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Id Subject Object Predicate Lexical cue
T1 0-49 Sentence denotes Ocular manifestations of coronavirus disease 2019
T2 51-59 Sentence denotes Abstract
T3 60-67 Sentence denotes Purpose
T4 68-262 Sentence denotes Coronavirus disease 2019 (COVID-19) is an ongoing global public health problem, and most of the COVID-19 research is focused mainly on the respiratory system because of life-threatening results.
T5 263-371 Sentence denotes However, manifestations in other organs should not be ignored since they can also be a mode of transmission.
T6 372-541 Sentence denotes We sought to describe the ocular manifestations of COVID-19 and investigate the association between ocular involvement and clinical presentation and laboratory outcomes.
T7 543-550 Sentence denotes Methods
T8 551-634 Sentence denotes This cross-sectional study was conducted between March 1, 2020, and April 30, 2020.
T9 635-744 Sentence denotes Ninety-three sequentially hospitalized and clinically confirmed COVID-19 patients were included in the study.
T10 745-836 Sentence denotes The systemic and ocular symptoms, clinical findings, and laboratory outcomes were recorded.
T11 838-845 Sentence denotes Results
T12 846-924 Sentence denotes Of the 93 COVID-19 patients, 54 (58.1%) were male, and 39 (41.9%) were female.
T13 925-988 Sentence denotes Mean age of the patients was 39.4 ± 21.9 (min 7, max 88) years.
T14 989-1051 Sentence denotes Twenty patients (n 21.5%) had at least one ocular abnormality.
T15 1052-1227 Sentence denotes Most common findings included hyperemia (n = 20), epiphora (n = 9), increased secretion (n = 6), chemosis (n = 3), follicular conjunctivitis (n = 2), and episcleritis (n = 2).
T16 1228-1275 Sentence denotes The most common symptom was photophobia (n 15).
T17 1276-1447 Sentence denotes Patients with ocular involvement were more likely to have higher neutrophil counts (p = 0.001), and increased CRP (p < 0.001), PCT (p = 0.001), and ESR levels (p < 0.001).
T18 1448-1545 Sentence denotes Mean lymphocyte count was statistically lower in patients with ocular manifestations (p = 0.001).
T19 1546-1694 Sentence denotes Mean age and number of patients with fever over 37.3 °C in the ocular involvement group was found to be higher (p < 0.001, p = 0.006, respectively).
T20 1696-1706 Sentence denotes Conclusion
T21 1707-1859 Sentence denotes Older age, high fever, increased neutrophil/lymphocyte ratio, and high levels of acute phase reactants seemed to be risk factors for ocular involvement.
T22 1861-1873 Sentence denotes Introduction
T23 1874-1982 Sentence denotes In December 2019, China reported a pneumonia outbreak in Wuhan, a city with more than 11 million people [1].
T24 1983-2214 Sentence denotes A new coronavirus (COV) was identified as the causative organism—namely, novel coronavirus, nCOV-Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2)—and the disease was named as the Coronavirus Disease 2019 (COVID-19) [2].
T25 2215-2418 Sentence denotes After its introduction, World Health Organization declared the situation as a public health emergency of international concern and published suggestions for protection and prevention of transmission [3].
T26 2419-2487 Sentence denotes The first case in Turkey was officially announced on March 11, 2020.
T27 2488-2594 Sentence denotes To date, COVID-19 has confirmed to affect a total of 115000 patients in Turkey with more than 3000 deaths.
T28 2595-2725 Sentence denotes Due to the life-threatening nature of its complications, most of the research about COVID-19 mainly focuses on respiratory system.
T29 2726-2837 Sentence denotes However, since other organ involvements might be alternative routes of transmissions, they must not be ignored.
T30 2838-2885 Sentence denotes Seven types of CoVs are known to infect humans:
T31 2886-2960 Sentence denotes 229E, NL63, OC 43, HKU, MERS-CoV, SARS-CoV, and the recent SARS-CoV-2 [4].
T32 2961-3117 Sentence denotes Most of these CoVs cause infections in the respiratory tract but also known to have manifestations in the gastrointestinal system and ocular tissues [5, 6].
T33 3118-3179 Sentence denotes HCoV-NL63 and SARS-CoV are known to affect the ocular system.
T34 3180-3292 Sentence denotes There have been reports of cases with conjunctivitis and bronchiolitis between 2000 and 2003 with HCoV-NL63 [7].
T35 3293-3431 Sentence denotes In addition, in 2004, SARS-CoV-RNA was identified in tear samples of three patients suggesting that the virus can be present in tears [5].
