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\begin{document}

\title{RELATIONSHIP BETWEEN OCULAR FINDINGS AND LABORATORY DATA IN PATIENTS
WITH HOSPITALIZED COVID-19 PATIENTS}



\author[1]{Emine elibol}%
\author[2]{Medine Güneş}%
\author[3]{AYŞE şabablı çetin}%
\affil[1]{Affiliation not available}%
\affil[2]{İstanbul Medeniyet Üniversitesi Tip Fakültesi}%
\affil[3]{Sancaktepe Şehit Prof Dr Ilhan Varank Training and Research Hospital}%


\vspace{-1em}



  
  \date{May 18, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Purpose To investigate the relationship between laboratory blood
parameters and ocular findings in hospitalized moderate or severe
COVID-19 patients. Methods Ophthalmologic examination of 215 patients
who were hospitalized with the diagnosis of COVID-19 was performed in
their beds and their ocular findings were noted. Blood parameters were
compared in patients with and without conjunctivitis like symptoms.
Results Conjunctivitis like inflammatory findings were detected in 15
(7.44\%) of 215 moderate or severe COVID-19 patients. There was no
difference between the patients with and without ocular findings in
terms of laboratory findings such as WBCs, neutrophil counts, lymphocyte
counts, NLR, LDH, procalcitonin, D-dimer, CRP, and ferritin. Conclusion
There was a significant relationship between COVID-19 and an acute
conjunctival inflammatory response. Blood parameters that determined
progression in patients with COVID-19 were not significant in terms of
ocular findings.%
\end{abstract}%



\sloppy


\textbf{RELATIONSHIP BETWEEN OCULAR FINDINGS AND LABORATORY DATA IN
PATIENTS WITH HOSPITALIZED COVID-19 PATIENTS}

1. Emine Savran Elibol, MD (Corresponding Author)

Medeniyet University, G\selectlanguage{ngerman}öztepe Research and Education Hospital,
Department of Ophtalmology, \selectlanguage{polish}İ\selectlanguage{english}stanbul, Turkey

Email: \emph{s\_emine@yahoo.com}

2. Medine G\selectlanguage{ngerman}üne\selectlanguage{polish}ş, \selectlanguage{english}MD

Medeniyet University, G\selectlanguage{ngerman}öztepe Research and Education Hospital,
Department of Ophtalmology, \selectlanguage{polish}İ\selectlanguage{english}stanbul, Turkey

3. Ay\selectlanguage{polish}ş\selectlanguage{english}e \selectlanguage{polish}Ş\selectlanguage{english}ababl\selectlanguage{polish}ı \selectlanguage{ngerman}Çetin, MD

Sancaktepe \selectlanguage{polish}Ş\selectlanguage{english}ehit Prof. Dr. \selectlanguage{polish}İ\selectlanguage{english}lhan Varank Research and Education Hospital
, Department of Infection Disease , \selectlanguage{polish}İ\selectlanguage{english}stanbul, Turkey

\textbf{ABSTRACT}

\textbf{Purpose}

To investigate the relationship between laboratory blood parameters and
ocular findings in hospitalized moderate or severe COVID-19 patients.

\textbf{Methods}

Ophthalmologic examination of 215 patients who were hospitalized with
the diagnosis of COVID-19 was performed in their beds and their ocular
findings were noted. Blood parameters were compared in patients with and
without conjunctivitis like symptoms.

\textbf{Results}

Conjunctivitis like inflammatory findings were detected in 15 (7.44\%)
of 215 moderate or severe COVID-19 patients. There was no difference
between the patients with and without ocular findings in terms of
laboratory findings such as WBCs, neutrophil counts, lymphocyte counts,
NLR, LDH, procalcitonin, D-dimer, CRP, and ferritin.

\textbf{Conclusion}

There was a significant relationship between COVID-19 and an acute
conjunctival inflammatory response. Blood parameters that determined
progression in patients with COVID-19 were not significant in terms of
ocular findings.

