Background

In January 2013, a persistent and hazardous dense haze episode (2013JHE) hit China, which covered 1.4 million km² and affected > 800 million people1,2. Based on measurements of 74 major cities, the daily average concentrations of particulate matter with an aerodynamic diameter were ≤ 2.5 μm (PM2.5) exceeded the updated national air quality standards of 75 µg/m3 for 69% of the days in the month, and a record-breaking daily concentration of 772 µg/m31, approaching the levels of the catastrophic London fog in 19523,4. As the most serious haze episode with record-breaking concentrations of air pollutants, duration, and scale in China, the health risks related to the 2013JHE have drawn widespread concern from the public, scientific societies, and government5,6. As in the findings from the previous serious smog episode in London and West Germany7,8, several studies, conducted mainly in Beijing and in other cities in China, showed that the rates of emergency room visits, outpatient visits, hospital admissions, and premature deaths during 2013JHE were significantly increased compared with the “non-haze” periods, and that respiratory and cardiovascular diseases were the most frequently reported adverse consequences2,4,9,10,11,12. The number of hazy days was positively correlated with the number of cases of respiratory diseases (r = 0.56) evaluated at the Beijing Emergency Center13.

In China, exposure to high levels of ambient air pollution and environmental tobacco smoke (ETS) remains a widespread public health concern14,15,16,17,18, and many studies have shown that smokers have more acute respiratory symptoms than non-smokers when exposed to the same level of smog15,16,17,18,19. However, the adverse health impact of air pollution on health may not only be associated with the level of exposure, but also mediated by perception of the pollution and the belief that the exposure is hazardous16,17,18,19,20. Air pollutants can be perceived to have a negative impact on health through olfaction and the trigeminal sensory system, which in turn may evoke protective mechanisms such as feelings of being annoyed, worried, and disgusted15,17,18,19,20, and also defense reflexes in the body in response to the chemical stimulation, such as tearing, coughing, and mucus release. A few studies have shown that persons with hypersensitivity or lower tolerance may evoke more symptoms when exposed to even weak odorous15,20,21, and non-smokers appear to be more sensitive to ETS than smokers14,15,22. Therefore, we hypothesized that non-smokers could have reported similar or even more acute respiratory symptoms than smokers during 2013JHE. All of the above studies2,4,9,10,11,12, however, have assessed the health risks of 2013JHE by retrospectively analyzing the medical records in the hospitals or mortality data with medical care service usage and death as endpoints. No study has assessed if and how 2013JHE influenced the perceived pollution, health risk perception, and respiratory symptoms or diseases among smokers and non-smokers in the communities because of a lack of data.

We experienced 2013JHE in Shenyang, Dalian, and Anshan cities located in northeast China. The average API values in January 2013 for the three cities were 175.0, 136.6, and 109.5, respectively, 1.5–2.0 times the corresponding values for the past 3 years (2010–2012). Shenyang (18–31 January 2013) had similar PM10 (270 vs. 283 µg/m3) and PM2.5 concentrations (202 vs. 230 µg/m3), but significantly higher SO2 (235 vs. 86 µg/m3) and lower NO2 concentrations (52 vs. 103 µg/m3) than Beijing (10–17 January 2013)4. We conducted a rapid cross-sectional survey among residents aimed to assess the following: (1) the perceived disturbance, irritations, respiratory symptoms, outpatient visits, and self-protective behaviors of people in the communities during 2013JHE; (2) if non-smokers are more sensitive than smokers, or if we observe the expected synthetic effects of smoking and air pollution on respiratory symptoms.

Methods

Site selection and subject recruitment

To make a rapid assessment on the perceived air pollution and prevalence of acute respiratory symptoms during 2013JHE, we conduct a rapid cross-sectional survey pertaining to general information, perceived heavy haze, protective behaviors, irritation feeling, and respiratory symptoms among community residents in three cities of Liaoning province (five districts in Shenyang, the Jinzhou district in Dalian, and the Lishan district in Anshan) between 5 and 20 February 2013 by taking advantage of the performance of the National Survey on Behavioral Risk Factors. All residential areas were included in the sampling frame, two blocks were randomly selected in each area, one building was randomly selected in each block, and all people > 18 years of age in the building were included in the survey. Of 5206 citizens, 4741 (91.07%) returned the questionnaire and 4304 were qualified and included in the final analysis.

