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Original Investigation |

Potential Importance of Ozone in the Association Between Outdoor Air Pollution and Dry Eye Disease in South Korea

Sung Ha Hwang, MD1; Yoon-Hyeong Choi, PhD2; Hae Jung Paik, MD, PhD1; Won Ryang Wee, MD, PhD3; Mee Kum Kim, MD, PhD3; Dong Hyun Kim, MD1
[+] Author Affiliations
1Department of Ophthalmology, Gachon University Gil Medical Center, Incheon, Korea
2Department of Preventive Medicine, Gachon University College of Medicine, Incheon, Korea
3Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea
JAMA Ophthalmol. 2016;134(5):503-510. doi:10.1001/jamaophthalmol.2016.0139.
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Importance  Air pollution is an important public health concern and the ocular surface is continuously exposed to pollutants in outdoor air. Ocular surface abnormalities related to air pollution are thought to be a subtype of dry eye disease (DED). However, to date, there is no large-scale study evaluating an association between air pollution and DED that includes multiple air pollutants.

Objective  To investigate associations between outdoor air pollution and DED in a Korean population.

Design, Setting, and Participants  A population-based cross-sectional study using data on 16 824 participants in the fifth Korea National Health and Nutrition Examination Survey was conducted from January 1, 2010, to December 31, 2012. Data analysis was conducted from September 1 to 30, 2015. Dry eye disease was defined as previously diagnosed by an ophthalmologist or the presence of frequent ocular pain and discomfort. Outdoor air pollution measurements (mean annual humidity, particulate matter with aerodynamic diameter <10 µm [PM10], ozone, and nitrogen dioxide levels) were collected from 283 national monitoring stations in South Korea.

Main Outcomes and Measures  Associations of multiple air pollutants with DED were assessed from multivariable logistic regression analyses. Sociodemographic factors and previously known factors associated with DED were applied as covariates (model 1 controlled for sociodemographic factors and model 2 controlled for sociodemographic, behavioral, and clinical factors).

Results  Among 16 824 participants (7104 men and 9720 women), higher ozone levels and lower humidity levels were significantly associated with symptoms and diagnosis of DED. In model 1, an increase in ozone levels of 0.003 ppm was significantly associated with symptoms and diagnosis of DED (symptoms: odds ratio [OR], 1.16; 95% CI, 1.02-1.30; P = .04; diagnosis: OR, 1.21; 95% CI, 1.05-1.40; P = .008), while a 5% increase in humidity levels was significantly associated with decreased symptoms and diagnoses of DED (symptoms: OR, 0.87; 95% CI, 0.77-0.98; P = .03; diagnosis: OR, 0.86; 95% CI, 0.76-0.97; P = .01). In model 2, an increase in ozone levels of 0.003 ppm was significantly associated with symptoms and diagnosis of DED (symptoms: OR, 1.17; 95% CI, 1.02-1.34; P = .03; diagnosis: OR, 1.27; 95 CI, 1.09-1.48; P = .002), while a 5% increase in humidity levels was significantly associated with decreased symptoms and diagnoses of DED (symptoms: OR, 0.88; 95% CI, 0.78-0.98; P = .045; diagnosis: OR, 0.86; 95% CI, 0.76-0.97; P = .02). In model 2, an increase in nitrogen dioxide of 0.003 ppm (OR, 1.12; 95% CI, 1.02-1.23 P = .02) was also associated with diagnosis of DED. Levels of sulfur dioxide and PM10 were not associated with symptoms or diagnosis of DED in model 1 or model 2 (P > .05 for each).

Conclusions and Relevance  Higher ozone levels and lower humidity levels were associated with DED in the Korean population, while PM10 level was not associated with DED.

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Figure 1.
Correlations Between Multiple Outdoor Air Pollution Factors

A, Particulate matter with aerodynamic diameter <10 µm (PM10) and humidity. B, Ozone and humidity. C, Nitrogen dioxide and humidity. D, Sulfur dioxide and humidity. E, Ozone and PM10. F, Nitrogen dioxide and PM10. G, Sulfur dioxide and PM10. H, Ozone and nitrogen dioxide. I, Ozone and sulfur dioxide. J, Nitrogen dioxide and sulfur dioxide. While nitrogen dioxide and PM10 were negatively correlated with humidity, ozone and sulfur dioxide were not. Ozone was negatively correlated with PM10, nitrogen dioxide, and sulfur dioxide and PM10 was positively correlated with nitrogen dioxide.

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Figure 2.
Relationship Between Air Pollution Factors and Regional Prevalence of DED Symptoms and Diagnosis

A, Symptoms and humidity. B, Symptoms and particulate matter with aerodynamic diameter <10 µm (PM10). C, Symptoms and ozone. D, Symptoms and nitrogen dioxide. E, Symptoms and sulfur dioxide. F, Diagnosis and humidity. G, Diagnosis and PM10. H, Diagnosis and ozone. I, Diagnosis and nitrogen dioxide. J, Diagnosis and sulfur dioxide. Increased humidity was associated with decreased prevalence of symtoms and diagnosis of dry eye disease (DED); however, PM10, ozone, nitrogen dioxide, and sulfur dioxide were not associated with regional prevalence of symptoms and diagnosis of DED.

