Abstract
Conjunctivitis is a common multifactorial inflammatory ocular surface disease characterized by symptoms such as congestion, edema, and increased secretion of conjunctival tissue, and the potential effects of meteorological factors as well as extreme meteorological factors on conjunctivitis and their lagging effects have not been fully evaluated. We obtained the electronic case information of 59,731 outpatients with conjunctivitis from the Ophthalmology Department of the First Affiliated Hospital of **njiang Medical University (Urumqi, **njiang, China) for the period from January 1, 2013, to December 31, 2020. Meteorological data for daily mean temperature (°C), daily relative humidity (%), daily average wind speed (m/s), and atmospheric pressure (hPa) were obtained from the China Meteorological Data Sharing Service. The air pollutant data were obtained from 11 standard urban background fixed air quality monitors. A time-series analysis design and a quasi-Poisson generalized linear regression model combined with a distributed lagged nonlinear model (DLNM) were used to fit the effects of exposure to different meteorological factors and extreme weather on conjunctivitis outpatient visits. Subgroup analyses were performed on gender, age and season, and type of conjunctivitis. Univariate and multifactorial model results indicated that each 10-unit increase in mean temperature and relative humidity was associated with an increased risk of conjunctivitis outpatient visits, while each 10-unit increase in atmospheric pressure was associated with a decreased risk. The results of the extreme weather analysis suggested that extremely low levels of atmospheric pressure and relative humidity as well as extreme levels of temperature were associated with an increased risk of outpatient conjunctivitis visits, and extreme wind speeds were associated with a decreased risk. The results of the subgroup analysis suggested gender, age, and seasonal differences. We conducted the first large sample size time-series analysis in the large city furthest from the ocean in the world and confirmed for the first time that elevated mean temperature and extreme low levels of relative humidity in Urumqi were risk factors for local conjunctivitis outpatient visits, while elevated atmospheric pressure and extreme low levels of wind speed were protective factors, and there were lagged effects of temperature and atmospheric pressure. Multicenter studies with larger sample sizes are needed.
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Introduction
Meteorological factors including temperature, humidity, wind speed, air pressure, and many other factors are closely related to human health (Liang and Gong 2017). In recent years, severe climate change such as global weather events with extreme surface temperatures has become more frequent and intense, taking the experience of the 2003 European summer heat wave as an example, which directly caused 44,000 additional deaths (Tobias et al. 2012). Severe meteorological (climate) changes are expected to continue to dominate the world in the coming decades (Peters et al. 2022). With the massive use of fossil fuels and modern industrial development leading to unstable climate change, there is growing concern about the direct impact of a range of extreme weather-related events on public health, such as temperature, humidity, or rainfall, which have been identified as risk factors for the spread of some common clinical diseases such as malaria (Ninphanomchai et al. 2014), childhood diarrhea (Bradatan et al. 2020), and COVID-19 (Zhang et al. 2020). In contrast, the risk of develo** eye surface problems such as conjunctivitis, keratitis, and dry eye disease, which are directly exposed to air (Zhang et al. 2021; Mandell et al. 2020), may be influenced by environmental meteorological factors such as temperature. The ocular surface can be affected by direct physical and chemical stimuli caused by meteorological factors, such as temperature (Craig et al. 2000), humidity (Cekic et al. 2002), and ultraviolet radiation (Zuclich and Connolly 1976), which contribute to the induction of oxidative stress and inflammation in the ocular surface and ultimately lead to imbalance and dysfunction of the intraocular environment and corresponding diseases. But the number of available relevant studies is very limited, and further detailed research is urgently needed.