\textbf{Key Words:} COVID-19, conjunctivitis, blood parameters,
laboratory findings, SARS-CoV2

\textbf{What is already known about this topic?}

Inflammatory findings such as conjunctivitis and dry eye in covid-19
patients have been proven by studies. In addition, studies have shown
that crp, procalcitonin, d-dimer and ferritin are associated with poor
prognosis in covid-19 patients. Conflicting results have been reported
in a small number of studies comparing ocular findings and laboratory
findings in covid-19 patients.

\textbf{What does this article add?}

In this study, a conclusion was reached by comparing the laboratory
findings and ocular findings of the patients who were hospitalized and
had severe disease, taking into account the conflicting results
presented in previous studies.

\textbf{INTRODUCTION}

The latest pandemic, which started on December 31st, 2019, when cases of
pneumonia of unknown etiology in Wuhan, Hubei province of China, were
reported to the World Health Organization (WHO), has continued with the
identification of a new coronavirus (2019-nCoV), and this new virus has
spread rapidly and become a global problem. The new virus was named
(SARS-CoV-2) due to its close similarity to severe acute respiratory
syndrome coronavirus (SARS-CoV), and the disease caused by the virus was
named COVID-19. In limited studies for SARS-CoV-2, the average
incubation period has been determined as 5-6 days. Symptoms may occur
within 2-14 days after contact and contamination may begin 1-2 days
earlier. In the clinical presentation of COVID-19, fever, dry cough, and
respiratory distress are considered as major findings (1,2). Although
patients mostly present with an asymptomatic or mild clinical picture,
it may progress to pneumonia or acute respiratory distress syndrome in
patients with additional disease and those aged over 65 years (3)(4).
Infection is transmitted from person to person by inhalation of droplets
or contact with the eyes, nose, and mouth after touching surfaces
contaminated by the virus (5).

Some respiratory system viruses such as adenovirus and H7 influenza
virus can strongly stimulate the immune system in the cornea and
conjunctiva, causing the inflammatory pathway to be activated and to
consequently form conjunctivitis or keratoconjunctivitis (6).

Coronaviruses that can cause conjunctivitis in humans have also been
reported. Human coronavirus NL 63 (HCoV-NL63) was first identified with
bronchiolitis and conjunctivitis in an infant. Then, conjunctivitis was
defined in 17\% of 29 In pediatric patients with HCoV-NL63. No ocular
involvement was reported in Middle East respiratory syndrome-related
coronavirus (MERS-CoV) or SARS-CoV infections (7). However, in animal
studies, ocular infection was observed as a result of direct inoculation
of SARS-COV in the mouth, nose or eye (8)(9)(10). A tear film mostly
covers the eye surface and prevents bacteria and viruses from adhering
to the cornea and conjunctiva with antimicrobial agents and the
immunoglobulins it contains (11).

It has been shown that SARS-CoV-2 infects host cells via
angiotensin-converting enzyme 2 (ACE2) just like SARS-CoV and has
similar receptor binding sites (12). ACE-2 receptor has been detected in
the retina (13), choroid (14) and conjunctival epithelium (15) in the
human eye. In previous studies, findings such as acute follicular
conjunctivitis, conjunctival hyperemia, chemosis, epiphora, and
increased secretion have been described in patients with COVID-19 (16).
As with other viral infections, it is assumed that the ocular symptoms
of COVID-19 are self-limited and can be managed with symptomatic
treatment.

It is known that SARS-COV-2 can be found in tears and adhere to the
ocular surface. Conjunctivitis in patients with COVID-19 has been
reported at different rates in various studies. It is not clear whether
it causes different findings or subclinical conditions on the ocular
surface.

The aim of this study was to evaluate the frequency of ocular
involvement in hospitalized patients with COVID-19 and to compare the
demographic findings and various blood parameters of patients with and
without ocular findings.