Questionnaire survey

Cross-sectional information was obtained through a questionnaire survey, including the detailed questions on the following: (1) six questions regarding general information (gender, age, education, respiratory disease history, cigarette smoking and number of cigarettes smoked daily); (2) three questions on the perceived heavy haze in the past month (smoky and dusty air [0/1], smoky odor in the air [0/1], and increased dust and ash on the furniture, cloth and car [0/1]); (3) four questions on the protective behaviors against the heavy haze in the past month (close windows [0/1], use of a facial mask [0/1], use of an air purifier [0/1], and increased indoor cleaning frequency [0/1]); (4) three questions on irritating feelings caused by the heavy haze in the past month (throat pain [0/1], eye irritation [0/1], and skin irritation [0/1]); and (5) three questions on the occurrence of the following respiratory symptoms caused by the heavy haze in the past month (coughing [0/1], phlegm [0/1], wheezing [0/1]). With the approval of the district staff, the study interviewers made presentations at the home explaining the purpose of the study to the citizens. After obtaining signed consent forms for participation, the study staff distributed questionnaires. The questionnaires were filled out by the citizens. All questionnaire responses were recorded electronically in a database according to a standardized code and file structure.

Statistical analysis

To enhance the clarification of heavy haze, three haze-related scores were drawn and treated as a rank variable during data analysis: (1) a score combining three questions on perceived heavy haze (smoky and dusty air [0/1], smoky odor in the air [0/1], and increased dust and ash on the furniture, cloth and car [0/1]), named as the perceived air pollution score [PAPS], ranging from 0 to 3; (2) a score combining four questions on the personal protective behavior against the heavy haze last month (close windows [0/1], use of a facial mask [0/1], use of an air purifier [0/1], and increased indoor cleaning frequency [0/1]), named as the protective behavior score [PBS], ranging from 0 to 4; and (3) a score combining three questions on irritating feelings caused by the heavy haze last month (throat pain [0/1], eye irritation [0/1], and skin irritation [0/1]), named as the irritating feeling score [IFS], ranging from 0 to 3. The odds ratio (ORs) with 95% confidence intervals (95% CIs) for each respiratory symptom (coughing; phlegm; and wheezing) were calculated and multiple logistic regression to determine which variables were associated with each respiratory symptom was conducted. The variables included as potential regressors were gender, age, respiratory disease history, cigarette smoking, number of cigarettes daily, PAPS, PBS, and IFS. Any covariates that were significant at the p < 0.05 level for a given endpoint were included in the final model. To test the hypothesis that non-smokers could be more sensitive to the heavy haze and reported more irritating feelings than smokers, we performed a path analysis to test and estimate the possible causal relationships of the number of cigarettes smoked daily to the PAPS, PBS, and IFS using a structural equation modelling. The goodness-of-fit index (GFI), and comparative fit index (CFI), and root mean squared error of approximation (RMSEA) were used as model test. The goodness-of-fit was evaluated by the following criteria: GFI > 0.90; CFI > 0.90; and RMSEA < 0.0523. Results of comparisons with the p < 0.05 level were considered to represent statistically significant differences. All data analysis was performed by using SPSS18.0 (SPSS Inc., Chicago, IL, USA).

Results

Concentrations of air pollutants during 2013JHE

The API values in January 2013 for Shenyang, Dalian, and Anshan cities were 175.0, 136.6, and 109.5, respectively. Table 1 shows that the average AQI and concentrations of PM2.5, PM10, SO2, NO2, and O3 for the 11 monitoring stations in Shenyang during the periods from 18 to 31 January 2013 were 255 µg/m3, 202 µg/m3, 270 µg/m3, 235 µg/m3, 52 µg/m3, and 49 µg/m3, respectively. Figure 1 compares the average air pollution levels between Shenyang (18–31 January 2013) and Beijing (10–17 January 2013)4. Shenyang had similar PM10 (270 vs. 283 µg/m3) and PM2.5 concentrations (202 vs. 230 µg/m3), but significantly higher SO2 (235 vs. 86 µg/m3) and lower NO2 concentrations (52 vs. 103 µg/m3) than Beijing.

