Conjunctival Swab Findings in 484 COVID-19 Patients in Four Hospital Centers in Slovakia
Abstract
:1. Introduction
2. Materials and Methods
Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Ethics Approval and Consent to Participate
References
- Sohrabi, C.; Alsafi, Z.; O’Neill, N.; Khan, M.; Kerwan, A.; Al-Jabir, A.; Iosifidis, C.; Agha, R. World Health Organization Declares Global Emergency: A Review of the 2019 Novel Coronavirus (COVID-19). Int. J. Surg. 2020, 76, 71–76. [Google Scholar] [CrossRef] [PubMed]
- Vesely, P.; Novakova, E.; Stubna, M.; Trnka, M.; Jurenova, D.; Lyskova, D.; Furda, R.; Plesnikova, P.; Himic, V.; Furdova, A. Coronavirus Disease (COVID-19) and Conjunctival Sac Swab Findings. J. Ophthalmic Inflamm. Infect. 2022, 12, 8. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Li, D.; Fang, J.; Liu, Q.; Cao, W.; Sun, X.; Xu, G. SARS-CoV-2 Receptor ACE2 Is Expressed in Human Conjunctival Tissue, Especially in Diseased Conjunctival Tissue. Ocul. Surf. 2021, 19, 249–251. [Google Scholar] [CrossRef] [PubMed]
- Coroneo, M.T. The Eye as the Discrete but Defensible Portal of Coronavirus Infection. Ocul. Surf. 2021, 19, 176–182. [Google Scholar] [CrossRef] [PubMed]
- Barnett, B.P.; Wahlin, K.; Krawczyk, M.; Spencer, D.; Welsbie, D.; Afshari, N.; Chao, D. Potential of Ocular Transmission of SARS-CoV-2: A Review. Vision 2020, 4, 40. [Google Scholar] [CrossRef]
- Chen, L.; Liu, M.; Zhang, Z.; Qiao, K.; Huang, T.; Chen, M.; Xin, N.; Huang, Z.; Liu, L.; Zhang, G. Ocular Manifestations of a Hospitalised Patient with Confirmed 2019 Novel Coronavirus Disease. Br. J. Ophthalmol. 2020, 104, 748–751. [Google Scholar] [CrossRef]
- Xia, J.; Tong, J.; Liu, M.; Shen, Y.; Guo, D. Evaluation of Coronavirus in Tears and Conjunctival Secretions of Patients with SARS-CoV-2 Infection. J. Med. Virol. 2020, 92, 589–594. [Google Scholar] [CrossRef] [Green Version]
- Sawant, O.B.; Singh, S.; Wright, R.E.; Jones, K.M.; Titus, M.S.; Dennis, E.; Hicks, E.; Majmudar, P.A.; Kumar, A.; Mian, S.I. Prevalence of SARS-CoV-2 in Human Post-Mortem Ocular Tissues. Ocul. Surf. 2021, 19, 322–329. [Google Scholar] [CrossRef]
- Kumar, K.; Prakash, A.A.; Gangasagara, S.B.; Rathod, S.B.L.; Ravi, K.; Rangaiah, A.; Shankar, S.M.; Basawarajappa, S.G.; Bhushan, S.; Neeraja, T.G.; et al. Presence of Viral RNA of SARS-CoV-2 in Conjunctival Swab Specimens of COVID-19 Patients. Indian J. Ophthalmol. 2020, 68, 1015–1017. [Google Scholar] [CrossRef]
- Güemes-Villahoz, N.; Burgos-Blasco, B.; Arribi-Vilela, A.; Arriola-Villalobos, P.; Rico-Luna, C.M.; Cuiña-Sardiña, R.; Delgado-Iribarren, A.; García-Feijoó, J. Detecting SARS-CoV-2 RNA in Conjunctival Secretions: Is It a Valuable Diagnostic Method of COVID-19? J. Med. Virol. 2021, 93, 383–388. [Google Scholar] [CrossRef]
