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Particulate matter concentrations during desert dust outbreaks and daily mortality in Nicosia, Cyprus

Abstract

Ambient particulate matter (PM) has been shown to have short- and long-term effects on cardiorespiratory mortality and morbidity. Most of the risk is associated with fine PM (PM2.5); however, recent evidence suggests that desert dust outbreaks are major contributors to coarse PM (PM10–2.5) and may be associated with adverse health effects. The objective of this study was to investigate the risk of total, cardiovascular and respiratory mortality associated with PM concentrations during desert dust outbreaks. We used a time-series design to investigate the effects of PM10 on total non-trauma, cardiovascular and respiratory daily mortality in Cyprus, between 1 January 2004 and 31 December 2007. Separate PM10 effects for non-dust and dust days were fit in generalized additive Poisson models. We found a 2.43% (95% CI: 0.53, 4.37) increase in daily cardiovascular mortality associated with each 10-μg/m3 increase in PM10 concentrations on dust days. Associations for total (0.13% increase, 95% CI: −1.03, 1.30) and respiratory mortality (0.79% decrease, 95% CI: −4.69, 3.28) on dust days and all PM10 and mortality associations on non-dust days were not significant. Although further study of the exact nature of effects across different affected regions during these events is needed, this study suggests adverse cardiovascular effects associated with desert dust events.

INTRODUCTION

Particulate matter (PM) concentrations have been shown to be associated with mortality and morbidity, particularly from cardiovascular and respiratory conditions, in a body of literature that has accumulated over more than 20 years.1 Recent evidence shows that most health effects are due to the fine fraction of PM (<2.5 μm in aerodynamic diameter, PM2.5) that is produced mainly by anthropogenic industrial combustion processes and traffic.2, 3, 4, 5, 6, 7 However, there have been suggestions of effects due to the coarse fraction (2.5< diameter≤10 μm, PM10–2.5), with differing effects depending on the sources of these particles.7, 8, 9

One particle source with potential health effects, which has recently been receiving special attention, is airborne desert dust. Desert dust is considered one of the biggest contributors to natural aerosols and PM concentrations.10, 11, 12, 13 Large amounts of Saharan desert dust in particular are transported around the world, thus increasing ambient dust concentrations.14 The Sahara desert is the largest mineral dust source, producing about half of the annual mineral dust globally.15 Saharan dust contains metals that induce oxidative stress as well as biological constituents (bacteria, fungi, endotoxins and so on)16, 17, 18 implicated in various inflammatory responses; it may also be a carrier of anthropogenic pollutants.19, 20, 21

Saharan dust has been detected as far away as the Americas, with potential health effects also reported in the form of increased pediatric asthma emergency admissions in Trinidad,16, 22, 23 but regions in southern Europe are especially prone to such events.14, 21, 24 Studies examining possible health effects of these events in Europe have resulted in mixed evidence, with some studies reporting increased mortality during these events whereas other studies reporting no associations.15 In morbidity studies, Saharan dust events have been associated with increased cardiovascular hospitalizations in Nicosia, Cyprus, and increased pediatric asthma emergency admissions in Athens, Greece.25, 26 Looking specifically at mortality studies, Perez et al.27 reported an increase in daily mortality in the city of Barcelona, Spain, during Saharan dust outbreaks, whereas in the Emilia-Romagna region in Italy, Sajani et al.28 reported increased risk of respiratory mortality among the elderly during Saharan dust days but no evidence of an association with total natural and cardiovascular mortality, or effect modification by dust outbreaks on the effect of PM <10 μm in aerodynamic diameter (PM10) concentrations on mortality. Another Italian study reports stronger PM10 and PM10–2.5 effects on cardiac mortality in Rome during Saharan dust outbreaks compared with dust-free days.29

Given the mixed results on the effects of dust outbreaks on mortality, further examination of this association is warranted. In this study we evaluate the health effects of Saharan dust outbreaks in Cyprus; the island of Cyprus is located in the Eastern Mediterranean, a region highly affected by African dust intrusions that occur at higher frequency and intensity compared with the Western Mediterranean Basin and regions further to the north.15, 21 PM sources on the island evaluated during non-Saharan dust events are believed to be local mineral dust resuspended by traffic, sea salt, combustion and traffic emissions.30 We use time-series analysis to examine associations between PM10 concentrations during dust outbreaks and non-dust outbreak days on daily mortality in Nicosia, Cyprus, in the time period between January 2004 and December 2007.