Table 1 The AQI and concentrations of PM2.5, PM10, SO2, NO2, and O3 (µg/m3) for 11 monitoring stations in Shenyang City during 18–31 January 2013.
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Fig. 1
figure 1

Comparison of the average air pollution levels between Shenyang (18–31 January 2013) and Beijing (10–17 January 2013) during 2013JHE4.

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The prevalence of perceived air pollution and acute respiratory symptoms during 2013JHE

Table 2 shows that 4304 adults completed the questionnaire; 49.0% were males, the average age was 47.07 ± 16.13 years, the history of a respiratory disease was 5.7%, the cigarette smoking rate was 23.2%, and the rates of 1–9, 10–19, and ≥ 20 cigarette smoked/day were 4.9%, 7.7% and 10.6%, respectively. Of the citizens, 55.6% reported smoky and dusty air, 23.5% reported a smoky smell in the air, and 15.3% reported increased ash or dust in the furniture or in the car, the rates of 1, 2 and 3 for PAPS were 43.7%, 15.5% and 6.6%, respectively. Approximately 50% citizens had taken personal protective behaviors against the heavy haze, such as using a facial mask (24.1%), closing the windows (20.1%), increasing the frequency of indoor cleaning (16.2%), and using an air purifier in the room (6.8%), the rates of 1, 2 and 3 for PBS were 36.2%, 11.4% and 2.7%, respectively. Of the citizens, 26.3% reported an irritating feeling in the throat (20.2%), eyes (11.3%), and skin (4.7%), the rates of 1, 2 and 3 for IFS were 36.2%, 11.4% and 2.7%, respectively.

The prevalence of coughing, phlegm, and wheezing was 22.9%, 6.6%, and 5.0%, respectively. The ORs for coughing, phlegm, and wheezing were all significantly elevated for those with a history of respiratory disease (OR range: 2.49–3.97) and increased significantly with the scores of PAPS (OR range: 2.29–20.15), PBS (OR range: 1.47–5.88), and IFS (OR range: 1.61–14.98). The prevalence of coughing and phlegm tended to increase significantly as the level of education increased, but not for wheezing. Compared to females, males had a significantly increased risk of experiencing phlegm (OR = 1.65, 95% CI = 1.29–2.11), while no statistically significant gender differences were observed for coughing and wheezing. Compared to individuals < 30 years of age, those > 50 years of age had a significantly elevated risk of wheezing (OR = 1.75, 95% CI = 1.10–2.77), but not statistically significant differences were found for coughing and phlegm. A similar pattern was also observed among those over 60 years of age (OR = 1.81, 95% CI = 1.14–2.87). We did not observe a significantly increased risk for cigarette smoking (0/1) and/or the number of cigarettes smoked daily.

Table 2 Odds ratios of univariable analysis for the prevalence of coughing, phlegm, and wheezing in three cities of Liaoning Province during 2013JHE.
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Table 3 shows the results of multiple analysis. A history of respiratory disease, and the PAPS and IFS were significant risk factors for all three endpoints. The ORs increased rapidly with an increase in the PAPS, and showed a clear dose-response relationship. Similar trends were also observed for PBS, with the exception of PBS and the prevalence of phlegm. Males had significantly elevated risks for coughing (OR = 1.23, 95% CI = 1.06–1.43) and phlegm (OR = 1.83, 95% CI = 1.42–2.37), and people > 50 years of age had significantly elevated risks for wheezing (OR = 1.98, 95% CI = 1.22–3.20). Smoking (0/1) and the number of cigarettes smoked daily were not included in the final model.

Table 3 Odds ratios of multiple logistic regression analysis of coughing, phlegm, and wheezing in three cities of Liaoning Province during 2013JHE.
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Table 4 shows that smokers had a significantly lower PAPS (0.87 ± 0.82 vs. 0.97 ± 0.88, p = 0.010) and PBS (0.56 ± 0.71 vs. 0.70 ± 0.80, p < 0.001) and a lower IFS, but which was not significant (0.33 ± 0.65 vs. 0.37 ± 0.70, p = 0.317), compared with non-smokers. In addition, the PAPS and PBS, but not the IFS, decreased significantly as the number of cigarettes smoked daily increased (p < 0.01).

