Association of Daily Wear of Eyeglasses with Susceptibility to Coronavirus Disease 2019 Infection

Research

JAMA Ophthalmology | Brief Report Association of Daily Wear of Eyeglasses With Susceptibility to Coronavirus Disease 2019 Infection

Weibiao Zeng, MS; Xiaolin Wang, MS; Junyu Li, MS; Yong Yang, MS; Xingting Qiu, MS; Pinhong Song, MS; Jianjun Xu, MD, PhD; Yiping Wei, MD, PhD

Invited Commentary IMPORTANCE The proportion of daily wearers of eyeglasses among patients with coronavirus page 1199 disease 2019 (COVID-19) is small, and the association between daily wear of eyeglasses and COVID-19 susceptibility has not been reported.

OBJECTIVE To study the association between the daily wearing of eyeglasses and the susceptibility to COVID-19.

DESIGN, SETTING, AND PARTICIPANTS This cohort study enrolled all inpatients with COVID-19 in Suizhou Zengdu Hospital, Suizhou, China, a designated hospital for COVID-19 treatment in the area, from January 27 to March 13, 2020. COVID-19 was diagnosed according to the fifth edition of Chinese COVID-19 diagnostic guidelines. The proportion of persons with myopia who wore eyeglasses in Hubei province was based on data from a previous study.

EXPOSURES Daily wearing of eyeglasses for more than 8 hours.

MAIN OUTCOMES AND MEASURES The main outcomes were the proportions of daily wearers of eyeglasses among patients admitted to the hospital with COVID-19 and among the local population. Data on exposure history, clinical symptoms, underlying diseases, duration of wearing glasses, and myopia status and the proportion of people with myopia who wore Author Affiliations: Department of eyeglasses in Hubei province were collected. People who wore glasses for more than 8 hours Thoracic Surgery, The Second a day were defined as long-term wearers. Affiliated Hospital of Nanchang University, Nanchang, China (Zeng, RESULTS A total of 276 patients with COVID-19 were enrolled. Of these, 155 (56.2%) were Xu, Wei); Department of Critical Care Medicine, Suizhou Zengdu Hospital, male, and the median age was 51 (interquartile range, 41-58) years. All those who wore Suizhou, China (Wang, Yang, Song); glasses for more than 8 hours a day had myopia and included 16 of 276 patients (5.8%; Department of Radiotherapy, Jiangxi 95% CI, 3.04%-8.55%). The proportion of people with myopia in Hubei province, based on Cancer Hospital, Nanchang, China a previous study, was 31.5%, which was much higher than the proportion of patients with (Li); Department of Computed Tomography and Magnetic COVID-19 who had myopia in this sample. Resonance Imaging, The First Affiliated Hospital of Gannan Medical CONCLUSIONS AND RELEVANCE In this cohort study of patients hospitalized with COVID-19 in University, Ganzhou, China (Qiu). Suizhou, China, the proportion of inpatients with COVID-19 who wore glasses for extended Corresponding Author: Yiping Wei, daily periods (>8 h/d) was smaller than that in the general population, suggesting that daily MD, PhD (weiyip2000@hotmail. wearers of eyeglasses may be less susceptible to COVID-19. com), and Jianjun Xu, MD, PhD ([email protected]), Department of Thoracic Surgery, JAMA Ophthalmol. 2020;138(11):1196-1199. doi:10.1001/jamaophthalmol.2020.3906 The Second Affiliated Hospital of Published online September 16, 2020. Nanchang University, 1 Min De Road, Nanchang 330006, China.

oronavirus disease 2019 (COVID-19), the pathogen of fore, we collected information on the wearing of eyeglasses which is severe acute respiratory syndrome coronavi- from all inpatients with COVID-19 as part of their medical his- C rus 2 (SARS-CoV-2), is a highly infectious disease that tory and used the data to examine the association between broke out in Wuhan, China, in December 2019 and has spread wearing eyeglasses and COVID-19 infection. to more than 200 countries.1 COVID-19 has been proven to be transmitted mainly through droplets and contact.2 The eye is also considered an important route of infection. Methods According to reports published in recent years, the prevalence of myopia in China is now more than 80% of the popu- This cohort study was approved by the ethics committee of lation. Wearing of eyeglasses is common among Chinese in- Suizhou Zengdu Hospital, Suizhou, China, and followed the dividuals of all ages.3 However, since the outbreak of COVID-19 Strengthening the Reporting of Observational Studies in Epi- in Wuhan in December 2019, we observed that few patients demiology (STROBE) reporting guideline. Patients signed with eyeglasses were admitted in the hospital ward. There- written informed consent and were not provided with any