\textbf{MATERIALS AND METHODS}

A total of 215 patients who were diagnosed as having COVID-19 with
clinical findings or with polymerase chain reaction (PCR) test
positivity and who were hospitalized between July 2020 and August 2020
were included in the study. The hospitalized patients were seen
individually in their rooms, and the lower eyelid conjunctiva and ocular
surface were macroscopically examined with penlight by inspection. The
eyes of the patients were examined in terms of conjunctival follicle in
the lower eyelid, congestion on the ocular surface, hyperemia or
chemosis. The patients were questioned as to whether there was burning,
foreign body sensation, itching, epiphora or blurred vision. Patients
with any symptoms were asked when they started, whether their symptoms
increased or not, and whether they had similar symptoms before the
COVID-19 infection. Patients who had previously been diagnosed as having
dry eye or allergic conjunctivitis or had symptoms and signs similar to
dry eye, and patients who used regular eye drops for any reason were
considered negative in terms of ocular findings.

Nasopharyngeal SARS-CoV-2 real-time (RT)-PCR results, lung computed
tomography (CT) imaging findings, lactate dehydrogenase (LDH), white
blood cells (WBC), neutrophil counts, lymphocyte counts,
neutrophil/lymphocyte ratio (NLR), procalcitonin, C-reactive protein
(CRP), and ferritin values were recorded.

Ethics approval was obtained from the Medeniyet University G\selectlanguage{ngerman}öztepe
Training and Research Hospital Ethics Board before the start of the
study. The study followed the tenets of the Declaration of Helsinki.

\textbf{Statistical analysis}

Statistical analysis was performed using the SPSS 16.0 (SPSS Inc.,
Chicago, IL) software. The Shapiro-Wilk test was used to test the
normality of data distribution. The independent sample t-test was used
for data with normal distribution; data shown as mean ± standard
deviation in the table. Numerical data without normal distribution were
analyzed using the Mann-Witney U test and shown as median
(maximum-minimum) values. Categorical data were analyzed using the
Chi-square and Fischer's exact tests and shown as percentage (\%).
Statistical significance was assessed as p-values \textless{}0.05.

\textbf{RESULTS}

Of the 215 patients hospitalized with COVID-19, 113 (53\%) were male
(mean age: 54.27 years) and 102 (47\%) were female (mean age: 58.71
years). One hundred forty-five (67\%) patients were found to be positive
due to nasopharyngeal SARS-CoV-2 RT-PCR tests and they were defined as
laboratory-proven patients. In 176 (82\%) patients, CT findings were
found to be significant for COVID-19.

During the examination, there were 15 patients (7.44\%) who had at least
two findings of conjunctivitis-related findings such as conjunctival
congestion, conjunctival hyperemia, conjunctival follicle, chemosis and
epiphora, who were considered as having conjunctivitis. The ocular
findings during the visit to the patients are given in Table 1.

\textbf{Table 1:} Ocular findigs of Covid-19 patients\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
\textbf{Findings of patients} & \textbf{n= 215}\tabularnewline
\midrule
\endhead
Conjunctival congestion & \% 1,86 n= 4\tabularnewline
Epiphora & \% 4,65 n= 10\tabularnewline
Hyperemia & \% 4,65 n= 10\tabularnewline
Chemosis & \% 2,79 n= 6\tabularnewline
Conjunctival follicle & \% 2,79 n=6\tabularnewline
\bottomrule
\end{longtable}

It was observed that the most common ocular findings in Covid-19
patients were epiphora and hyperemia. Patients with chronic dry eye or
allergic conjunctivitis who had such symptoms before were not included
in the study. When the patients with and without ocular findings were
evaluated in terms of age, sex, CT findings, and nasopharyngeal PCR
positivity, no significant difference was found (Table 2).