Table 4 Comparison of the PAPS, PBS, and IFS with smoking and number of cigarette smoked/day.
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Figure 2 shows that the number of cigarettes smoked daily was negatively associated with PAPS (coefficient = − 0.064, p < 0.001) and PBS (coefficient = − 0.093, p < 0.001), but without a significant relationship with IFS. Significant associations existed between the PAPS and IFS (coefficient = 0.364, p < 0.001) and between the PAPS and PBS (coefficient = 0.086, p < 0.001). The model had a good fit (CFI = 1.00; GIF = 1.00; RMSEA < 0.001).

Fig. 2
figure 2

Path analytic mode of number of cigarettes smoked daily (NCS), perceived air pollution score (PAPS), protective behavior score (PBS), and irritating feeling score (IFS).

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The standardized path coefficients are given (*p < 0.05; **p < 0.01; ***p < 0.001). e: error.

Discussion

The average daily API values in January 2013 for Shenyang, Dalian, and Anshan cities were 1.5–2.0 times the corresponding values for the past 3 years (2010–2012). The levels of PM2.5 and PM10 for 18–31 January 2013 in Shenyang was close to the monthly mean level in January 2013 for Beijing. Specifically, 13 of 15 days had a PM2.5 concentration > 150 µg/m3 (86.7%) and the hourly peak concentration of PM2.5 reached 1000 µg/m3 in two sites, which indicated that the three cities in Liaoning province had similar record-breaking heavy particulate pollution as occurred in Beijing in January 20134. The significantly higher SO2 (235 vs. 86 µg/m3) levels in Shenyang compared with Beijing was consistent with more coal being used for central heating during the winter in Shenyang and the lower level of NO2 (52 vs. 103 µg/m3) may be related to the smaller number of automobiles in Shenyang.

To the best of our knowledge, this is the first population-based study of acute respiratory damage risk assessment during 2013JHE in China. We observed that the prolonged and severe haze episode seriously annoyed the residents, significantly increased the prevalence of respiratory symptoms and related medical care use, and evoked the self-protective behaviors. The leading irritation feelings and acute respiratory symptoms were throat pain (20.2%) and coughing (22.9%), indicating that the hazardous levels of PM2.5, PM10, and SO2, with a maximum value > 40 times the standard, predominantly influenced the upper respiratory tracts of residents. The increased irritation and respiratory symptoms in the present study were similar to the findings among people in the 2013 Southeast Asian haze episode24 and children in the 2003 southern California wildfires25, when people were exposed to extremely high levels of air pollution, although there were some differences in the content of air pollutants between urban air pollution and the smoke of wildfires burning agricultural waste. The personal protective behaviors (closing windows, facial masks, and air purifiers) and the PBS were all significant risk factors for coughing, phlegm, and wheezing, which suggests that these simple modes of protection cannot prevent or reduce the adverse health risks in serious air pollution environments. Another possibility may be that such protective actions could just be the passive responses to the irritating feelings, as shown in the path model. As expected, residents with a history of respiratory disease were more susceptible to heavy air pollution with 1.8–2.8-fold higher prevalence of coughing, phlegm, and wheezing, which is consistent with previous findings21,22.

In contrast to our expectations, we did not find a significantly increased risk of respiratory symptoms among smokers. The absence of a clear dose-response relationship between the odds ratios of respiratory symptoms and the number of cigarettes smoked per day, as well as the borderline or non-significant associations for coughing (OR = 0.89, 95% CI: 0.75–1.05) and wheezing (OR = 0.68, 95% CI: 0.47–0.98), may indicate a complex relationship between smoking status and susceptibility to haze-related respiratory symptoms. Indeed, the acute effects of 2013JHE on respiratory symptoms among non-smokers was comparable to the combined effects of smoking and haze exposure among smokers. Previous studies have shown that non-smokers appear to be more sensitive to ETS than smokers because of the physiologic adaptions of smokers as a result of long-term exposure to cigarette smoke14,15. A large cohort study from southern China also showed that non-smokers were more vulnerable to PM exposure26.