T36 3432-3687 Sentence denotes Theories, including the conjunctiva being the direct inoculation site of pathogen-loaded droplets, migration of the infection from the respiratory tract through the nasolacrimal duct or even hematogenous infection of the lacrimal gland, were proposed [5].
T37 3688-3870 Sentence denotes Genomic and structural analyses show a similar receptor-binding motive between SARS-CoV and SARS-CoV-2 with resembling pathologic features and epidemiological characteristics [8, 9].
T38 3871-3947 Sentence denotes As a result, a similar involvement of the ocular tissues has been suspected.
T39 3948-4065 Sentence denotes Nevertheless, there have only been few reports about the ophthalmic manifestations of the recent SARS-CoV-2 [10, 11].
T40 4066-4251 Sentence denotes The purpose of our study is to investigate ocular findings and symptoms of clinically confirmed COVID-19 patients and assess the relationship with those findings and laboratory results.
T41 4253-4274 Sentence denotes Materials and methods
T42 4275-4439 Sentence denotes This cross-sectional study was conducted at the Kars Harakani State Hospital, Kars, Turkey, in accordance with the ethical standards of the Declaration of Helsinki.
T43 4440-4555 Sentence denotes The study protocol was approved by the institutional board of the Okan University Medical Faculty ethics committee.
T44 4556-4720 Sentence denotes Between March 11th and April 30th, 2020, 93 consecutive patients who were hospitalized in Kars Harakani State Hospital with the diagnosis of COVID-19 were included.
T45 4721-4984 Sentence denotes The COVID-19 diagnosis was made according to real time reverse transcriptase-polymerase chain reaction (RT-PCR) assay of respiratory specimens which revealed positive results for SARS-CoV-2 nucleic acid and thorax CT findings consistent with viral pneumonia [12].
T46 4985-5073 Sentence denotes The COVID-19 diagnosis was confirmed with RT-PCR in all included patients in this study.
T47 5074-5376 Sentence denotes The patient symptoms, fever at presentation, thorax computerized tomography (CT) scans, neutrophil, lymphocyte and monocyte counts, C-reactive protein (CRP), pro-calcitonin (PCT), erythrocyte sedimentation rate (ESR), lactate dehydrogenase (LDH), creatine kinase (CK), and d-dimer levels were recorded.
T48 5377-5421 Sentence denotes Older age was accepted as 65 years or older.
T49 5422-5464 Sentence denotes Fever was classified as 37.3 °C or higher.
T50 5465-5531 Sentence denotes Ocular findings and symptoms were evaluated at hospital admission.
T51 5532-5708 Sentence denotes Ophthalmological examination including ocular surface and anterior segment assessment was performed by the same experienced clinician using a binocular indirect ophthalmoscope.
T52 5709-5752 Sentence denotes Ocular symptoms and findings were recorded.
T53 5753-5847 Sentence denotes Statistical analyses were performed with SPSS Statistics (Version 22.0, Armonk, NY: IBM Corp).
T54 5848-5936 Sentence denotes The assumption of normal distribution of data was tested by the Kolmogorov-Smirnov test.
T55 5937-6005 Sentence denotes Association of descriptive data was tested with the chi-square test.
T56 6006-6094 Sentence denotes Differences in the outcomes between the groups were tested with the Mann–Whitney U test.
T57 6095-6161 Sentence denotes A p value less than 0.05 was considered statistically significant.
T58 6163-6170 Sentence denotes Results
T59 6171-6255 Sentence denotes Ninety-three patients with clinically confirmed COVID-19 were included in the study.
T60 6256-6324 Sentence denotes Of the 93 patients, 54 (58.1%) were male and 39 (41.9%) were female.
T61 6325-6388 Sentence denotes Mean age of the patients was 39.4 ± 21.9 (min 7, max 88) years.
T62 6389-6554 Sentence denotes Ninety-two patients (98.9%) tested positive for SARS-CoV-2 by RT-PCR of nasopharyngeal swabs; while 1 (1.1%) was positive in the RT-PCR of the endotracheal aspirate.
T63 6555-6769 Sentence denotes Twenty (21.5%) patients had fever, 18 (19.4%) patients had cough, 3 (3.2%) patients had respiratory distress, 2 (2.2%) patients had headache, and 50 (53.8%) patients had no symptoms at presentation to the hospital.
T64 6770-7004 Sentence denotes Fifty-eight (62.4%) patients had no sign of abnormality at thorax CT, whereas 23 (24.7%) patients had typical CT findings of SARS CoV-2 pneumonia, and 12 (12.9%) patients had possible SARS CoV-2 pneumonia according to the CT findings.