\textbf{Table 2:} Comparison of demographic and clinical features and
laboratory findings of patients with COVID-19 with and without ocular
findings\selectlanguage{english}
\begin{longtable}[]{@{}llll@{}}
\toprule
& \textbf{Patients with ocular findings (n=16)} & \textbf{Patients
without ocular findings (n=199)} & \textbf{P-value}\tabularnewline
\midrule
\endhead
\textbf{Age} & 51.87\selectlanguage{ngerman}±16.05 & 56.76\selectlanguage{ngerman}±14.84 & 0.212\tabularnewline
\textbf{Male sex n (\%)} & 8 (50) & 105 (52.8) & 0.831\tabularnewline
\textbf{PCR positivity n (\%)} & 12 (75) & 133 (66.8) &
0.502\tabularnewline
\textbf{Presence of CT findings} & 11 (68.8) & 165 (82.9) &
0.157\tabularnewline
\textbf{WBC} & 5680 (3700-8150) & 6100 (4540-7680) &
0.643\tabularnewline
\textbf{Neutrophil} & 4020 (2245-6345) & 3650 (2680-5170) &
0.835\tabularnewline
\textbf{Lymphocyte} & 1470 (1018-1938) & 1440 (1070-1960) &
0.962\tabularnewline
\textbf{NLR} & 2.27 (1.47-4.89) & 2.56 (1.63-3.88) &
0.877\tabularnewline
\textbf{LDH} & 216.50 (190.50-267.0) & 233 (196.0-272.0) &
0.573\tabularnewline
\textbf{Procalcitonin} & \textless{}0.05 (\textless{}0.05-0.55) &
\textless{}0.05 (\textless{}0.05-0.08) & 0.379\tabularnewline
\textbf{D-Dimer} & 0.64 (0.49-1.34) & 0.66 (0.37-1.12) &
0.624\tabularnewline
\textbf{CRP} & 2.85 (0.54-9.36) & 2.90 (0.80-7.0) & 0.853\tabularnewline
\textbf{Ferritin} & 242.96 (54.78-363.0) & 221.29 (98.43-374.59) &
0.622\tabularnewline
\bottomrule
\end{longtable}

WBC: White blood cell, NLR: Neutrophil/lymphocyte ratio, LDH: Lactate
dehydrogenase, CRP: C-reactive Protein

In addition, there was no difference between the patients with and
without ocular findings in terms of laboratory findings such as WBCs,
neutrophil counts, lymphocyte counts, NLR, LDH, procalcitonin, D-dimer,
CRP, and ferritin (Table 1).

\textbf{DISCUSSION}

There is suspicion and some evidence that SARS-COV2 invades ocular
surfaces. Possible mechanisms such as direct conjunctival contact of
infected droplets, hematogenous infection of the lacrimal gland or viral
migration from the upper respiratory system have been described for the
SARS-COV-2 virus to infect the ophthalmic surface (17). The incidence of
conjunctivitis in patients with COVID-19 has been reported as 0.8 and
4.76 percent (18)(19)(20).

In the study conducted by Ping Wu et al., the ocular symptoms of 38
patients who were clinically diagnosed as having COVID-19 and treated as
inpatients were questioned, and RT-PCR was performed by taking
nasopharyngeal and conjunctival samples. Although SARS-CoV-2 was
detected in nasopharyngeal samples in 28 (73.7\%) patients, it was shown
in conjunctival samples in only 2 (5.2\%) patients. However, in 12 of 38
patients (31.6\%), symptoms related to conjunctivitis such as
conjunctival hyperemia, chemosis, and epiphora were observed. Ocular
symptoms were mostly observed in patients with severe pneumonia and the
middle stage of the disease (16).

In an epidemiologic study conducted in China on 534 patients who were
SARS-CoV-2--positive, 25 (4.68\%) patients had conjunctival congestion,
and dry eye (112, 20.97\%), blurred vision (68, 12.73\%), and foreign
body sensation (63, 11.80\%) were reported as the most common symptoms
associated with COVID-19 (21). In another epidemiologic study conducted
in a total of 30 hospitals in China, conjunctivitis was found in 9
(0.8\%) of 1099 patients who had a positive SARS-CoV-2 test and were
hospitalized (22).

