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\begin{document}

\title{Retinal hemorrhage of late post COVID-19 and post vaccine related
pathogenic mechanisms: A new challenge for ophthalmologist in COVID era}



\author[1]{Mohammad Ashraful Amin}%
\author[2]{Sabrina Nahin}%
\author[3]{Taslima Ahmed Dola}%
\author[1]{Sadia Afrin}%
\author[1]{Mohammad Delwer Hossain Hawlader}%
\affil[1]{North South University}%
\affil[2]{Green Life Medical College and Hospital}%
\affil[3]{East West Medical College and Hospital}%


\vspace{-1em}



  
  \date{June 10, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
COVID-19 infection results in extensive organ dysfunction. Thrombotic
problems linked to COVID--19 disease is common and can affect the
retina. We will report a case of retina hemorrhage with possibility of
linkage between COVID-19 infection or immunization to determine whether
these abnormalities are causal or coincidental.%
\end{abstract}%



\sloppy


\textbf{Introduction:}

COVID-19 is a highly contagious that spreads from person to person
primarily by affected person's respiratory droplets and contamination
objects or bodily limbs via the nostrils, mouth, and ocular route (1,
2). COVID-19 may affects multiple organ system (cardiovascular diseases,
respiratory failure, renal failure, liver damage, ocular adverse effect)
but it is difficult to monitor all the system (3). The nasolacrimal
system allows pulmonary virus spreads through the eye. As a result,
virus-infected nanoparticles interacted with the ocular surface and can
then infiltrate the lung tissue through the nasolacrimal channel. The
angiotensin converting enzyme 2 (ACE2) binding site is present in the
retina as a facilitator for virus entry into human host which may leads
to retinal involvement by SARS-CoV-2 (4-6). Conjunctivitis, conjunctival
erythema, chemosis, epiphora, cotton wool spots (CWS), and
microhemorrhages have been confirmed on fundus assessment.
Hyperreflective abnormalities at the point of the ganglion cell and
internal plexiform layer at the papillomacular region can be detected
through spectral-domain optical coherence tomography (SD-OCT)(7, 8). In
Germany, SARS-CoV-2 virus RNA was found in the retinas where three of
the 14 number COVID-19 patients who died (4) and another study conducted
in Italy found additional papillary focal retinal hemorrhage in the
post-COVID-19 group(9). Severe capillary lesions such as cotton wool
spots, retinal hemorrhages, sectoral retinal infarction have
subsequently been reported in admitted, severe COVID-19 patients which
suggests a new SARS-CoV-2 association (10). The generation of cytokines,
which are responsible for the activation of a procoagulant prothrombotic
response, is causing concern about these retinal microvascular
observations, which could be a symptom of COVID-19's intravascular
coagulopathies and endothelial damage (11). As COVID-19 vaccinations
become more common, the might be a increases concern of ophthalmic
consequence due to vaccination (12), however a microvascular anomaly in
the deep capillary plexus of the retina is suspected, the pathogenesis
is unexplained (13, 14). In one case series, eye adverse events take
place immediately after getting an inactivated COVID-19 vaccination were
observed (12) and according to an interim analysis of four randomized
controlled studies based on vaccine safety data, ocular consequences are
uncommon with Live-virus vaccinations (AstraZeneca vaccine) (15, 16). In
this report, we present a patient with secondary retinal hemorrhage who
had recovered back from COVID-19 and had also received COVID-19
vaccination.