Previous studies showed that the perception or annoyance of air pollution among residents correlated well with the levels of air pollutants15,27,28,29,30, belief of exposure is potentially hazardous may generate more health symptoms compared to the belief of having positive health effects15,18,19. The significant correlation between the PAPS and IFS (r = 0.390, p < 0.001), PBS and IFS (r = 0.239, p < 0.001), and PAPS and PBS (r = 0.350, p < 0.001), as well as the significantly monotonically increasing risks of coughing, phlegm, and wheezing with increasing levels of PAPS, PBS, and IFS supported that the acute respiratory symptoms could be caused by the direct effect of the high level air pollutants during 2013JHE and also mediated by perceived pollution16,17,18,19,20,27. Perception of air pollution is predominantly based on visual and chemosensory cues and has been shown to be a good indicator of air pollution28,29 and serves as a mediator between environmental exposure and health30. The dominant substances of 2013JHE were particulate matter, SO2, NO2 and O3. In addition to evoking odor sensations31, these substances activate the chemo-somatosensory system, thus leading to throat, eye, and skin irritation, and cause acute respiratory symptoms via pulmonary and systemic inflammation and oxygenic stress32. The significantly decreased levels of PAPS and PBS with an increased number of cigarettes smoked daily, as well as the significantly negative associations between the number of cigarettes smoked daily and PAPS (coefficient = − 0.064, p < 0.001) and PBS (coefficient = − 0.093, p < 0.001) in Fig. 2 support previous findings that smokers are accustomed to high smoke exposure, decreased awareness of ambient air quality33, and tend to have a lower perceived risk of health-related problems34. An interpretation of the results from the path model is that 2013JHE directly led to perceived air pollution, acute irritating feelings and/or respiratory symptoms, and personal protective behaviors. In contrast, perceived pollution might result in stress-induced physiologic activity and thereby irritating symptoms through a top-down defense mechanism. Irritating feelings promote people to take more personal protection actions to protect themselves. Cigarette smoking may play a negatively mediating role by reducing sensitivity to perceive the hazardous exposure and health risk perception (irritating symptoms) and decreasing motivation to take protective actions because of a higher tolerance to smog17,33,34. It is necessary to assess the etiologic roles of the differences in exposure perceptions in relation to the occurrence and self-reporting of symptoms between smokers and non-smokers in further epidemiologic research.

There were several limitations of this study. First, the assessment of acute respiratory symptoms, perceived air pollution, and adverse influence may have been biased because these were all self-reported 10–20 days after 2013JHE. Second, perceived exposure may have an important role in the occurrence and reporting of symptoms. If non-smokers are more likely than smokers to perceive harm and report respiratory symptoms, the lack of data on physiological adaptation among smokers may contribute to bias in the interpretation of health risks. Third, because we did not assess the frequency, period, and quality of the personal protective behaviors, it is impossible to determine if such actions were useful or not. Fourth, The cross-sectional design of this study and the use of ambient air pollution data from central monitoring stations, rather than personal exposure measurements, may result in exposure misclassification, which limits our ability to draw causal inferences between air pollutants and respiratory symptoms. Fifth, the 4303 subjects of the assessment were selected from three districts in three cities in Liaoning province and our findings may not be generalizable to other regions in China.

Despite these limitations, our findings provide clear evidence that 2013JHE seriously annoyed people and significantly increased the prevalence of acute upper respiratory tract symptoms. Non-smokers perceived more influence of air pollution, took more protective behaviors, and reported more irritating symptoms than smokers. Non-smokers and residents with a history of respiratory diseases were the more susceptible subpopulations. The findings from residents in communities, rather than patients in the hospitals, may be generalized more broadly to other comparable populations. The lack of such studies maybe related, in part, to the logistical challenge of implementing rapid population-based studies during the heavy haze episode.

China has paid increasing attention to the improvement of air quality and enforced relevant control measures and laws to tackle pollution after 2013JHE, and significant reductions have been observed for major air pollutants (PM2.5, SO2, NO2 and CO) in recent years35. However, it is still necessary to study the efficient and useful methods to protect the population from such impacts if such heavy haze occur in the future, particularly the early warning and personal protection actions for the susceptible people.