- Zimmerman, K.; Kearns, F.; Tzekov, R. Natural Protection of Ocular Surface from Viral Infections—A Hypothesis. Med. Hypotheses 2020, 143, 110082. [Google Scholar] [CrossRef] [PubMed]
- Belser, J.A.; Rota, P.A.; Tumpey, T.M. Ocular Tropism of Respiratory Viruses. Microbiol. Mol. Biol. Rev. MMBR 2013, 77, 144–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vabret, A.; Mourez, T.; Dina, J.; van der Hoek, L.; Gouarin, S.; Petitjean, J.; Brouard, J.; Freymuth, F. Human Coronavirus NL63, France. Emerg. Infect. Dis. 2005, 11, 1225–1229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peiris, J.S.M.; Yuen, K.Y.; Osterhaus, A.D.M.E.; Stöhr, K. The Severe Acute Respiratory Syndrome. N. Engl. J. Med. 2003, 349, 2431–2441. [Google Scholar] [CrossRef] [Green Version]
- Loon, S.-C.; Teoh, S.C.B.; Oon, L.L.E.; Se-Thoe, S.-Y.; Ling, A.-E.; Leo, Y.-S.; Leong, H.-N. The Severe Acute Respiratory Syndrome Coronavirus in Tears. Br. J. Ophthalmol. 2004, 88, 861–863. [Google Scholar] [CrossRef] [Green Version]
- Chan, W.M.; Yuen, K.S.C.; Fan, D.S.P.; Lam, D.S.C.; Chan, P.K.S.; Sung, J.J.Y. Tears and Conjunctival Scrapings for Coronavirus in Patients with SARS. Br. J. Ophthalmol. 2004, 88, 968–969. [Google Scholar] [CrossRef] [Green Version]
- Yuen, K.S.C.; Chan, W.-M.; Fan, D.S.P.; Chong, K.K.L.; Sung, J.J.Y.; Lam, D.S.C. Ocular Screening in Severe Acute Respiratory Syndrome. Am. J. Ophthalmol. 2004, 137, 773–774. [Google Scholar] [CrossRef]
- Bonn, D. SARS Virus in Tears? Lancet Infect. Dis. 2004, 4, 480. [Google Scholar] [CrossRef]
- Tong, T.; Lai, T.S. The Severe Acute Respiratory Syndrome Coronavirus in Tears. Br. J. Ophthalmol. 2005, 89, 392. [Google Scholar] [CrossRef] [Green Version]
- Wu, P.; Duan, F.; Luo, C.; Liu, Q.; Qu, X.; Liang, L.; Wu, K. Characteristics of Ocular Findings of Patients with Coronavirus Disease 2019 (COVID-19) in Hubei Province, China. JAMA Ophthalmol. 2020, 138, 575–578. [Google Scholar] [CrossRef]
- Loffredo, L.; Pacella, F.; Pacella, E.; Tiscione, G.; Oliva, A.; Violi, F. Conjunctivitis and COVID-19: A Meta-Analysis. J. Med. Virol. 2020, 92, 1413–1414. [Google Scholar] [CrossRef] [PubMed]
- Matsuyama, S.; Nagata, N.; Shirato, K.; Kawase, M.; Takeda, M.; Taguchi, F. Efficient Activation of the Severe Acute Respiratory Syndrome Coronavirus Spike Protein by the Transmembrane Protease TMPRSS2. J. Virol. 2010, 84, 12658–12664. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoffmann, M.; Kleine-Weber, H.; Schroeder, S.; Krüger, N.; Herrler, T.; Erichsen, S.; Schiergens, T.S.; Herrler, G.; Wu, N.-H.; Nitsche, A.; et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell 2020, 181, 271–280.e8. [Google Scholar] [CrossRef] [PubMed]
