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Figure 1.  Triage System
Triage System

COVID-19 indicates coronavirus disease 2019.

Figure 2.  The Examination Room Separated Into 5 Zones
The Examination Room Separated Into 5 Zones

Considering the patient in the center of the circles, each circle was determined to be 1 m distant from the previous circle. Zone 1 included a slitlamp shield, phoropter, and biomicroscope stage; zone 2, a tonometer; zones 3 and 4, a desk; and zone 5, the door handles.

1.
Wu  F, Zhao  S, Yu  B,  et al.  A new coronavirus associated with human respiratory disease in China.   Nature. 2020;579(7798):265-269. doi:10.1038/s41586-020-2008-3 PubMedGoogle ScholarCrossref
2.
Yezli  S., and Otter  J.A.,  Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.   Food Environ Microbiol. 2011; 3: 1–30. doi:10.1007/s12560-011-9056-7Google Scholar
3.
Geller  C, Varbanov  M, Duval  RE.  Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies.   Viruses. 2012;4(11):3044-3068. doi:10.3390/v4113044 PubMedGoogle ScholarCrossref
4.
van Doremalen  N, Bushmaker  T, Munster  VJ.  Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions.   Euro Surveill. 2013;18(38):19. doi:10.2807/1560-7917.ES2013.18.38.20590PubMedGoogle ScholarCrossref
5.
Chan  KH, Peiris  JS, Lam  SY, Poon  LL, Yuen  KY, Seto  WH.  The effects of temperature and relative humidity on the viability of the SARS coronavirus.   Adv Virol. 2011;2011:734690. doi:10.1155/2011/734690 PubMedGoogle Scholar
6.
Coulliette  AD, Perry  KA, Edwards  JR, Noble-Wang  JA.  Persistence of the 2009 pandemic influenza A (H1N1) virus on N95 respirators.   Appl Environ Microbiol. 2013;79(7):2148-2155. doi:10.1128/AEM.03850-12 PubMedGoogle ScholarCrossref
7.
Bai  Y, Yao  L, Wei  T,  et al.  Presumed asymptomatic carrier transmission of COVID-19.   JAMA. 2020;323(14):1406-1407. doi:10.1001/jama.2020.2565PubMedGoogle ScholarCrossref
8.
Moriarty  LF, Plucinski  MM, Marston  BJ,  et al; CDC Cruise Ship Response Team; California Department of Public Health COVID-19 Team; Solano County COVID-19 Team.  Public health responses to COVID-19 outbreaks on cruise ships—worldwide, February-March 2020.   MMWR Morb Mortal Wkly Rep. 2020;69(12):347-352. doi:10.15585/mmwr.mm6912e3PubMedGoogle ScholarCrossref
9.
van Doremalen  N, Bushmaker  T, Morris  DH,  et al.  Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1.   N Engl J Med. 2020;382(16):1564-1567. doi:10.1056/NEJMc2004973 PubMedGoogle ScholarCrossref
10.
Rabenau  HF, Cinatl  J, Morgenstern  B, Bauer  G, Preiser  W, Doerr  HW.  Stability and inactivation of SARS coronavirus.   Med Microbiol Immunol. 2005;194(1-2):1-6. doi:10.1007/s00430-004-0219-0PubMedGoogle ScholarCrossref
11.
Duan  SM, Zhao  XS, Wen  RF,  et al; SARS Research Team.  Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.   Biomed Environ Sci. 2003;16(3):246-255.PubMedGoogle Scholar
12.
Yang  Y, Yang  M, Shen  C,  et al. Evaluating the accuracy of different respiratory specimens in the laboratory diagnosis and monitoring the viral shedding of 2019-nCoV infections. Published February 17, 2020. Accessed July 24, 2020. https://www.medrxiv.org/content/10.1101/2020.02.11.20021493v2
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    1 Comment for this article
    Interventions in the study
    Juan Carlos Corbera, MD | Peruvian Society of Ophthalmology
    Did the asymptomatic patients In the study use masks or wash their hands before entering the office ?
    CONFLICT OF INTEREST: None Reported
    Views 19,980
    Citations 0
    Brief Report
    August 3, 2020

    Detection of Coronavirus Disease 2019 Viral Material on Environmental Surfaces of an Ophthalmology Examination Room

    Author Affiliations
    • 1Department of Ophthalmology, İzmir Tepecik Training and Research Hospital, İzmir, Turkey
    • 2Department of Ophthalmology, Turkish Republic Health Sciences University, Tepecik Training and Research Hospital, İzmir, Turkey
    • 3Department of Medical Microbiology, Turkish Republic Health Sciences University, Tepecik Training and Research Hospital, İzmir, Turkey
    JAMA Ophthalmol. 2020;138(9):990-993. doi:10.1001/jamaophthalmol.2020.3154
    Key Points

    Question  Do ophthalmologists run the risk of encountering individuals who are asymptomatically carrying severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) when maintaining elective examinations during the coronavirus disease 2019 pandemic?