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incentive or compensation to participate in the study.The study enrolled patients admitted to the hospital from January 27 Key Points to March 13, 2020, with the admission criteria of a diagnosis Question What is the association between the daily wear of of COVID-19. The diagnostics and clinical classification of eyeglasses and susceptibility to coronavirus disease 2019 COVID-19 were based on the fifth edition of Chinese COVID-19 (COVID-19)? diagnostic guidelines.4 Throat swab samples were obtained Findings In this cohort of 276 patients hospitalized with COVID-19 from patients at admission and tested using real-time reverse in Suizhou, China, the proportion of daily wearers of eyeglasses transcriptase–polymerase chain reaction assays to identify was lower than that of the local population (5.8% vs 31.5%). COVID-19 infection. Patients were specifically asked about Meaning These findings suggest that daily wearers of eyeglasses the reason they wore eyeglasses, the length of time that they may be less likely to be infected with COVID-19. wore eyeglasses during daily activities, and whether they wore contact lenses or had ever undergone refractive surgery. This information was recorded by the patients’ treating physicians glasses and COVID-19 infection. Our main finding was that pa- while taking their medical history, starting February 4, 2020. tients with COVID-19 who wear eyeglasses for an extended pe- Information on exposure history and clinical symptoms riod (>8 h/d) every day were relatively uncommon, which could was extracted from the medical records. People who wore be preliminary evidence that daily wearers of eyeglasses are eyeglasses for more than 8 hours a day were defined as long- term wearers, and these people were considered to wear Table. Clinical Characteristics of the Study Patients eyeglasses when socializing. Data To estimate the population myopia rate, we extracted data Characteristic (n = 276)a from the Research on Chinese Student Physique and Health Age, median (IQR), y 51 (41-58) Study,5 which recorded data from a survey about the physical Severe illness 14 (5.1) and health status of Chinese students, organized by state edu- Male 155 (56.2) cational institutions and the Ministry of Health of China in 1985. Reason for wearing eyeglasses We used descriptive statistics to characterize the study sample. Presbyopia 14 (5.1) Myopia 16 (5.8) Wearing glasses >8 h/d 16 (5.8) Results Current smokers 42 (15.2) BMI, median (IQR) 23.7 (22.0-25.4) As shown in the Table, a total of 276 patients with COVID-19 Exposure historyb were enrolled in the study. The median age was 51 (interquar- Recently visited Wuhan 43 (15.6) tile range, 41-58) years; 155 patients (56.2%) were male and 121 Contact with people who had traveled 166 (60.1) (43.8%) were female. Most patients with COVID-19 were mod- to Wuhan or diagnosed with COVID-19 erately ill, with 14 (5.1%) severely ill. Common symptoms were Contact with wildlife 0 fever (227 [82.2%]), cough (218 [79.0%]), and fatigue (141 Median incubation period, median (IQR), dc 6.0 (4.0-9.0) [51.1%]). Underlying disease was present in 88 patients (31.9%), Symptoms with hypertension the most common, accounting for 47 (17.0%) Fever 227 (82.2) of all admitted patients. Thirty patients with COVID-19 wore Cough 218 (79.0) eyeglasses (10.9%), including 16 cases of myopia and 14 cases Sputum production 137 (49.6) of presbyopia. None of the patients in this study wore contact Fatigue 141 (51.1) lenses or underwent refractive surgery. All 16 patients with Shortness of breath 42 (15.2) COVID-19 who wore glasses for more than 8 hours per day had Comorbidities myopia, accounting for 5.8% (95% CI, 3.0%-8.6%), and the me- Any 88 (31.9) dian age was 33 years. Their symptoms, underlying disease, Hypertension 47 (17.0) and COVID-19 severity were not significantly different from Chronic obstructive pulmonary disease 7 (2.5) those of other patients. Diabetes 14 (5.1) The results from previous research5 showed that the mean Coronary heart disease 12 (4.3) rate of myopia among students aged 7 to 22 years in Hubei prov- Cerebrovascular disease 6 (2.2) ince was 31.5%. By 2020, these students were aged 42 to 57 d years, which is close to the median age of our patients with Cancer 3 (1.1) COVID-19. The myopia rate of 31.5% is higher than the 5.8% Abbreviations: BMI, body mass index (calculated as weight in kilograms among our patients with COVID-19. divided by square of height in meters); COVID-19, coronavirus disease 2019; IQR, interquartile range. a Unless otherwise indicated, data are expressed as number (percentage) of patients. Discussion b Source of exposure was unknown in 67 patients. c Undetermined incubation period for 205 patients. At the time of writing, this study was the only research, to our d Included any kind of cancer. knowledge, to assess the association between wearing eye-