- Ma, D.; Chen, C.-B.; Jhanji, V.; Xu, C.; Yuan, X.-L.; Liang, J.-J.; Huang, Y.; Cen, L.-P.; Ng, T.K. Expression of SARS-CoV-2 Receptor ACE2 and TMPRSS2 in Human Primary Conjunctival and Pterygium Cell Lines and in Mouse Cornea. Eye 2020, 34, 1212–1219. [Google Scholar] [CrossRef]
- Zhou, L.; Xu, Z.; Castiglione, G.M.; Soiberman, U.S.; Eberhart, C.G.; Duh, E.J. ACE2 and TMPRSS2 Are Expressed on the Human Ocular Surface, Suggesting Susceptibility to SARS-CoV-2 Infection. Ocul. Surf. 2020, 18, 537–544. [Google Scholar] [CrossRef]
- Raboud, J.; Shigayeva, A.; McGeer, A.; Bontovics, E.; Chapman, M.; Gravel, D.; Henry, B.; Lapinsky, S.; Loeb, M.; McDonald, L.C. Risk Factors for SARS Transmission from Patients Requiring Intubation: A Multicentre Investigation in Toronto, Canada. PLoS ONE 2010, 5, e10717. [Google Scholar] [CrossRef]
- Wan, Y.; Shang, J.; Graham, R.; Baric, R.S.; Li, F. Receptor Recognition by the Novel Coronavirus from Wuhan: An Analysis Based on Decade-Long Structural Studies of SARS Coronavirus. J. Virol. 2020, 94, e00127-20. [Google Scholar] [CrossRef] [Green Version]
- Ozturker, Z.K. Conjunctivitis as Sole Symptom of COVID-19: A Case Report and Review of Literature. Eur. J. Ophthalmol. 2021, 31, NP161–NP166. [Google Scholar] [CrossRef]
- Robbins, S.G.; Detrick, B.; Hooks, J.J. Ocular Tropisms of Murine Coronavirus (Strain JHM) after Inoculation by Various Routes. Investig. Ophthalmol. Vis. Sci. 1991, 32, 1883–1893. [Google Scholar]
- Nagata, N.; Iwata-Yoshikawa, N.; Taguchi, F. Studies of Severe Acute Respiratory Syndrome Coronavirus Pathology in Human Cases and Animal Models. Vet. Pathol. 2010, 47, 881–892. [Google Scholar] [CrossRef] [Green Version]
- Martina, B.E.E.; Haagmans, B.L.; Kuiken, T.; Fouchier, R.A.M.; Rimmelzwaan, G.F.; van Amerongen, G.; Peiris, J.S.M.; Lim, W.; Osterhaus, A.D.M.E. Virology: SARS Virus Infection of Cats and Ferrets. Nature 2003, 425, 915. [Google Scholar] [CrossRef] [PubMed]
- Andries, K.; Pensaert, M.B. Immunofluorescence Studies on the Pathogenesis of Hemagglutinating Encephalomyelitis Virus Infection in Pigs after Oronasal Inoculation. Am. J. Vet. Res. 1980, 41, 1372–1378. [Google Scholar] [PubMed]
- Doherty, M.J. Ocular Manifestations of Feline Infectious Peritonitis. J. Am. Vet. Med. Assoc. 1971, 159, 417–424. [Google Scholar] [PubMed]
- Lai, Y.L.; Jacoby, R.O.; Bhatt, P.N.; Jonas, A.M. Keratoconjunctivitis Associated with Sialodacryoadenitis in Rats. Investig. Ophthalmol. 1976, 15, 538–541. [Google Scholar]
- Ulhaq, Z.S.; Soraya, G.V. The Prevalence of Ophthalmic Manifestations in COVID-19 and the Diagnostic Value of Ocular Tissue/Fluid. Graefes Arch. Clin. Exp. Ophthalmol. 2020, 258, 1351–1352. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Y.; Duan, C.; Zeng, Y.; Tong, Y.; Nie, Y.; Yang, Y.; Chen, Z.; Chen, C. Ocular Findings and Proportion with Conjunctival SARS-CoV-2 in COVID-19 Patients. Ophthalmology 2020, 127, 982–983. [Google Scholar] [CrossRef]