    Finding  In this quality improvement study of samples from 1 examination room, slitlamp breath shield and phoropter surface samples were analyzed by real-time polymerase chain reaction. In 2 of 7 postexamination samples, SARS-CoV-2 viral material was found.

    Meaning  Despite triage systems to exclude patients with coronavirus disease 2019, viral material was found on ophthalmology examination room surfaces; however, the infectivity of the virus samples was unknown.

    Abstract

    Importance  The new coronavirus disease 2019 (COVID-19) pandemic poses a particular threat to health care professionals; however, there appear to be no objective data that demonstrate the risks of encountering individuals carrying the virus asymptomatically in the case of maintained elective examinations.

    Objective  To investigate the presence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) on the environmental surfaces of an ophthalmology examination room after visits by patients who were asymptomatic and had passed COVID-19 triage.

    Design, Setting, and Participants  This is a quality improvement study conducted 1 week after the first officially confirmed COVID-19 case in İzmir Tepecik Training and Research Hospital, İzmir, Turkey, on March 20, 2020. A triage system was used to determine the risk of COVID-19 from patients who were asymptomatic and presented for examination in an ophthalmology clinic. Real-time polymerase chain reaction testing was used to detect the presence of viral RNA material in samples from the biomicroscope stage, slitlamp breath shield, phoropter, tonometer, and door handles. The first group of samples was taken before the beginning of the examinations, and the second group of the samples was taken after the last patient had left the room.

    Main Outcomes and Measures  The main outcome was the presence of viral material on surfaces in 5 circular zones with a diameter of 1 m each around where the patients sat.

    Results  Thirty-one persons visited the room, of whom 22 underwent ophthalmic examination and 9 were companions. The mean (SD) examination time was 9 (4) minutes (range, 5-13 minutes). Seven samples were taken before examinations and 7 after examinations. Two samples that were taken after examinations were found to be positive for COVID-19, 1 from the slitlamp breath shield and 1 from the phoropter.

    Conclusions and Relevance  This study showed the presence of COVID-19 viral material in a circle 1 m in diameter around where the patients sat. However, real-time polymerase chain reaction could only detect viral material, not the infectivity of these virus samples.

    Introduction

    Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an enveloped, single-stranded RNA virus that causes coronavirus disease 2019 (COVID-19).1 Person-to-person contact through droplets is believed to be the primary route of virus transmission. However, it has also been suggested that virus can be spread via contaminated surfaces. The survival of enveloped viruses, such as influenza, Middle Eastern respiratory syndrome coronavirus (MERS-CoV), and severe acute respiratory syndrome coronavirus (SARS-CoV), on dry surfaces is generally believed to be limited.2,3 In contrast, a few studies have suggested that those viruses can remain viable on dry surfaces for a sufficient time to facilitate forward transmission.4-6 The presence of SARS-CoV-2 has also been reported7 to have been spread by asymptomatic transmission in a patient who possibly infected 5 family members. A study8 of cruise ship outbreaks of SARS-CoV-2 reported that viral RNA was identified on the surfaces of cabins up to 17 days after patient disembarkation. Another study9 found that viable SARS-CoV-2 was present in aerosols up to 3 hours postaerosolization. However, it should be noted that this experiment9 did not reflect examination room conditions but was conducted using a nebulizer and a Goldberg drum that generates aerosols and disperses microdroplets.

    Therefore, we designed this study during an examination day in an outpatient eye clinic without interventions for patients who were asymptomatic. This study aimed to observe viral shedding on the surfaces of an ophthalmology examination room.

    Methods

    This prospective observational study was approved by the Turkish Republic Ministry of Health Scientific Research Platform and a local institutional review board. Informed consent was not obtained because of the nature of the study did not require human participation, biologic material, or personal data.

    The study was performed on March 20, 2020, after the first officially confirmed COVID-19 case in Turkey on March 11, 2020. The pandemic management committee applied a triage system to the patients and health care workers. Patients and their companions with foreign travel histories to then-affected areas (eg, China, Italy, and Iran) or contact with any person with a confirmed or suspected case and patients with fever, coughing, or general illness were excluded from the elective examinations (Figure 1). Patients showing no symptoms were examined. Medical personnel with no symptoms were not screened for COVID-19 with real-time polymerase chain reaction (RT-PCR).