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less susceptible to COVID-19. Considering the prevalence of this study can be used as evidence of the importance of COVID-19, conducting a sample survey among the local popu- these 2 recommendations. lation would have been difficult. Instead, we used data from a previous survey for approximate reference and compari- Limitations son, although the age, region, and educational level of the Our study had some notable limitations. First, it was a single- students in that survey had some differences compared with center study with a small sample size. The numbers of pa- our study population. tients who wear eyeglasses and long-term wearers were lim- We hypothesized that eyeglasses prevent or discourage ited, which limits the extension of the results to a larger wearers from touching their eyes, thus avoiding transferring population, so our results need to be verified by large-sample the virus from the hands to the eyes.6 Studies have shown multicenter studies. Second, the proportion of wearers of eye- that normal people will involuntarily touch their eyes about glasses was based on data from previous literature and was not 10 times per hour.7 Eyes usually lack protection, and calculated from current local populations. Third, the myopia an abundance of the SARS-CoV-2 receptor angiotensin- rate obtained in previous studies included a small number of converting enzyme 2 has been found on the ocular surface,8 people with myopia who did not wear eyeglasses. Informa- through which SARS-CoV-2 can enter the human body. tion on these people was lacking and partly affected the in- SARS-CoV-2 may also be transported to the nasal and naso- tegrity and validity of our data. Fourth, none of our research pharyngeal mucosa through continuous tear irrigation of the participants wore contact lenses, so the association between lacrimal duct, causing respiratory infection.9 According wearing contact lenses and susceptibility to COVID-19 re- to available statistics, nearly 1% to 12% of patients with mains to be studied. In addition, further studies are needed COVID-19 have ocular manifestations,10,11 SARS-CoV-2 was to clarify the reasons that wearing eyeglasses may decrease detected in tears or the conjunctival sacs of patients with susceptibility to COVID-19. COVID-19,12 and some ophthalmologists were reported to be infected during routine treatment.13 Therefore, the eyes are considered an important channel for SARS-CoV-2 to enter Conclusions the human body.11 For daily wearers of eyeglasses, who usually wear eyeglasses on social occasions, wearing eyeglasses Our study found that the proportion of inpatients with may become a protective factor, reducing the risk of virus COVID-19 who wear eyeglasses for extended daily periods transfer to the eyes and leading to long-term daily wearers of was lower than that of the general population, suggesting eyeglasses being rarely infected with COVID-19. Presently, that daily wear of eyeglasses is associated with less suscepti- many COVID-19 guidelines state the need to pay attention to bility to COVID-19 infection. These findings suggest that preventing infections through the eyes,14 but most people the eye may be an important infection route for COVID-19, only focus on wearing masks and home isolation, ignoring and more attention should be paid to preventive measures recommendations such as washing hands frequently and such as frequent hand washing and avoiding touching avoiding touching the eyes with the hands.15 The results of the eyes.