Conjunctivitis is an inflammatory disease of the conjunctival tissues and is one of the most common ophthalmic diseases, which manifests clinically with increased discharge, conjunctival congestion, photophobia, and itchy sensations. The conjunctiva is directly exposed to the air and is therefore susceptible to immune inflammatory reactions due to exposure to environmental particles or allergens. Conjunctivitis significantly affects the patient physically and psychologically with a significant loss of quality of life (Zhang et al. 2017, 2021). In the USA, outpatient visits for conjunctivitis account for 1/3 of annual visits for ophthalmology-related diseases, while data from the Chinese Center for Disease Control and Prevention suggest that conjunctivitis cases in China are also increasing annually, with allergic conjunctivitis patients alone increasing by 0.3% in 2020 compared to the previous year, reaching 295 million (Azari and Barney 2013). According to an emergency ophthalmology study in the USA, the economic burden of eye diseases in emergency room visits is estimated at $2 billion per year, with conjunctivitis alone accounting for 28% of the total (Channa et al. 2016). Therefore, it has become a public health problem that cannot be ignored (epidemiology of eye-related emergency department visits). As a multicausal disease, numerous risk factors for conjunctivitis, such as pollen (Sheng et al. 2022), air pollutants (Nucci et al. 2017), and dust (Chien et al. 2014), have been shown to be associated with the risk of conjunctivitis. The impact of changes in ambient environmental conditions including temperature, humidity, and atmospheric pressure on conjunctivitis has received insufficient attention, but a series of recent studies have confirmed that multiple meteorological factors may be associated with the risk of conjunctivitis while showing potential lagged effects and geographic variation (Zhang et al. 2021; Patel et al. 2021), but the number of relevant studies remains limited. In addition, except for a few types such as allergic conjunctivitis, most other different types of conjunctivitis have not been studied in detail.
Urumqi is one of the most economically developed large cities in Northwest China and the capital of the ** of the four seasons suggests that the effects of relative humidity, atmospheric pressure, and wind speed exhibit seasonal differences, with the most significant effects mainly in summer and winter (Table 4).
The relationship between different types of conjunctivitis and different meteorological factors varies. Specifically, our results suggest that acute conjunctivitis is only associated with atmospheric pressure (RR = 1.147). However, in chronic conjunctivitis, the increase in atmospheric pressure showed exactly the opposite effect (RR = 0.728), like the relative humidity (RR = 0.728). Allergic conjunctivitis showed a significant correlation with an increase in mean temperature and relative humidity (RR = 1.216 and 1.553), but there was a significant correlation between increased wind speed and decreased outpatient visits for allergic conjunctivitis (RR = 0.220). In addition, follicular conjunctivitis showed significant correlations with increases in relative humidity and atmospheric pressure (RR = 0.855 and 4.037), and nonspecific conjunctivitis showed significant correlations with increases in mean temperature (RR = 1.076) (Table 4).
The effect of extreme weather is demonstrated in Table 5, where the results show that low levels of atmospheric pressure (for P1 RR = 1.092, for P5 RR = 1.055, for P10 RR = 1.040) and relative humidity (for P1 RR = 1.123, for P5 RR = 1.084, for P10 RR = 1.067) increase the risk of conjunctivitis outpatient visits and the effect increased with the decreasing levels. Extreme high levels of mean temperature were statistically correlated with increased outpatient visits for conjunctivitis and this effect increased progressively with increasing mean temperature (for P90 RR = 1.112, for P95 RR = 1.135, and for P99 RR = 1.164). Extreme wind speed demonstrated the protective effect on outpatient visits for conjunctivitis, which increased with decreasing wind speed levels under very low levels, and the protective effect was strongest at extremely low wind speeds (for P1 RR = 0.954). The results were similar under single meteorological factor as well as multimeteorological factor models.
In addition, we also investigated the relationship between six major air pollutants and conjunctivitis outpatient visits in Urumqi from January 1, 2013, to December 31, 2020. The results of single-pollutant and multipollutant models suggested that PM2.5, O3, and SO2 did not show significant correlations with conjunctivitis outpatient visits, and PM10 (RR = 1.004–1.005), NO2 (RR = 1.019–1.046) and CO (RR = 0.981) showed weak correlations with conjunctivitis outpatient visits in Urumqi. The results of single-lag and cumulative-lags are shown in Supplementary Material A, Table S1-2. Overall, these results suggest that there may be little significant substantial correlation between air pollution and local conjunctivitis outpatient visits in Urumqi.