T65 7005-7127 Sentence denotes Five patients were intubated due to respiratory distress and 4 of them died due to SARS CoV-2 pneumonia and comorbidities.
T66 7128-7239 Sentence denotes Table 1 represents age, fever, and the laboratory findings of the patients with and without ocular involvement.
T67 7240-7438 Sentence denotes Mean neutrophil count, neutrophil to lymphocyte ratio, CRP, PCT, and ESR levels were significantly higher in patients with ocular involvement; whereas, mean lymphocyte count was significantly lower.
T68 7439-7590 Sentence denotes No significant difference was observed between patients with and without ocular involvement regarding mean monocyte count, LDH, CK, and d-dimer levels.
T69 7591-7690 Sentence denotes Table 1 Age, fever, and the laboratory findings of the patients with and without ocular involvement
T70 7691-7785 Sentence denotes Patients with ocular involvement (n = 20) Patients without ocular involvement (n = 73) P value
T71 7786-7829 Sentence denotes Age (years) 60.7 ± 19.8 33.6 ± 18.6 <0.001*
T72 7830-7880 Sentence denotes Fever over 37.3 °C (n) 12 (60.0%) 8 (11.0%) 0.006*
T73 7881-7937 Sentence denotes Neutrophil (/mm3) 6453.0 ± 4856.7 3662.2 ± 2132.3 0.001*
T74 7938-7993 Sentence denotes Lymphocyte (/mm3) 1368.0 ± 680.2 2246.5 ± 1173.3 0.001*
T75 7994-8050 Sentence denotes Neutrophil/lymphocyte ratio 7.5 ± 11.5 2.3 ± 2.8 <0.001*
T76 8051-8100 Sentence denotes Monocyte (/mm3) 471.5 ± 194.4 480.8 ± 207.5 0.918
T77 8101-8141 Sentence denotes CRP (mg/L) 55.4 ± 48.6 6.1 ± 8.8 <0.001*
T78 8142-8183 Sentence denotes PCT (μg/L) 0.30 ± 0.47 0.08 ± 0.11 0.001*
T79 8184-8227 Sentence denotes ESR (mm/hr) 42.7 ± 20.6 15.1 ± 13.3 <0.001*
T80 8228-8270 Sentence denotes LDH (U/L) 308.6 ± 132.8 242.1 ± 97.6 0.094
T81 8271-8312 Sentence denotes CK (U/L) 109.7 ± 105.9 110.1 ± 97.9 0.389
T82 8313-8362 Sentence denotes d-dimer (μg/L) 1314.2 ± 611.3 789.9 ± 658.4 0.492
T83 8363-8488 Sentence denotes CRP C-reactive protein, PCT pro-calcitonin, ESR erythrocyte sedimentation rate, LDH lactate dehydrogenase, CK creatine kinase
T84 8489-8515 Sentence denotes *Statistically significant
T85 8516-8580 Sentence denotes Table 2 represents ocular findings and symptoms of the patients.
T86 8581-8828 Sentence denotes Hyperemia was found to be associated with high fever (p = 0.006), typical radiological findings of SARS CoV-2 pneumonia (p = 0.046), high ESR and CRP (p < 0.001 for all), PCT levels (p = 0.001) and neutrophil to lymphocyte ratio (NTL) (p < 0.001).
T87 8829-9117 Sentence denotes Epiphora and increased secretion were found to be associated with high fever (p = 0.012, p = 0.006, respectively), high ESR (p = 0.001, p = 0.023, respectively), CRP (p < 0.001, p = 0.001 respectively), PCT (p = 0.002, p = 0.004 respectively), and NTL (p = 0.001, p < 0.001 respectively).
T88 9118-9216 Sentence denotes Chemosis was positively correlated with high CRP (p = 0.017), PCT (p = 0.39), and NTL (p = 0.008).
T89 9217-9406 Sentence denotes Follicular conjunctivitis was also correlated with high fever (p = 0.037), high neutrophil count (p < 0.001), ESR (p = 0.001), and CRP (p < 0.001), PCT (p = 0.001) and high NTL (p = 0.001).
T90 9407-9517 Sentence denotes Episcleritis was found to be associated with higher d-dimer (p = 0.017), PCT (p = 0.045), and CRP (p = 0.020).
T91 9518-9620 Sentence denotes No ocular finding was associated with gender, LDH or CK levels, and monocyte count (p > 0.05 for all).