- Gunduz, A.; Firat, M.; Turkoglu, G. Comparison of the Simultaneous Conjunctiva and Oropharynx-Nasopharynx Swab Results in Patients Applying to the SARS-CoV-2 Outpatient Clinic for the First Time. J. Med. Virol. 2021, 93, 4516–4522. [Google Scholar] [CrossRef]
- Nasiri, N.; Sharifi, H.; Bazrafshan, A.; Noori, A.; Karamouzian, M.; Sharifi, A. Ocular Manifestations of COVID-19: A Systematic Review and Meta-Analysis. J. Ophthalmic Vis. Res. 2021, 16, 103–112. [Google Scholar] [CrossRef]
- Jones, L.; Walsh, K.; Willcox, M.; Morgan, P.; Nichols, J. The COVID-19 Pandemic: Important Considerations for Contact Lens Practitioners. Contact Lens Anterior Eye 2020, 43, 196–203. [Google Scholar] [CrossRef]
- Lai, T.H.; Tang, E.W.; Chau, S.K.; Fung, K.S.; Li, K.K. Stepping up Infection Control Measures in Ophthalmology during the Novel Coronavirus Outbreak: An Experience from Hong Kong. Graefes Arch. Clin. Exp. Ophthalmol. 2020, 258, 1049–1055. [Google Scholar] [CrossRef] [Green Version]
- Romano, M.R.; Montericcio, A.; Montalbano, C.; Raimondi, R.; Allegrini, D.; Ricciardelli, G.; Angi, M.; Pagano, L.; Romano, V. Facing COVID-19 in Ophthalmology Department. Curr. Eye Res. 2020, 45, 653–658. [Google Scholar] [CrossRef] [PubMed]
- Sadhu, S.; Agrawal, R.; Pyare, R.; Pavesio, C.; Zierhut, M.; Khatri, A.; Smith, J.R.; de Smet, M.D.; Biswas, J. COVID-19: Limiting the Risks for Eye Care Professionals. Ocul. Immunol. Inflamm. 2020, 28, 714–720. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sengupta, S.; Honavar, S.G.; Sachdev, M.S.; Sharma, N.; Kumar, A.; Ram, J.; Shetty, R.; Rao, G.S.; Ramasamy, K.; Khanna, R. All India Ophthalmological Society–Indian Journal of Ophthalmology Consensus Statement on Preferred Practices during the COVID-19 Pandemic. Indian J. Ophthalmol. 2020, 68, 711. [Google Scholar] [PubMed]
- Aggarwal, K.; Agarwal, A.; Jaiswal, N.; Dahiya, N.; Ahuja, A.; Mahajan, S.; Tong, L.; Duggal, M.; Singh, M.; Agrawal, R.; et al. Ocular Surface Manifestations of Coronavirus Disease 2019 (COVID-19): A Systematic Review and Meta-Analysis. PLoS ONE 2020, 15, e0241661. [Google Scholar] [CrossRef]
- Shimmura, S.; Shimazaki, J.; Tsubota, K. Results of a Population-Based Questionnaire on the Symptoms and Lifestyles Associated with Dry Eye. Cornea 1999, 18, 408–411. [Google Scholar] [CrossRef]
- Marinho, P.M.; Marcos, A.A.; Romano, A.C.; Nascimento, H.; Belfort, R. Retinal Findings in Patients with COVID-19. Lancet 2020, 395, 1610. [Google Scholar] [CrossRef]
- Tostmann, A.; Bradley, J.; Bousema, T.; Yiek, W.-K.; Holwerda, M.; Bleeker-Rovers, C.; Ten Oever, J.; Meijer, C.; Rahamat-Langendoen, J.; Hopman, J. Strong Associations and Moderate Predictive Value of Early Symptoms for SARS-CoV-2 Test Positivity among Healthcare Workers, the Netherlands, March 2020. Eurosurveillance 2020, 25, 2000508. [Google Scholar] [CrossRef]