Discussion
Conjunctivitis can affect people of all ages and genders, imposing a significant economic burden and severely diminishing the ability of patients to learn and work effectively. Approximately 15–40% of the population in developed countries experience a reduced quality of life from conjunctivitis (Pitt et al. 2004), for example, 3–6 million people suffer from conjunctivitis each year in the USA, with acute conjunctivitis comprising the largest number (Ramirez et al. 2017; Azari and Barney 2013). A report from Hangzhou, China, indicates that the average cost of examination and treatment of conjunctivitis is estimated to total about $30 per case (Fu et al. 2017), and similar conditions exist in other develo** countries.
Urumqi is in the hinterland of the Eurasian continent and is the world’s farthest city from the ocean, nicknamed the “Capital of Asia,” and is an important gateway for China's economic development to the west as the second bridgehead of the Asia–Europe Continental Bridge in western China. Until 2021, it has a permanent population of 4.07 million and is the main transportation route and local political, economic, cultural, technological, educational, and transportation center in Northwest China. In recent decades, the local economy and society have developed rapidly, so more and more people have begun to pay attention to the impact of local environmental factors such as extreme meteorological factors on health problems. As the most inland city in the world and the farthest from the ocean and coastline (2500 km), Urumqi located in the hinterland of Eurasia, the northern foot of the Tianshan Mountains, southern Junggar Basin, covers an area of 12,000 km2 and has a vast mountainous area that blocks ocean water vapor from reaching the city, so the climate is arid throughout the year, showing typical characteristics of a temperate continental arid climate, with the hottest months being July and August (mean temperature 25.7 °C) and the coldest month being January (mean temperature − 15.2 °C) (Hu et al. 2018). Spring and autumn are short in duration while winter and summer are long. Due to drought and other factors resulting in less surface cover vegetation, the Urumqi region is highly susceptible to windy weather and the formation of dust storms in the downstream region by affecting the exposed surface dust source sites, which not only causes meteorological disasters for agricultural production and transportation in the ** of the four seasons could see relative humidity and air pressure as risk factors for conjunctivitis in summer as well as in winter, while wind speed is a protective factor similar to previous results, which may be related to the fact that elevated temperature and humidity provide a suitable environment for bacteria and allergens to live (Stockmann et al. 2013).
In addition, further ty** of the types of conjunctivitis revealed that the effects of different meteorological factors differed. Weather conditions are known to induce and exacerbate allergic diseases such as allergic conjunctivitis, through the interplay of pollen and air pollutants (McMichael et al. 2006). Our findings similarly confirm that the increase in outpatient visits for allergic conjunctivitis in the Urumqi region was statistically significantly correlated with an increase in mean air temperature as well as relative humidity, while increased wind speed exhibited the opposite effect, similar to the results of a time-series study on allergic conjunctivitis published by Jiaxu Hong et al. in 2016, which may be related to the availability of allergens of suitable temperature and humidity conditions as well as airborne routes (Hong et al. 2016). Contrary to the effect of increased atmospheric pressure on acute conjunctivitis versus chronic conjunctivitis, a study based on a Taiwanese population published by Chun-Chi Chiang et al. in 2012 suggested that chronic conjunctivitis is characterized by two peaks in incidence per year compared to acute conjunctivitis (Chiang et al. 2012), especially during the warmer months, which may indicate seasonal and environmental variations associated with the etiology of the chronic course, thus producing different responses to different meteorological factors.
