference in incidence might be explained by the higher rate of smoking among Mongolian men than women (males, 46.3%; females, 6.8%) [41]. In the present study, smoking was more prevalent in males compared to females (males, 44%; females, 6%). Plenty of epidemiological and biological studies provide insight into the biological mechanism underlying the association between tobacco smoking and TB. Tobacco smoke exposure attenuates cytokine production and TB killing by macrophages, and exposure to nicotine impairs the anti-TB defense of macrophages by two mechanisms, including the inhibition of autophagy and activation of immunosuppressive Treg cells [42].
Numerous epidemiological studies demonstrate that both the exposure from active and passive smoking have been shown to be associated with TB infection and the transmission from being infected to developing TB disease [43,44,45]. However, our present study could not find the relationship between passive tobacco exposure and TB association. Passive smoking exposure is lower than that experienced by active smokers, while the smoke is generally similar and contains the same gases and particles including a wide range of irritating compounds and carcinogens [46]. Indoor PM2.5 concentrations can become extremely high when burning solid fuels than tobacco smoking, therefore a relatively small effect size might also partly explain why it has previously proved so difficult to establish such a relationship in this study.
The present study has several strengths. First, we used data from a nationally representative population-based survey which targeted households throughout the country. Thus, our sample size was very large, reducing potential type 2 error. Second, detailed information about potential risk factors for TB were recorded, allowing us to comprehensively adjust for confounders. Third, TB was diagnosed by laboratory test results rather than subjectively by self-report or based on a clinically-diagnosed previous history of the disease.
The present study also has some limitations worth noting. First, as with other observational studies, associations observed may be due to unmeasured confounders. However, the associations between household solid fuel use and TB reported in the present study were independent of other potential confounders such as smoking, gender, marital status, education, alcohol intake, BMI, contact with an active TB case, and previous history of TB. Second, we adopted a cross-sectional design. Data on assessed variables were obtained only at the time of recruitment, and thus the duration of risk factors and its impact to the individual’s level could not be assessed. Moreover, the exposure to solid fuel smoke from cooking and heating was self-reported, and the duration of exposure to solid fuels and concentration of pollutants in indoor settings were not measured. That said, the study team visited every household and confirmed the type of dwelling and stoves used in order to minimize recall bias.