In a study from Wuhan, China, conducted by Deng et al., SARS-CoV-2 was
detected using RT-PCR in nasopharyngeal samples in 90 (76\%) of 114
patients followed up in hospital due to COVID-19 pneumonia, and the
virus was not detected in any of the conjunctival samples. In addition,
none of the 114 patients had ocular symptoms such as red eyes or pain
(23). In another study, five patients with COVID-19 presenting only with
symptoms and signs of conjunctivitis were described (24).

In our study, there were 15 (7.44\%) patients showing conjunctival
inflammatory response who had foreign body sensation, epiphora, and
conjunctival congestion symptoms, which were not present prior to the
COVID-19 infection. Although more comprehensive studies are needed, our
study seems to be compatible with the existing literature. The rate of
conjunctivitis or conjunctival inflammatory response has been shown in a
wide spectrum in these studies. These spectra were explained by the fact
that no biomicroscopy examination was performed on patients in any
studies in the literature, and even that the data in most studies were
based on patients' subjective symptoms obtained through teleconferences.
During our study, the fact that the patients were seen by an
ophthalmologist in person and evaluated with a penlight, although a
biomicroscopic examination was not performed, was a positive situation
for the safety of our data.

In a meta-analysis evaluating laboratory findings, 5350 patients from 25
studies were included and high levels of CRP, procalcitonin, D-dimer,
and ferritin were associated with poor outcomes (25). In another study,
it was shown that patients with COVID-19 with ocular symptoms had higher
WNC counts, neutrophil counts, and CRP, LDH, and procalcitonin values
compared with patients without ocular symptoms (16). In another study,
no significant difference was found between patients with and without
SARS-CoV 2 virus isolated from the conjunctiva in terms of laboratory
findings (26). In our study, when the laboratory data of 234 patients
were compared, no significant difference was found between patients with
and without ocular symptoms. Our patients had moderate or severe
symptoms and were hospitalized patients. Patients with very severe
disease in the intensive care unit (ICU) or asymptomatic patients
followed up at home were excluded from the study. As far as we know, no
other comprehensive studies have investigated the relationship between
conjunctivitis and laboratory data in patients with COVID-19.

It was suggested that the ocular surface might be an entry point for
SARS-CoV-2, and ocular involvement was less common thanks to the
antiviral defense system in the conjunctiva and cornea, as well as
lactoferrin and secretory immunoglobulin (Ig)-A (27).

Viruses trigger the immune system, leading to an increase in
immunoglobulin, chemokine and antibody production, and cause tissue
damage, apoptosis, and inflammation (28).

Ocular findings associated with COVID-19 may be due to viral effects or
to dry eye that develops in these patients. There may be several reasons
why dry eye occurs in these patients. The first is the prolongation of
the time of watching screens following restrictions of social activities
in patients. Another reason is that with the use of a mask, the airflow
from the mask to the ocular surface evaporates the tears earlier.
Indeed, there are some viruses associated with dry eye disease (29).
Considering the presence of viruses associated with dry eye disease, it
can be thought that the SARS-CoV-2 virus will affect the conjunctival
goblet cells or the lacrimal gland through blood, disrupting the tear
structure and playing a role in the development of dry eye or
conjunctival inflammatory response.

Our study had some limitations. The sample size was relatively small,
patients with severe clinical findings in the ICU were not included, and
SARS-CoV-2 RT-PCR examinations were not performed on conjunctival
samples.

As a result, there was a significant relationship between COVID-19 and
an acute conjunctival inflammatory response. Blood parameters that
determined progression in patients with COVID-19 were not significant in
terms of ocular findings.

Declarations of interest: none

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