There is no consensus on the exact mechanism of action of meteorological factors on the development of conjunctivitis. However, in recent years, with the increase in climate change and the frequency of extreme weather times, more and more attention has been paid to the relationship between meteorological factors and disease, and many studies have revealed that meteorological factors such as temperature and air pollutants could exert some influence on human health, especially the extreme weather effects are stronger (Rocque et al. 2021). Air pollutants have been widely recognized as an important risk factor for the development of conjunctivitis, and several previous studies have shown that meteorological factors modulate the local concentrations and effects of air pollutants and indirectly play a role (Fu et al. 2017; Lu et al. 2019). A study published by Iny Jhun et al. in 2014 suggested that the association between ozone and mortality in 97 US cities becomes stronger in hotter and colder environments (Jhun et al. 2014). In addition, high wind speed can promote the dispersion of outdoor particulate matter (including pollen and mold spores) and thus reduce its concentration, and high temperature and solar radiation can increase the effect of photosynthesis on ozone and thus affect the development of allergic diseases (e.g., eczema, allergic conjunctivitis) (Novaes et al. 2010), and our correlation analysis also confirmed this, suggesting a correlation between mean temperature and relative humidity and ozone in Urumqi (r = 0.81 and − 0.72, p-value < 0.001). In addition, inflammatory cell activity may be elevated in high-temperature environments, leading to inflammation in the eye, especially the ocular surface and possibly playing a role in the development of conjunctivitis (Chen et al. 2018). In addition to acting on the inflammatory response, low temperatures can also affect the function of the ocular surface and related diseases by modulating the level of oxidative stress in concert with air pollutants (Duan et al. 2019). Variations in temperature as well as air pressure are not only directly related to the stability of the tear film, affecting the lubricating and protective capacity of the eye (Mandell et al. 2020), but also can further directly induce the development of conjunctivitis through ocular surface dynamics (Abusharha et al. 2016). In addition, changes in temperature, wind speed, air pressure, and humidity can affect not only the concentration, distribution, and composition of particulate matter and gaseous pollutants, but also evaporation from the surface, thereby affecting the concentration and transmission of airborne allergens such as pollen (D’Amato and Cecchi 2008), of which pollen sensitivity is widely considered to be the most common factor in allergic conjunctivitis, and the association may vary with the seasonality of meteorological factors leading to seasonal changes in conjunctivitis outpatient visits (Leonardi et al. 2015).
A growing number of studies in recent years have shown that many human health problems, including ocular surface diseases, may be adversely affected by changes in weather patterns, especially extreme meteorological factors (Lu et al. 2019). The effects of weather factors on neurodegenerative pathologies (Bongioanni et al. 2021), cardiovascular system diseases (Khraishah et al. 2022), and some infectious diseases (Williams et al. 2021) have been extensively studied, but there are still fewer studies on the effects of direct exposure to the environment on ocular surface diseases. In a nationwide, population‐based, cross‐sectional study, Lee et al. found that patients with allergic conjunctivitis had increased incidence in May (spring), September (autumn), and the valley in winter (Lee et al. 2020). However, data from a case-crossover study between the years 2009 and 2014 conducted by Khalaila et al. suggested that patients for conjunctivitis increased during summer and autumn, excluding spring and winter (Khalaila et al. 2021). In addition, a study based on the population in Northeast China, between the years 2014 and 2018, showed that with the increase in temperature and the decrease in humidity, allergic conjunctivitis appears to increase significantly, indicating dry and hot climate is likely to induce allergic conjunctivitis (Lu et al. 2021). It is interesting that long-term exposure to higher mean temperature and relative humidity were associated with an increased risk of acute hemorrhagic conjunctivitis in a study by Zhang et al. (2021). Similarly, in another major study, Seo et al. demonstrated that the number of conjunctivitis outpatients was elevated with higher exposure to temperature and humidity (Seo et al. 2018) Conversely, Sheng et al. published a time-series analysis in 2022, which indicated that there was a negative correlation between temperature and allergic conjunctivitis visits (Sheng et al. 2022). Our results showed that increased mean temperature and extremely low levels of relative humidity in Urumqi were significantly associated with increased local conjunctivitis outpatient visits, while increased atmospheric pressure and extremely low levels of wind speed were significantly associated with decreased local conjunctivitis outpatient visits. In addition, the dose effect of local temperature and conjunctivitis risks showed a “U”-shaped curve, suggesting that extreme levels (very high or very low) of temperature conditions are also risk factors for conjunctivitis. These results suggest that the relationship between meteorological factors and conjunctivitis visits is different in Urumqi than in other regions, which may be related to its unique geographical location and social development pattern (Ren et al. 2022) (Yao et al. 2018).