METHODS

Mortality Data

Data on daily mortality were collected in Cyprus during the period between January 2004 and December 2007 from the Health Monitoring Unit of the Ministry of Health via the Cyprus Statistical Services. All-cause natural mortality was defined as all deaths excluding those due to external causes such as accidents, suicides, homicide/assault and so on (ICD10 codes S00-Z99, representing 4.8% of all deaths in the district of Nicosia during the study period). Cardiovascular deaths were defined as ICD10 codes I00-I52 and respiratory deaths ICD10 codes J00-J99. Data on age, sex and district of residence were also available. Deaths were restricted to residents of the district of Nicosia.

Air Pollution Data

Data on air pollutant concentrations were obtained from the Air Quality Section of the Department of Labor Inspection (DLI) of the Cyprus Ministry of Labor and Social Insurance. Hourly concentrations of PM10 and O3 were available from two ambient air quality monitoring stations: (1) a traffic representative urban station located centrally in the city of Nicosia and (2): a rural background level station in the village of Ayia Marina, 40 km southwest of Nicosia. Hourly measurements of NO2, NOx, SO2 and CO were available from the urban station. Data from the urban station were used in the mortality models, whereas data from the rural station were used in the classification of dust days in a sensitivity analysis step. Particle monitoring was performed with TEOM (tapered element oscillating microbalance), O3 with UV absorption, SO2 with UV fluorescence, NOx with chemiluminescence and CO with infrared absorption. The 24-h average pollutant concentrations using the hourly measurements were calculated for all days with at least 12 hourly observations.

Meteorological Data

Daily average, minimum and maximum air temperature and relative humidity measurements were obtained from the meteorological station in closest proximity to the relevant urban air quality monitoring station from the Cyprus Meteorological Services.

Dust Days

Dust storms lasting 1–5 days originating primarily from the Sahara Desert affect the island of Cyprus. PM10 concentrations can reach daily concentrations of >250 μg/m3 during these events. Dust outbreaks are reported by the Meteorological Services as days with poor visibility due to “dust in suspension” in contrast to reports of “hazy” conditions or “locally resuspended dust”. In addition, the Barcelona Super Computer Dust REgional Atmospheric Model (BSC-DREAM)31 provides daily indicators of air masses with elevated eroded desert dust concentrations in the Southern Europe and Mediterranean region. We defined dust days as days with both (1) reported “dust in suspension” at the Larnaca International Airport meteorological station, and (2) an indication of an air mass with desert dust from the BSC-DREAM dust maps. For sensitivity analysis, days that were not reported by the Meteorological Services, but with elevated eroded desert dust concentrations as indicated by BSC-DREAM, were also considered as dust days if during these days daily average concentrations at the rural station were at least 50% of the concentrations at the urban station according to previous practice.27

Statistical Analysis

We used Poisson regression models to investigate the association between the 24-h PM10 concentrations and daily mortality with all days considered together and for dust and non-dust days considered separately. For the latter, PM10 was modeled as a linear term plus an interaction with an indicator for dust days. Separate models were considered for total natural daily mortality, cardiovascular mortality and respiratory mortality.