- Zhang, X.; Chen, X.; Chen, L.; Deng, C.; Zou, X.; Liu, W.; Yu, H.; Chen, B.; Sun, X. The Evidence of SARS-CoV-2 Infection on Ocular Surface. Ocul. Surf. 2020, 18, 360–362. [Google Scholar] [CrossRef]
- Jin, Y.-P.; Trope, G.E.; El-Defrawy, S.; Liu, E.Y.; Buys, Y.M. Ophthalmology-Focused Publications and Findings on COVID-19: A Systematic Review. Eur. J. Ophthalmol. 2021, 31, 1677–1687. [Google Scholar] [CrossRef]
Gender | Number | Gestational Age a (Years) | Non-Mechanically Ventilated Patients b | Mechanically Ventilated Patients b | Positive Result from the Conjunctival Sac | Eye Symptoms b |
---|---|---|---|---|---|---|
Male | 264 | 65.59 ± 13.43 | 215 (26) | 5 (0) | 31 | 36 (4) |
Female | 220 | 68.01 ± 13.71 | 179 (22) | 6 (2) | 27 | 23 (4) |
Overall | 484 | 66.69 ± 13.59 | 394 (48) | 11 (2) | 58 | 59 (8) |
Age Range (Years) | Male a | Female a | Non-Mechanically Ventilated Patients b | Mechanically Ventilated Patients b | Eye Symptoms b |
---|---|---|---|---|---|
21–30 | 1 (0) | 1 (0) | 1 (1) | 0 (0) | 0 (0) |
31–40 | 9 (0) | 7 (0) | 8 (5) | 0 (0) | 0 (0) |
41–50 | 22 (1) | 17 (1) | 16 (13) | 0 (1) | 8 (1) |
51–60 | 60 (6) | 32 (5) | 46 (25) | 2 (3) | 5 (8) |
61–70 | 71 (6) | 64 (6) | 49 (55) | 3 (1) | 9 (9) |
71–80 | 64 (9) | 58 (9) | 59 (45) | 0 (1) | 9 (3) |
81–90 | 30 (6) | 33 (5) | 29 (29) | 0 (0) | 5 (1) |
>91 | 7 (3) | 8 (1) | 7 (6) | 0 (0) | 0 (1) |
Gender | Number | CT Value in Nasopharynx a | CT Value in Conjunctiva a | p |
---|---|---|---|---|
Male | 27 | 22.98 ± 5.14 | 29.53 ± 4.11 | <0.001 |
Female | 31 | 22.47 ± 4.98 | 32.32 ± 3.87 | <0.001 |
Overall | 58 | 22.71 ± 5.01 | 30.98 ± 4.19 | <0.001 |
Age Range (Years) | Male | Female | ||||
---|---|---|---|---|---|---|
Number | CT Value in Nasopharynx a | CT Value in Conjunctiva a | Number | CT Value in Nasopharynx a | CT Value in Conjunctiva a | |
40–49 | 1 | 29.80 ± 0.00 | 33.54 ± 0.00 | 1 | 18.50 ± 0.00 | 32.02 ± 0.00 |
50–59 | 6 | 20.87 ± 5.08 | 31.13 ± 4.12 | 5 | 21.78 ± 5.41 | 35.35 ± 2.17 |
60–69 | 6 | 21.47 ± 6.60 | 31.11 ± 4.97 | 6 | 26.39 ± 5.01 | 33.28 ± 5.08 |
70–79 | 9 | 24.06 ± 6.33 | 29.81 ± 3.92 | 9 | 21.96 ± 4.62 | 33.05 ± 4.22 |
80–89 | 6 | 23.60 ± 3.22 | 29.09 ± 5.82 | 5 | 22.49 ± 4.12 | 31.41 ± 1.96 |
>90 | 3 | 21.51 ± 4.78 | 29.99 ± 3.62 | 1 | 14.00 ± 0.00 | 22.56 ± 0.00 |
Bratislava | Zilina | Nitra | Nove Zamky | Overall | ||||||
---|---|---|---|---|---|---|---|---|---|---|
Number | % a | Number | % a | Number | % a | Number | % | Number | % a | |
Male | 76 | 51.01 | 70 | 59.83 | 58 | 58.59 | 60 | 50.42 | 264 | 54.55 |
Female | 73 | 48.99 | 47 | 40.17 | 41 | 41.41 | 59 | 49.58 | 220 | 45.45 |
Overall | 149 | 100 | 117 | 100 | 99 | 100 | 119 | 100 | 484 | 100 |