ARTICLE INFORMATION REFERENCES 6. van Doremalen N, Bushmaker T, Morris DH, et al. Accepted for Publication: July 28, 2020. 1. Wu Z, McGoogan JM. Characteristics of and Aerosol and surface stability of SARS-CoV-2 as important lessons from the coronavirus disease compared with SARS-CoV-1. N Engl J Med.2020; Published Online: September 16, 2020. 382(16):1564-1567. doi:10.1056/NEJMc2004973 doi:10.1001/jamaophthalmol.2020.3906 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for 7. Kwok YL, Gralton J, McLaws ML. Face touching: Author Contributions: Drs Wei and Xu had full Disease Control and Prevention. JAMA.2020. a frequent habit that has implications for hand access to the study data and take responsibility for doi:10.1001/jama.2020.2648 hygiene. Am J Infect Control. 2015;43(2):112-114. the integrity of the data and the accuracy of the doi:10.1016/j.ajic.2014.10.015 data analysis. 2. Pongpirul WA, Pongpirul K, Ratnarathon AC, Concept and design: Xu, Yiping. Prasithsirikul W. Journey of a Thai taxi driver and 8. Holappa M, Vapaatalo H, Vaajanen A. Many faces Acquisition, analysis, or interpretation of data: Zeng, novel coronavirus. N Engl J Med. 2020;382(11): of renin-angiotensin system—focus on eye. Open Xiaolin, Junyu, Qiu, Yong, Song, Yiping. 1067-1068. doi:10.1056/NEJMc2001621 Ophthalmol J. 2017;11:122-142. doi:10.2174/ Drafting of the manuscript: Zeng, Xiaolin, Junyu, 3. Chen M, Wu A, Zhang L, et al. The increasing 1874364101711010122 Qiu, Song, Yiping. prevalence of myopia and high myopia among high 9. Xiao X, Chakraborti S, Dimitrov AS, Critical revision of the manuscript for important school students in Fenghua City, eastern China: Gramatikoff K, Dimitrov DS. The SARS-CoV S intellectual content: Zeng, Yong, Xu, Yiping. a 15-year population-based survey. BMC Ophthalmol. glycoprotein: expression and functional Statistical analysis: All authors. 2018;18(1):159. doi:10.1186/s12886-018-0829-8 characterization. Biochem Biophys Res Commun. Obtained funding: Zeng, Xu, Yiping. 4. General Office of National Health Commission. 2003;312(4):1159-1164. doi:10.1016/j.bbrc.2003.11. Administrative, technical, or material support: Zeng, Diagnosis and treatment protocols for novel 054 Junyu, Yong, Xu, Yiping. coronavirus pneumonia (trial version 5, revised) [in 10. Guan WJ, Ni ZY, Hu Y, et al; China Medical Supervision: Yong, Xu, Yiping. Chinese]. Published February 4, 2020. Accessed Treatment Expert Group for Covid-19. Clinical Conflict of Interest Disclosures: None reported. March 15, 2020. http://www.gov.cn/zhengce/ characteristics of coronavirus disease 2019 in Additional Contributions: We thank the physicians zhengceku/2020-02/09/content_5476407.htm China. N Engl J Med. 2020;382(18):1708-1720. who supported Suizhou Zengdu Hospital, Suizhou, 5. Chinese Student Physique and Health Research doi:10.1056/NEJMoa2002032 China, in the fight against coronavirus disease 2019 Group. Research on Chinese Students' Physique and 11. Wu P, Duan F, Luo C, et al. Characteristics of for their contribution to patient management and Health [in Chinese]. People's Education Press; 1987. ocular findings of patients with coronavirus disease data collection for this study. 2019 (COVID-19) in Hubei Province, China. JAMA

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Ophthalmol. 2020;138(5):575-578. doi:10.1001/ 13. Lu CW, Liu XF, Jia ZF. 2019-nCoV transmission 15. Machida M, Nakamura I, Saito R, et al. Adoption jamaophthalmol.2020.1291 through the ocular surface must not be ignored. of personal protective measures by ordinary 12. Seah IYJ, Anderson DE, Kang AEZ, et al. Lancet. 2020;395(10224):e39. doi:10.1016/S0140- citizens during the COVID-19 outbreak in Japan. Assessing viral shedding and infectivity of tears in 6736(20)30313-5 Int J Infect Dis. 2020;94:139-144. doi:10.1016/j.ijid. coronavirus disease 2019 (COVID-19) patients. 14. World Health Organization. Coronavirus 2020.04.014 Ophthalmology. 2020;127(7):977-979. doi:10.1016/j. disease (COVID-19) advice for the public. Updated ophtha.2020.03.026 June 4, 2020. Accessed April 1, 2020. https://www. who.int/emergencies/diseases/novel-coronavirus- 2019/advice-for-public