We used generalized additive models (GAM) with penalized cubic splines for time (5 degrees of freedom per year), temperature and relative humidity (4 degrees of freedom each), indicators for day of the week as a categorical variable (0–6, Sunday being the referent day), whereas daily average concentrations of co-pollutants (O3, NO2, NOx, SO2 and CO) were considered in single-pollutant exposure models and also one at a time as potential confounders in the PM models. We also lagged the PM10 and PM10 and dust day interaction effects by 1 and 2 days. Finally, a model with a simple indicator variable for dust days as opposed to the PM10 concentration terms was also considered. We assumed a quasipoisson distribution rather than simple Poisson to account for overdispersion in the daily mortality counts. Statistical analyses were performed using R software (version R 2.15.0)

RESULTS

There were on average 5.1 natural-cause deaths per day (SD 2.5). Mean daily cardiovascular mortality was 1.46 deaths and respiratory mortality was 0.41 (Table 1). Twelve days were excluded because of lack of sufficient PM10 hourly observations. One day with extreme PM10 concentrations (24-h average concentration of 1400 μg/m3) was also excluded. The mean 24-h average PM10 concentration in the restricted data set was 54.7±25.3 μg/m3 with an IQR of 24.0 μg/m3 (53.0 μg/m3, IQR=22.8 μg/m3 and 114.9 μg/m3, IQR=108.2 μg/m3 on non-dust days and dust days, respectively). There were 39 dust days in the 4-year period (Table 1). PM10 concentrations from the urban monitoring station across the study period are illustrated in Figure 1.

Table 1 Summary statistics for the district of Nicosia, Cyprus, during the study period of 1 January 2004 to 31 December 2007.
Figure 1
figure1

The 24-h average PM10 concentrations from the urban monitoring station across the study period, with dust days highlighted in red. The additional days used in the sensitivity analysis are in orange.

The percent change in mortality associated with PM10 concentrations by dust versus non-dust days and adjusting for long- and short-term time trends and weather variables are summarized in Table 2. In all days, irrespective of dust presence, there was a 1.62% increase in daily cardiovascular mortality (95% CI: −0.17, 3.44) with each 10 μg/m3 increase in PM10 concentrations, which was not statistically significant. There was no apparent association with total or respiratory mortality.

Table 2 Percent change in daily mortality (95% CI) associated with a 10 μg/m3 increase in PM10 concentrations for the district of Nicosia, Cyprus, during the study period.a

When we considered the effect of PM10 concentrations on mortality separately for dust and non-dust days, we did not observe an association between PM10 and total or cause-specific mortality on non-dust days. However, we found a 2.43% increase (95% CI: 0.53, 4.37) in cardiovascular mortality associated with each 10 μg/m3 increase in PM10 concentrations on dust days. When considering a simple indicator variable for dust days without PM in the model, we observed a suggestive association with cardiovascular mortality with a 27.8% (95% CI: −0.6, 64.2) increase associated with dust days compared with non-dust days, but no significant change in total and respiratory mortality.

Adjusting for co-pollutants did not alter results nor did any statistically significant associations appear between co-pollutants and mortality; therefore, all results presented in this study are from single-pollutant models. There was a suggestive increase in total (0.9% increase; 95% CI: −0.3, 2.1) and cardiovascular mortality (2.1% increase; 95% CI: −0.3, 4.6) associated with each p.p.b. increase in SO2 concentrations.

Exposure response curves for the effect of PM10 on total and cardiovascular mortality by dust versus non-dust days are presented in Figure 2. The curves were produced in models identical to the ones used in the main analysis using penalized cubic splines for PM10 instead of linear terms.

Figure 2
figure2

Penalized spline terms (d.f.=3) for the PM10 effect on cardiovascular mortality for dust days (left, P=0.012) and non-dust days (P=0.062).

Associations for total, cardiovascular mortality and respiratory mortality with the exposure lagged 0, 1 and 2 days with a different PM10 effect for dust and non-dust days as in the main model are illustrated in Figure 3. The effect of PM10 on non-dust days on total and cardiovascular mortality increases slightly with a 1-day lag of exposure, whereas the association between PM10 on dust days and cardiovascular mortality decreased steadily with each lag day. None of these findings were statistically significant.