Positive d overall | 25 | 16.78 | 9 | 7.69 | 9 | 9.09 | 15 | 12.61 | 58 | 11.98 |
Positive d male | 13 | 8.72 | 3 | 2.56 | 7 | 7.07 | 8 | 6.72 | 31 | 6.40 |
Positive d female | 12 | 8.05 | 6 | 5.13 | 2 | 2.02 | 7 | 5.88 | 27 | 5.58 |
Negative d overall | 115 | 77.18 | 108 | 92.31 | 90 | 90.91 | 104 | 87.39 | 417 | 86.16 |
Negative d male | 58 | 38.93 | 67 | 57.26 | 51 | 51.52 | 52 | 43.70 | 228 | 47.11 |
Negative d female | 57 | 38.26 | 41 | 35.04 | 39 | 39.39 | 52 | 43.70 | 189 | 39.05 |
Unclear overall | 9 | 6.04 | - | - | - | 9 | 1.86 | |||
Unclear male | 5 | 3.36 | - | - | - | 5 | 1.03 | |||
Unclear female | 4 | 2.68 | - | - | - | 4 | 0.83 | |||
Eye symptoms male | 1 | 0.67 | 27 | 23.08 | 5 | 5.05 | 3 | 2.52 | 36 | 7.42 |
Eye symptoms female | 1 | 0.67 | 14 | 11.97 | 6 | 6.06 | 2 | 1.68 | 23 | 4.74 |
Eye symptoms overall | 2 | 1.33 | 41 | 35.04 | 11 | 11.11 | 5 | 4.20 | 59 | 12.16 |
Number b | Number b | Number b | Number b | Number b | ||||||
Mean duration c of interval in all patients | 6.13 ± 4.86 | 7.20 ± 3.18 | 13.53 ± 7.13 | 10.79 ± 6.26 | 9.01 ± 6.14 | |||||
Mean duration c of interval in positive d patients | 5.88 ± 4.68 | 5.89 ± 2.57 | 13.11 ± 7.72 | 9.50 ± 5.52 | 7.85 ± 5.78 | |||||
Mean duration c of interval in negative d patients | 6.27 ± 4.92 | 7.31 ± 3.21 | 13.57 ± 7.12 | 10.98 ± 6.36 | 9.26 ± 6.18 | |||||
Average age | 70 ± 13.09 | 62.41 ± 13.60 | 65.59 ± 12.67 | 67.71 ± 13.86 | 66.67 ± 13.59 | |||||
The average age of the positive d patients | 73.76 ± 14.11 | 69.00 ± 13.35 | 65.33 ± 10.97 | 71.33 ± 9.51 | 71.09 ± 12.53 | |||||
The average age of the negative d patients | 68.71 ± 12.66 | 61.86 ± 13.53 | 65.62 ± 12.88 | 67.19 ± 14.34 | 65.85 ± 13.58 |
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Furdova, A.; Vesely, P.; Trnka, M.; Novakova, E.; Stubna, M.; Furda, R.; Branikova, L.; Pridavkova, Z. Conjunctival Swab Findings in 484 COVID-19 Patients in Four Hospital Centers in Slovakia. Vision 2022, 6, 46. https://doi.org/10.3390/vision6030046
Furdova A, Vesely P, Trnka M, Novakova E, Stubna M, Furda R, Branikova L, Pridavkova Z. Conjunctival Swab Findings in 484 COVID-19 Patients in Four Hospital Centers in Slovakia. Vision. 2022; 6(3):46. https://doi.org/10.3390/vision6030046
Chicago/Turabian StyleFurdova, Alena, Pavol Vesely, Michal Trnka, Elena Novakova, Michal Stubna, Robert Furda, Lubica Branikova, and Zuzana Pridavkova. 2022. "Conjunctival Swab Findings in 484 COVID-19 Patients in Four Hospital Centers in Slovakia" Vision 6, no. 3: 46. https://doi.org/10.3390/vision6030046
APA StyleFurdova, A., Vesely, P., Trnka, M., Novakova, E., Stubna, M., Furda, R., Branikova, L., & Pridavkova, Z. (2022). Conjunctival Swab Findings in 484 COVID-19 Patients in Four Hospital Centers in Slovakia. Vision, 6(3), 46. https://doi.org/10.3390/vision6030046