    In the examination room, a plastic slitlamp breath shield was adapted to maintain a physical barrier. The measurements of the room in length, width, and height were 6 m, 3 m, and 2.5 m respectively. Room humidity was 55.3%, and the temperature was 24 °C. There was no automated disinfection system, such as hydrogen peroxide vapor or ultraviolet light, in the room.

    The room was cleaned with hydrogen peroxide, 3%, after the last examination and had no visitors for approximately 18 hours after cleaning. No room cleaning was done between patients, but chin and forehead rests were wiped with isopropyl alcohol, 70%, between the patients. The same physician (H.A.) performed all examinations, and 1 health care worker visited the room during examinations. Only companions of patients of pediatric age and patients with communication and mobility problems were allowed to enter the room. The numbers of companions were recorded.

    The investigator (H.A.) collected and numbered the samples according to the zones and time of sampling. We only included environmental surface samples from the examination room. The patient’s chair was defined as the center of a circle 6 m in diameter, and samples were taken at each 1 m of distance. Five zones that were 1 m distant from each other were defined (Figure 2). According to the zone definition, the slitlamp shield, biomicroscope stage, and phoropter were within zone 1; the tonometer, zone 2; the desk, zones 3 and 4; and the door handles, zone 5. Samples were taken from the biomicroscope stage, slitlamp shield, phoropter, tonometer, and door handles twice daily.

    Dacron swabs were used to gather the surface samples. The first samples were taken at 8:30 am before the beginning of daily examinations. The second group of samples was taken at 5:00 pm, after the last patient had left the room. Samples were tested by RT-PCR. Laboratory evaluation of the samples was single masked. Excel version 16.37 (Microsoft) was used to analyze the data.

    Results

    Twenty-nine patients came to the hospital for an eye examination; 7 were directed for COVID-19 tests following triage and did not come to the examination room. The remaining 22 patients came to the eye examination room, along with 9 companions and 1 health care professional. This health care worker was not symptomatic. Thus, 31 visitors entered the room, of whom 22 underwent ophthalmic examinations. The mean (SD) examination time was 9 (4) minutes (range, 5-13 minutes).

    Fourteen samples were collected from the surfaces in the examination room. All 7 samples taken before the beginning of the examinations had negative results. While 5 of 7 samples taken after the last patient had left the room had negative results, 2 samples obtained in zone 1, from the slitlamp shield and phoropter, were found to be positive for COVID-19 viral material. The negative sample that was closest to the patient was taken in zone 2, at 1.5 m distance. The other negative samples were from 3 to 4 m and 5 m, respectively.

    Discussion

    A laboratory study9 has shown that viable SARS-CoV-2 could be found viable in aerosols for about 3 hours. Also, the virus can be found on dry surfaces, depending on the material of the surface, for 8 to 72 hours.9 In addition to the surface materials, it also depends on the conditions (eg, temperature, humidity), as well as whether droplet or aerosol-generated conditions exist. Viability of SARS-CoV-2 on dry surfaces seems to be identical to that of SARS-CoV-1 and MERS-CoV.4,5,9-11 However, the main difference between SARS-CoV-2 and the other viruses is the higher transmission rate, which is currently being attributed to individuals carrying the virus asymptomatically. Despite laboratory studies showing the presence of the virus on various surfaces, they had some practical limitations. An important limitation of laboratory studies is the difficulty of evaluating individuals who are infected and asymptomatic in routine examinations. Since we were examining patients who are asymptomatic during the pandemic, we wanted to know if we could detect COVID-19 viral material at the end of a day of examinations of patients who were asymptomatic and seen in an eye examination room.

    Contamination from the preceding days was ruled out, considering that all samples that were taken before examinations had negative results for viral material. Two of the 3 samples that were taken from the slitlamp shield and phoropter in zone 1 after examinations had positive results. The closest negative sample that was taken after the examinations was located at 1.5 m. The other negative samples were located at 3 to 4 m and 5 m, respectively.

    In addition, RT-PCR technique has some limitations with respect to sample collection, transportation, and kit performance. In a recent study, the total positive rate of PCR was reported as 30% to 60% at the initial presentation.12 The relatively low positivity rate of the PCR technique may be responsible for the lack of detection of viral materials on the other zone surfaces and in samples that were taken before the examinations.

    Limitations

    This study had some limitations. First, RT-PCR establishes only the presence of viral material but provides no information about infectivity, virulence, viability, or viral load. This is why the outcomes of this study cannot comment on the potential infection risk of encountering an individual carrying the virus asymptomatically during a routine eye examination. Second, the study had a small sample size, because it was conducted over the course of only 1 day. Third, it was not known whether patients, companions, and health care worker developed symptoms.