Figure 3
figure3

Percent changes (with 95% CI bars) of all-cause, cardiovascular and respiratory daily mortality associated with a 10 μg/m3 increase in PM10 concentrations for same day (0), and 1- and 2-day exposure lags, for non-dust days (A) and dust days (B).

For the sensitivity analysis of a broader definition of dust days, 56 days were identified with mean PM10 concentrations at 52.2 μg/m3 and 116.6 μg/m3 on non-dust and dust days, respectively. The association between PM10 concentrations on dust days and cardiovascular mortality in this analysis was somewhat attenuated. As with the main analysis, a significant increase in cardiovascular mortality associated with PM10 concentrations only on dust days was the main observation. The magnitude of the increase was 1.94% (95% CI: 0.10, 3.81).

DISCUSSION

We observed an association between daily cardiovascular mortality and short-term exposure to PM10 during dust days, specifically a 2.43% increase in daily cardiovascular mortality associated with each 10 μg/m3 increase in PM10 concentrations but no associations during non-dust days. No associations were observed for total and respiratory mortality; the power of the study to detect more modest effects was limited though. Associations (although not statistically significant) between cardiovascular mortality and PM10 concentrations during all days irrespective of dust presence seem to be mostly driven by dust days. This may add to the significance of the health effects of these events and potentially influence our approach of assessing health effects of air pollution in general.

Studies of the health effects of transported desert dust have been few, and evidence is conflicting. A study in Spokane, Washington, examining episodes of high coarse (but not fine) particle concentrations identified as dust storms reports no association between high coarse particle concentrations and increased mortality.32 Some more recent studies from Taiwan, Korea and Japan were suggestive of a moderate increase in total and cardiovascular mortality associated with Asian Dust Storms (ADS), but not all studies had statistically significant findings.33, 34, 35, 36 Increased mortality associated with dust storms has also been reported in Australia,37 but source heterogeneity may also limit our ability to compare effects with Saharan dust outbreaks.

The Barcelona, Emilia-Romagna and Rome27, 28, 29 studies look specifically at Saharan desert dust outbreaks and mortality in southern Europe. In Emilia-Romagna, the investigators observed a more substantial respiratory association whereas we saw a stronger association for cardiovascular mortality, as was the case in the Rome study. A subsequent analysis of the Barcelona data, with a source apportionment method incorporated in the analysis, also yielded a larger cardiovascular mortality effect of PM10 during Saharan dust compared with non-Saharan dust days, with greater effects for anthropogenic particulates during dust days also present during these outbreaks. According to the authors, this may suggest that effects seen during these events may be due to the increase in the effect of anthropogenic particles.38

Different exposure characteristics led to a slightly different analysis model in the current study. Mean PM10 concentrations on all days during the study period were slightly higher in Nicosia than in the previous studies (mean daily concentrations of 55 μg/m3 compared with 40 μg/m3). In Barcelona and Emilia-Romagna, the PM10 (and PM2.5 when considered) concentrations were similar on dust days and non-dust days, whereas in Nicosia there were dramatic increases in PM10 levels on days with reported dust outbreaks, and less dramatic increases in PM10 were seen in the Rome data during these outbreaks.

The nature of the statistical model used in the present study (two separate linear terms for PM10 effect for dust and non-dust days, respectively) suggests a different association with PM10 for each scenario. Given the differences in PM10 concentrations between dust and non-dust days, an exponential dose-response relationship or the presence of a threshold potentially could yield similar results as true different slopes. However, the spline term for dust days indicates that the relationship is indeed linear, which suggests that the difference in association is primarily due to some change in composition because of the different source of PM. The spline term for non-dust days indicates that even at higher concentrations of PM there does not seem to be an increase in mortality associated with increased PM concentrations on non-dust days, but this association seems unstable at higher concentrations because of the small number of observations. A linear relationship is in agreement with previous findings suggesting roughly linear relationships between ambient PM and total and cardiovascular mortality.39

We found no evidence of lagged effects, indicating that the association of PM10 during dust days is short-lived and does not extend past the day of exposure. Previous evidence regarding general ambient PM10 exposure and mortality associations indicate that cardiovascular effects seem to be more strongly related with same-day exposures but that there are also short-term effects 1 to 2 days after exposure in all-cause, cardiovascular and respiratory mortality.40, 41 There was an indication of an increasing effect of PM10 when lagged for 1 day on total and cardiovascular mortality for non-dust days, although this association was not statistically significant.