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Potential Importance of Ozone in the Association Between Outdoor Air Pollution and Dry Eye Disease in South Korea
Posted on June 18, 2016
Parul Chawla Gupta; MS Ophthalmology, Jagat Ram; MS Ophthalmology
Department of Ophthalmology, Post Graduate Institute of Medical Education and Research, Chandigarh, India
Conflict of Interest: None Declared
To the Editor,

We commend Hwang and colleagues (1) for an excellent study investigating associations between outdoor air pollution and Dry Eye Disease (DED) in a Korean population. In their study, multivariable logistic regression demonstrated that higher ozone levels and lower humidity levels were significantly associated with symptoms and diagnosis of dry eye disease. However, we believe some issues need further discussion. Firstly, diabetes mellitus should have been added as a covariate as it can lead to severe dry eye especially in patients with diabetic peripheral neuropathy.(2) Secondly, use of preserved antiglaucoma drugs could have been considered as a covariate since preservatives like benzalkonium chloride are known to cause dry eye.(3) History of use of systemic drugs causing DED like antihistaminics, antidepressents, antihypertensives (beta-blockers and thiazides) should also be incldued, as they may act as potential confounders. Thirdly, why were the participants not assessed for DED on the basis of standardized questionnaires like Ocular Surface Disease Index (OSDI) or Visual Function Questionnaire (VFQ-25) or Standard Patient Evaluation of Eye Dryness (SPEED)?(4) Lastly, in accordance with previous studies, the present study revealed a higher prevalence of DED among older individuals especially women.(1) The higher prevalence of DED among women has been associated with various systemic conditions, such as complete androgen insensitivity syndrome, premature ovarian failure, and polycystic ovarian syndrome (PCOS). In addition, the tear film and ocular surface can be affected by hormonal changes in various situations, such as pregnancy, lactation, contraceptive use, hormone replacement therapy, oophorectomy, hysterectomy, menopause as well as with irregular menstruation.(5) All of these entities may act as confounders. Moreover, since high altitude exposure leads to an altered tear film resulting in an increased tear film osmolarity and a reduced tear film break up time leading to dry eye symptoms, it would also be interesting to know if altitude was accounted for before analyzing the results.(6)

References
1. Hwang SH, Choi YH, Paik HJ, Wee WR, Kim MK, Kim DH. Potential Importance of Ozone in the Association Between Outdoor Air Pollution and Dry Eye Disease in South Korea. JAMA Ophthalmol. 2016;134(5):503-510.
2. DeMill DL, Hussain M, Pop-Busui R, Shtein RM. Ocular Surface Disease in Patients with Diabetic Peripheral Neuropathy. Br J Ophthalmol. 2015 Oct 23. pii: bjophthalmol-2015-307369. doi: 10.1136/bjophthalmol-2015-307369. [Epub ahead of print]
3. Noecker R. Effects of common ophthalmic preservatives on ocular health. Adv
Ther 2001; 18(5): 205–215.
4. Asiedu K, Kyei S, Mensah SN et al. Ocular Surface Disease Index (OSDI) Versus the Standard Patient Evaluation of Eye Dryness (SPEED): A Study of a Nonclinical Sample. Cornea 2016;35:175–180.
5. Song J, Kim M, Paik S et al. Association Between Menstrual Irregularity and Dry Eye Disease: A Population-Based Study. Cornea 2016;35:193–198.

6. Willmann G, Schatz A, Fischer MD, Schommer K, Zrenner E, Bartz-Schmidt KU et al. Exposure to high altitude alters tear film osmolarity and breakup time. High Alt Med Biol. 2014;15(2):203-7.

__________________________

From the article authors:

Thank you for taking a profound interest in our study. First, we also thought that diabetes mellitus was important in dry eye disease (DED). However, diabetes mellitus was not associated with DED in KNHANES data (Am J Ophthalmol. 2014 Dec;158(6):1205-1214), and our pilot results using KNHANES data also demonstrated that diabetes mellitus was not associated with DED. Second, use of preserved antiglaucoma drugs and systemic drugs could affect DED. Unfortunately, history of use of preserved antiglaucoma drugs and systemic drugs like antihistaminics, antidepressents, antihypertensives was not available in KNHANES data. Instead, we added a history of hypertension, depression, rheumatoid arthritis, atopic dermatitis, malignancy, thyroid disease, dyslipidemia, etc. in pilot analysis. In that analyses, dyslipidemia and thyroid dysfunction were associated with DED. Therefore, we used these factors as covariates in the final models. Third, DED was not defined from physical examination findings, but rather from answers on self-reported simple questionnaires in this study. We agree that this is a limitation. However, standardized questionnaires like the Ocular Surface Disease Index (OSDI) or Visual Function Questionnaire (VFQ-25) were not available in KNHANES data. We also did not take into consideration the changes in sex hormones and the difference in altitude because accurate information about sex hormonal changes and altitude were not available. We agree that those would be important factors in DED. We have been conducting a clinical study regarding the role of air pollution and DED, and we included an ocular staining score, OSDI, Schirmer test, tear break up time as outcome measures.  Several of the aforementioned confounding factors were also included as covariates. We think that the results of this ongoing study may present more clear information about the relationship between air pollution and DED.


References
1. Hwang SH, Choi YH, Paik HJ, Wee WR, Kim MK, Kim DH. Potential Importance of Ozone in the Association Between Outdoor Air Pollution and Dry Eye Disease in South Korea. JAMA Ophthalmol. 2016;134(5):503-510.
2. Ahn JM, Lee SH, Rim TH el al. Prevalence of and risk factors associated with dry eye: the Korea National Health and Nutrition Examination Survey 2010-2011.Am J Ophthalmol. 2014 Dec;158(6):1205-1214.

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