    Conclusion

    In conclusion, this study provided objective data about the potential for patients who are asymptomatic, those accompanying them, or health care personnel in an eye examination room to leave viral material on the surfaces tested. Further studies are needed to determine the clinical relevance of these findings.

    Back to top
    Article Information

    Accepted for Publication: June 28, 2020.

    Corresponding Author: Hasan Aytoğan, MD, Department of Ophthalmology, İzmir Tepecik Training and Research Hospital, Yenişehir, Gaziler Cad. No. 468, Konak, İzmir 35020, Turkey (hasan_aytogan@hotmail.com).

    Published Online: August 3, 2020. doi:10.1001/jamaophthalmol.2020.3154

    Author Contributions: Dr Aytoğan had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Drs Aytoğan, Ayıntap, and Özkalay Yılmaz contributed equally.

    Concept and design: Aytoğan.

    Acquisition, analysis, or interpretation of data: All authors.

    Drafting of the manuscript: Aytoğan.

    Critical revision of the manuscript for important intellectual content: All authors.

    Administrative, technical, or material support: All authors.

    Supervision: Ayıntap, Özkalay Yılmaz.

    Conflict of Interest Disclosures: None reported.

    References
    1.
    Wu  F, Zhao  S, Yu  B,  et al.  A new coronavirus associated with human respiratory disease in China.   Nature. 2020;579(7798):265-269. doi:10.1038/s41586-020-2008-3 PubMedGoogle ScholarCrossref
    2.
    Yezli  S., and Otter  J.A.,  Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.   Food Environ Microbiol. 2011; 3: 1–30. doi:10.1007/s12560-011-9056-7Google Scholar
    3.
    Geller  C, Varbanov  M, Duval  RE.  Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies.   Viruses. 2012;4(11):3044-3068. doi:10.3390/v4113044 PubMedGoogle ScholarCrossref
    4.
    van Doremalen  N, Bushmaker  T, Munster  VJ.  Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions.   Euro Surveill. 2013;18(38):19. doi:10.2807/1560-7917.ES2013.18.38.20590PubMedGoogle ScholarCrossref
    5.
    Chan  KH, Peiris  JS, Lam  SY, Poon  LL, Yuen  KY, Seto  WH.  The effects of temperature and relative humidity on the viability of the SARS coronavirus.   Adv Virol. 2011;2011:734690. doi:10.1155/2011/734690 PubMedGoogle Scholar
    6.
    Coulliette  AD, Perry  KA, Edwards  JR, Noble-Wang  JA.  Persistence of the 2009 pandemic influenza A (H1N1) virus on N95 respirators.   Appl Environ Microbiol. 2013;79(7):2148-2155. doi:10.1128/AEM.03850-12 PubMedGoogle ScholarCrossref
    7.
    Bai  Y, Yao  L, Wei  T,  et al.  Presumed asymptomatic carrier transmission of COVID-19.   JAMA. 2020;323(14):1406-1407. doi:10.1001/jama.2020.2565PubMedGoogle ScholarCrossref
    8.
    Moriarty  LF, Plucinski  MM, Marston  BJ,  et al; CDC Cruise Ship Response Team; California Department of Public Health COVID-19 Team; Solano County COVID-19 Team.  Public health responses to COVID-19 outbreaks on cruise ships—worldwide, February-March 2020.   MMWR Morb Mortal Wkly Rep. 2020;69(12):347-352. doi:10.15585/mmwr.mm6912e3PubMedGoogle ScholarCrossref
    9.
    van Doremalen  N, Bushmaker  T, Morris  DH,  et al.  Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1.   N Engl J Med. 2020;382(16):1564-1567. doi:10.1056/NEJMc2004973 PubMedGoogle ScholarCrossref
    10.
    Rabenau  HF, Cinatl  J, Morgenstern  B, Bauer  G, Preiser  W, Doerr  HW.  Stability and inactivation of SARS coronavirus.   Med Microbiol Immunol. 2005;194(1-2):1-6. doi:10.1007/s00430-004-0219-0PubMedGoogle ScholarCrossref
    11.
    Duan  SM, Zhao  XS, Wen  RF,  et al; SARS Research Team.  Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.   Biomed Environ Sci. 2003;16(3):246-255.PubMedGoogle Scholar
    12.
    Yang  Y, Yang  M, Shen  C,  et al. Evaluating the accuracy of different respiratory specimens in the laboratory diagnosis and monitoring the viral shedding of 2019-nCoV infections. Published February 17, 2020. Accessed July 24, 2020. https://www.medrxiv.org/content/10.1101/2020.02.11.20021493v2
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