Evidence from the literature regarding possible lagged effects of these specific events is rather inconsistent. We only observed a significant association between PM10 and cardiovascular mortality at lag zero, whereas the highest effect on mortality in Barcelona is reported at lag one,27, 38 and more lagged effect structures are reported in the Rome study.29 A wide variety of lags and moving averages are reported in the literature about dust effects outside of Southern Europe as well,33, 34, 36, 37 although it is worth mentioning that differences in primary outcomes and exposure sources may result in not directly comparable studies. A distributed lag model taking into account the varying durations of these events could be the most appropriate way to examine for any potential lagged effects, but we lacked the power to perform such an analysis.

Additional limitations in this study existed that hindered further examination of the associations between desert dust and mortality. Information on fine PM fraction (PM2.5) was not available for most of the duration of the study period, and hence separate associations for the fine and coarse fraction of PM could not be examined. Saharan dust events have been shown to be associated with elevated concentrations of both the fine and coarse fraction as reported in the Barcelona study,27 and dust storm effects on PM2.5 have also been documented elsewhere.13, 21, 42 A possible separate effect of fine and coarse fraction could provide further insight into the mechanism of action as concentrations of chemical and biological components differ between fractions, leading to different effects and underlying mechanisms.43, 44

Information on chemical and biological constituents was lacking that prevented examination of dust components with possible greater effects. Possible misclassification of dust days is a major limitation of the study but steps were taken to account for this. The broader definition used in a sensitivity analysis step showed somewhat attenuated effects, indicating that there was no association in the additional days under this definition. Limitations of using ambient air pollution concentrations as the exposure of interest have been documented elsewhere,45 and any misclassification of cause of death, if present, would not be related to air pollution concentrations or presence of desert dust.

Our power was limited because of the small number of daily deaths, especially when cause-specific mortality was considered. We were also unable to assess effects within specific age groups, which have been shown to be more prone to certain effects of air pollution.46, 47 However, despite the limitations due to the restricted sample size, results from studies in cities with smaller populations such as Nicosia can add to the literature as small-city characteristics may contribute to heterogeneity of effect in addition to differences in effect because of differences in pollution sources, latitude and climate characteristics.

A more detailed exposure assessment approach with data on chemical and biological constituents and source composition as well as separation of potential differences in fine and coarse particle effects during desert dust events on cause-specific mortality would help in a better understanding of the possible health effects of such events and their underlying mechanisms. Additionally, larger studies with possible incorporation of multiple affected sites may be useful (after accounting for sources of heterogeneity in exposure and health effects). Although these desert dust outbreaks are natural, non-preventable events, a better understanding of their possible effects and increased awareness may still prevent adverse health effects, and the current findings could aid in this. Despite the study limitations, the significant findings as well as the indications of a linear dose-response curve may be useful in future evaluations of such events.

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Acknowledgements

We acknowledge the A.G. Leventis Foundation for financial assistance and the HSPH Cyprus Initiative under which the project was developed.

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Correspondence to Andreas M Neophytou.

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Neophytou, A., Yiallouros, P., Coull, B. et al. Particulate matter concentrations during desert dust outbreaks and daily mortality in Nicosia, Cyprus. J Expo Sci Environ Epidemiol 23, 275–280 (2013). https://doi.org/10.1038/jes.2013.10

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Keywords

  • particulate matter
  • desert dust
  • cardiovascular mortality
  • time series

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