T92 9621-9666 Sentence denotes Table 2 Ocular manifestations of the patients
T93 9667-9676 Sentence denotes Value (n)
T94 9677-9692 Sentence denotes Ocular findings
T95 9693-9714 Sentence denotes  Hyperemia 20 (21.5%)
T96 9715-9733 Sentence denotes  Epiphora 9 (9.7%)
T97 9734-9763 Sentence denotes  Increased secretion 6 (6.5%)
T98 9764-9782 Sentence denotes  Chemosis 3 (3.2%)
T99 9783-9818 Sentence denotes  Follicular conjunctivitis 8 (8.6%)
T100 9819-9841 Sentence denotes  Episcleritis 2 (2.2%)
T101 9842-9857 Sentence denotes Ocular symptoms
T102 9858-9881 Sentence denotes  Photophobia 15 (16.1%)
T103 9882-9903 Sentence denotes  Itchiness 13 (15.7%)
T104 9904-9931 Sentence denotes  Burning sensation 7 (8.4%)
T105 9932-9956 Sentence denotes  Gritty feeling 5 (6.0%)
T106 9957-9981 Sentence denotes  Blurred vision 4 (4.8%)
T107 9983-9993 Sentence denotes Discussion
T108 9994-10089 Sentence denotes Ocular involvement with Coronavirus family has been shown in various publications [10, 13, 14].
T109 10090-10297 Sentence denotes On January 22, 2020, when a visiting doctor in Wuhan developed conjunctivitis, and later yielded positive for SARS-CoV-2, call for research on ocular transmission and involvement of SARS-CoV-2 was made [14].
T110 10298-10473 Sentence denotes In a prospective study by Xia et al. [10], tear and conjunctival secretions of 30 COVID-19 patients were collected, and the presence of the virus was evaluated by RT-PCR [10].
T111 10474-10714 Sentence denotes Virus was detected in only one patient’s conjunctival scrapes who had conjunctivitis at the time of specimen collection; therefore, it was proposed that the virus only existed in the tear and conjunctiva of the patients with conjunctivitis.
T112 10715-11015 Sentence denotes On the other hand, in the same study, it was stated that the sample volume of tear and conjunctival secretion might be insufficient for RT-PCR detection, and therefore, the possibility of viral particles’ presence in tears and conjunctiva should not be ignored in patients without conjunctivitis.[10]
T113 11016-11165 Sentence denotes In the present study, we reported the ocular findings and symptoms of COVID-19 patients and risk factors associated with those ocular manifestations.
T114 11166-11264 Sentence denotes Results of our study suggest that 20.5% of the COVID patients had at least one ocular abnormality.
T115 11265-11443 Sentence denotes Mean age, fever, neutrophil count, CRP, PCT, and ESR levels were significantly higher in patients with ocular involvement; whereas, mean lymphocyte count was significantly lower.
T116 11444-11612 Sentence denotes The aggressive inflammatory response is a significant component in the pathophysiology of SARS-CoV-2 infection, strongly implicated in the resulting airway damage [15].
T117 11613-11723 Sentence denotes Severity of the disease is reported to be not only due to the viral infection but also the host response [16].
T118 11724-11885 Sentence denotes There are many studies highlighting the role of inflammatory markers such as ESR, CRP, and PCT to predict the onset of an inflammatory process or infection [17].
T119 11886-12037 Sentence denotes In the case of SARS-CoV-2 infection, many studies demonstrated that most of the patients present with elevated levels of acute immune markers [18, 19].
T120 12038-12147 Sentence denotes C-reactive protein begins to rise within 4–6 h in settings of inflammation and has a half-life of 4–7 h [20].
T121 12148-12231 Sentence denotes Therefore, serum level of CRP is considered to be a measure of active inflammation.
T122 12232-12375 Sentence denotes CRP levels were found to be positively correlated with the diameter of lung lesions and severity of the presentation in COVID-19 patients [21].
T123 12376-12530 Sentence denotes In our study, all of the ocular findings were correlated with high CRP levels which may indicate active inflammatory response and severity of the disease.
T124 12531-12671 Sentence denotes Procalcitonin is a peptide precursor of calcitonin, released primarily by lung and intestine, in response to bacterial toxins and cytokines.
T125 12672-12845 Sentence denotes Production of PCT is amplified during bacterial infections but downregulated during viral infections which make it a particularly interesting acute inflammatory marker [22].
T126 12846-12988 Sentence denotes Levels of PCT become detectable in patient’s serum in 3–6 h after onset of inflammation and remain elevated for 12–36 h after resolution [22].
T127 12989-13133 Sentence denotes A metaanalysis of the literature suggests that serial PCT measurement may be beneficial to evaluate progression towards a more severe form [23].
T128 13134-13245 Sentence denotes The production of PCT is inhibited by interferon-γ, whose concentration increases during viral infections [24].