Our study has several advantages. First, this is the first large-scale time-series analysis study with a long-time span in a large city farthest from the ocean in the world and is the first exploratory investigation of local meteorological factors and the correlation between extreme weather and conjunctivitis clinic visits in Urumqi, which is the largest city in northwest China. Second, our study provides new evidence in this field, confirming for the first time that mean temperature and extremely low levels of relative humidity in Urumqi are risk factors for conjunctivitis, while elevated air pressure and extremely low levels of wind speed are protective factors for conjunctivitis, and suggesting the potential lag effect of mean temperature and air pressure. Third, we further distinguished specific types of conjunctivitis and as comprehensively as possible investigated different meteorological factors and exposure to extreme weather in relation to the outpatient risk of specific types of conjunctivitis and performed subgroup analyses to detect differences in the effects of gender, age, and cold and warm as well as seasonal factors in local conjunctivitis patients in Urumqi.
It is undeniable that our study still has some limitations. First, although the Ophthalmology Department of the First Affiliated Hospital of **njiang Medical University, the largest and most modern ophthalmology clinic in the region, which attracts more than 50% of dry eye patients to outpatient clinics, is the preferred medical institution for patients with ophthalmic disease in the surrounding area; it is important to consider patients who are missed due to proximity or other reasons for visiting other hospitals. Second, although we used screening procedures to retain patients living in the main local area as much as possible to ensure that the screening results were closest to the patient’s residence at the monitoring station, individual-level exposure and indoor pollution were still inevitably omitted that could lead to errors in the results. Third, individual characteristics of study subjects such as whether they smoked and drank alcohol, underlying disease states, and household income were not available in the electronic medical records, which prevented us from further analysis of individual differences. Fourth, in addition to the main meteorological factors we studied, other meteorological factors, such as rainfall and duration of UV exposure, may have potential effects on the ocular surface and were not considered. Future multicenter epidemiological studies with larger sample sizes and longer span of periods are still needed.
Conclusion
Overall, we conducted the first time-series analysis of a large sample size covering 59,731 conjunctivitis patients in Urumqi, the farthest from the ocean in the world and the largest city in northwest China (**njiang), from January 1, 2013, to December 31, 2020. The association of four major meteorological factors with conjunctivitis outpatient clinics in the region and the lagged effects was revealed by constructing single meteorological factor as well as multimeteorological factor models. We demonstrated for the first time that elevated mean temperature and extremely low relative humidity in Urumqi were risk factors for local conjunctivitis outpatient visits, while elevated atmospheric pressure and extremely low wind speed were protective factors significantly associated with decreased local conjunctivitis risks. In addition, we revealed the U-shaped and inverted U-shaped curves for the dose–response of local temperature and atmospheric pressure on conjunctivitis outpatient visits, with extreme levels (very high or very low) of temperature conditions and extremely low levels of atmospheric pressure also being risk factors for conjunctivitis, providing new evidence in this area of research. Subgroup analysis results suggest that the impact of meteorological factors on conjunctivitis is influenced by gender, age, and seasonal differences. Considering the significant economic burden of conjunctivitis and the impact on the quality of patients’ lives, meteorological factors, especially extreme weather, are strongly associated with the risk of conjunctivitis, which requires larger sample sizes and multicenter epidemiological studies spanning longer periods.
Data availability
Access to any dataset used can be obtained by contacting the corresponding author.
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Funding
This study was supported by Key Projects of Natural Science Research of Anhui Provincial Department of Education (KJ2020A0163) and National Natural Science Foundation of China (82070986, 82171043).
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Si-Yu Gui, Jiao-Chao Qiao, and **n-Cheng Wang wrote the main manuscript text; Fan Yang and Jian-Chao Qiao prepared figures and tables. All authors reviewed the manuscript. Fang-Biao Tao revised the manuscript and provided methodological support, **ang-Long Yi provided data and revised the manuscript, and Zheng-Xuan Jiang reviewed and revised the manuscript.
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The Medical Ethics Committee of the First Affiliated Hospital of **njiang Medical University approved and supervised the whole process of the study, and the process was conducted in accordance with the Declaration of Helsinki (No. K202205-08).
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Gui, SY., Qiao, JC., Wang, XC. et al. Long-term effects of meteorological factors and extreme weather on daily outpatient visits for conjunctivitis from 2013 to 2020: a time-series study in Urumqi, China. Environ Sci Pollut Res 30, 58041–58057 (2023). https://doi.org/10.1007/s11356-023-26335-4
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DOI: https://doi.org/10.1007/s11356-023-26335-4