Invited Commentary Eye Protection and the Risk of Coronavirus Disease 2019 Does Wearing Eye Protection Mitigate Risk in Public, Non–Health Care Settings? Lisa L. Maragakis, MD, MPH

Transmission of the severe acute respiratory syndrome coro- tional study. The study demonstrates an apparent inverse as- navirus 2 (SARS-CoV-2), the pathogen that causes coronavi- sociation between routinely wearing eyeglasses and the risk rus disease 2019 (COVID-19), continues in many countries and of subsequent COVID-19. Observational studies such as this communities around the world. Until 1 or more effective vac- one, however, have inherent limitations due to the possibil- cines or therapeutic agents ity of various forms of bias in the study data and possible con- 4 Related article page 1196 are available, basic infection founding variables. Of note, the authors acknowledge sev- prevention measures, such as eral limitations to the study design, including the fact that the universal masking, physical distancing, and hand hygiene, of- data for the general population comparison group were gleaned fer the best known protection against the disease.1,2 In health from a study that took place decades earlier in a different re- care settings, eye protection is an important part of the per- gion of China.3 The study results may be misleading owing to sonal protective equipment (PPE) ensemble recommended for confounding variables, and there may be an alternative expla- frontline health care personnel who come into close and pro- nation for the findings if, for instance, wearing eyeglasses is longed contact with patients, including those who are in- associated with another unknown and unmeasured factor as- fected with SARS-CoV-2.1 Eye protection, such as goggles or a sociated with the risk of COVID-19. If this is the case, we would face shield, used with a mask or respirator that covers the nose be incorrect to conclude that wearing eyeglasses reduces a per- and mouth protects health care personnel’s eyes and mucous son’s susceptibility to COVID-19 or to recommend that people membranes from the virus, which can be transmitted by virus- should begin wearing eye protection in public to prevent containing respiratory droplets, possibly by airborne viral par- COVID-19 acquisition. Another limitation of the study is that ticles in smaller droplet nuclei, or by touching one’s face or eyes the investigation took place very early in the pandemic, and with virus-contaminated hands. To date, however, public the descriptive statistics do not include data on hand wash- health guidelines do not recommend that members of the pub- ing or physical distancing, 2 main interventions to mitigate the lic, outside of the health care setting, wear any type of eye pro- risk of COVID-19. This makes it difficult to assess any incre- tection in addition to a wearing a mask, physical distancing, mental benefit of eye protection in public settings over and and hand washing.1,2 above these basic interventions that are now the mainstay of In this issue of JAMA Ophthalmology,Zengetal3 describe COVID-19 prevention. a study of patients in Hubei Province, China, at the beginning In 1965, Austin Bradford Hill5 published a framework for of the pandemic in which they found that, among a group interpretation of observational epidemiologic studies that of- of 276 patients admitted to a hospital with laboratory- fers guidelines to interpret whether a demonstrated epide- confirmed COVID-19, the proportion of the patients who re- miologic association is likely to represent causation. Several ported routinely wearing eyeglasses more than 8 hours per day of the factors require examination of multiple studies over time, was lower than in the general population. From these data, the rather than relying on a single study, so that the strength, con- authors conclude that wearing eyeglasses more than 8 hours sistency, specificity, and coherence of the findings can be com- per day may be protective against SARS-CoV-2 infection, and pared across the various reports. When presented with a single they hypothesize that this may be due to eyeglasses acting as study such as the one by Zeng and colleagues,3 the data sug- a barrier that reduces the frequency with which people touch gest that the observed difference in wearing eyeglasses be- their eyes. tween the group of patients with COVID-19 vs the general popu- Although it is tempting to conclude from this study that lation is unlikely to have occurred by chance alone, but it does everyone should wear eyeglasses, goggles, or a face shield in not indicate a causal relationship between wearing eye- public to protect their eyes and themselves from COVID-19, glasses and preventing the disease. What we can say from this from an epidemiological perspective, we must be careful to single study is that it appears to satisfy the considerations by avoid inferring a causal relationship from a single observa- Hill5 of both temporality, because the eyeglasses were worn

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