T129 13246-13518 Sentence denotes PCT levels remain within the reference range in several patients with noncomplicated SARS-CoV-2 infection, whereas substantially increase in the severe form of the disease, possibly secondary to a bacterial coinfection which contributes to complicate the clinical picture.
T130 13519-13718 Sentence denotes Procalcitonine levels of the patients with ocular symptoms were higher than the patients without ocular involvement, which may also be indicative for the severity of the disease in those individuals.
T131 13719-13815 Sentence denotes Patients with ocular manifestations had higher ESR levels according to the results of our study.
T132 13816-13920 Sentence denotes Erythrocyte sedimentation rate typically begins to increase within 24 h after the onset of inflammation.
T133 13921-14088 Sentence denotes ESR can be a useful tool to aid in the diagnosis and management of certain specific situations, like inflammation or infection, but like CRP it lacks specificity [25].
T134 14089-14164 Sentence denotes Elder patients seemed to be at certain risk for developing ocular symptoms.
T135 14165-14359 Sentence denotes This may be secondary to the already existing age related changes in the ocular tissues of the older population such as dry eye disease, meibomian gland dysfunction, or demodex infestation [26].
T136 14360-14531 Sentence denotes It may be expected that ocular problems would be exacerbated in older adults, where the communication between innate and adaptive immunity is known to be compromised [27].
T137 14532-14624 Sentence denotes The pathogenesis and organ manifestations of SARS-CoV-2 virus are not fully understood [28].
T138 14625-14757 Sentence denotes Cytokine storm and viral evasion of cellular immune responses are considered to have crucial roles in the severity of COVID-19 [29].
T139 14758-14961 Sentence denotes In this study, patients with COVID-19 who had ocular manifestations had significantly high levels of CRP, PCT, and ESR, perhaps as a result of the active immune response of the host and disease severity.
T140 14962-15056 Sentence denotes This may partly explain the positive association between high fever and ocular manifestations.
T141 15057-15218 Sentence denotes Lymphocytopenia and increased levels of neutrophils have been reported to reflect an enhanced inflammatory process and suggest a poor prognosis in COVID-19 [28].
T142 15219-15350 Sentence denotes In our group, patients with higher neutrophil-to-lymphocyte ratio seemed to be in higher risk for developing ocular manifestations.
T143 15351-15459 Sentence denotes This can also be secondary to the severity of the disease with generalized aggressive inflammatory response.
T144 15460-15559 Sentence denotes Limited sample size and absence of conjunctival RT-PCR evaluation are the limitations of our study.
T145 15560-15717 Sentence denotes A larger cohort study of patients with COVID-19 from multiple centers would help to further define the ocular manifestations and risk factors of the disease.
T146 15718-15909 Sentence denotes Regardless, the findings of our study are the preliminary results shared in an effort to serve as a starting platform for research into ocular involvement immunological responses of COVID-19.
T147 15910-16083 Sentence denotes Older age, high fever, increased neutrophil/lymphocyte ratio, and high levels of acute phase reactants were associated with greater risk of developing ocular manifestations.
T148 16084-16281 Sentence denotes Care must be taken when evaluating patients with those characteristics to prevent ocular complications and viral spread, since other organ involvements might be alternative routes of transmissions.
T149 16282-16415 Sentence denotes As the current pandemic continues, a better understanding of both the transmission routes and manifestations of COVID-19 will emerge.
T150 16417-16488 Sentence denotes This article is part of topical collection on Perspectives on COVID-19.
T151 16489-16505 Sentence denotes Publisher’s note
T152 16506-16624 Sentence denotes Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
T153 16626-16659 Sentence denotes Availability of Data and Material
T154 16660-16762 Sentence denotes The data supporting the findings of this study are available from the corresponding author on request.
T155 16764-16785 Sentence denotes Authors’ contribution
T156 16786-16895 Sentence denotes All authors contributed to the study conception, design, material preparation, data collection, and analysis.
T157 16896-17032 Sentence denotes The first draft of the manuscript was written by Basak Bostanci Ceran, and all authors commented on previous versions of the manuscript.
T158 17033-17084 Sentence denotes All authors read and approved the final manuscript.
T159 17086-17119 Sentence denotes Compliance with ethical standards
T160 17121-17141 Sentence denotes Conflict of Interest
T161 17142-17201 Sentence denotes The authors declare that they have no conflict of interest.
T162 17203-17218 Sentence denotes Ethics Approval
T163 17219-17246 Sentence denotes The study protocol (Number:
T164 17247-17357 Sentence denotes 91412548-899) was approved by the institutional board of the Okan University Medical Faculty ethics committee.