\textbf{Case Report:}

A male patient aged 41-years felt a mild cough followed by fever and
also anosmia on October 14, 2020. He had previous contact with a
COVID-19 family member with whom he was staying, but no prior history of
traveling outside of the country prior to this occurrence. As his family
history was positive, he went for RT-PCR testing for SARS-CoV-2 and
became positive as COVID-19 on 16th October, 2020 and was in isolation
at home. On the next day, 17\textsuperscript{th} October, he had fever
with dry cough constantly, sore throat followed by fatigue. His
temperature was 104 \selectlanguage{ngerman}°F, blood pressure 130/70\selectlanguage{english} mmHg, pulse rate 98\selectlanguage{english} bpm
(regular) and oxygen saturation on pulse-oximetry was 98-99 \% without
oxygen. Routine blood tests or chest X-ray was not done on that time.
The patient started medications from October 17, 2020 (Table 1). On 22th
October 2020, physical examination indicated normal vital signs.
Throughout this time, he had a mild covid symptom and was
self-medicating at home, with no need for hospitalization. On
10\textsuperscript{th} November 2020, the patient went for COVID-19 test
that was negative and was completely stable without any complication.
After the symptom free from Covid-19, December 2020, he was diagnosed as
systemic hypertensive and started medication (Table 1) as recently six
months diagnosed as hypertension without no other history of any
significant co-morbidities. Later on, he gave his
1\textsuperscript{st}dose of COVID-19 vaccine which was Live-virus
vectored based vaccine (COVISHIELD vaccine-AstraZeneca) on 16 February
2021. He completed his 2\textsuperscript{nd} dose of vaccine on 17 April
2021. From 1\textsuperscript{st} dose of vaccine up to completing date
of 2\textsuperscript{nd} dose of vaccine he had no complication arises.
Although the patient complaints of fatigue that last for 4 months after
acute COVID-19. He had no history of diabetic and no history of
Rheumatoid arthritis or no trauma of history on eye previously. He
noticed 3-4 number floaters in his right eye on June 1, 2021, which
changed or grew dramatically. Other complaints were light flashes, a
curtain moving into and obstructing his vision, and diminished vision in
his right eye and became red in colour on right eye. He had no
complaints of watering of eye, headache, eye ache, eyelid swelling, any
foreign body sensation. He had no other history of any trauma on eye or
previous eye operations. On, 7\textsuperscript{th} June, 2021, he went
to ophthalmologist of the Ispahani Islamia Eye Institute and Hospital,
Dhaka for this complication. Details of eye examination finding are
given in (Table 2) \textbf{.} and fundus of R/E: Total vitreous
hemorrhage shows in figure 1 and other blood investigation (Table 1) was
also done and on same day he had immediately underwent Yag Laser
Hyalodotomy as outdoor base case. He was discharged on same day and
advised with medication (Table 2). On, 19 June, 2021 and 26 June, 2021
two outdoor follow up done with medication (Table 2) as continue
treatment. Then, on July 28, 2021, it appeared to be clearing in some
stages, but it was still a nonrevolving vitreous haemorrhage. Following
that, he was scheduled to undergo Pars plana vitrectomy (PPV) with
endolaser and anti-vascular endothelial growth factor (anti-VEGF)
medications by an ophthalmologist at the Ispahani Islamia Eye Institute
and Hospital in Dhaka. On, 29 July, 2021 he went to india for further
follow-up and visited Sankara Nethralaya eye hospital, Chennai, India
and done Ultrasound biomicroscopy (UBM) on 31 July, 2021 (Figure 2) and
found on the right eye, there was a retinal detachment as well as a
complete posterior vitreous detachment, and the vitreous displayed a
large number of low reflective dot mobile echoes. On, 3rd August 2021,
he again consults with doctor and advise to do OPTOS Retinal Exam and
examination revealed plenty of low reflective dot and clump echos on
right eye (Table 3). He continues his eye drop medication. For further
better management, he planned to go LV Prasad eye institute, Hydarabed
on 11\textsuperscript{th} August 2021. As recommended by an
ophthalmologist, the operation was conducted properly and he was
discharged from the hospital that day in a stable condition with
medicine. Procedure done successfully and discharged from hospital in a
stable condition on same day with medication. On follow-up, 16 August,
2021, eye examination, On right eye examination: eyelids edematous,
conjunctiva chemosis, cornea clear (Table 3). During the whole period
scenario, physician not found any significant cause of this retinal
haemorrhage except may be complication of post COVID or vaccine related
retinal complication. Last follow up in Bangladesh on 6 October 2021,
VAR:6/6 and VAL:6/6.

In summary, this patient was diagnosed COVID-19 on 16 October, 2020
(RT-PCR positive) and nasopharyngeal swab for SARS-CoV-2 was negative on
10\textsuperscript{th} November 2020. The patient took first dose of
COVID-19 vaccine (Live-virus vectored based vaccine, COVISHIELD
vaccine-AstraZeneca) on the 16th February 2021 and
2\textsuperscript{nd}dose on 17th April 2021. Retinal hemorrhage was
seen on 1\textsuperscript{st} June,2021 and underwent Yag Laser
Hyalodotomy and medication in Dhaka on 7 June, 2021.Then he went to
chennai eye hospital, India and go through further investigation. Later
on, again he admitted into the Hydarabed hospital on
12\textsuperscript{th} August 2021 for right sided Pars plana vitrectomy
(PPV) and later was discharged on same day. His blood pressure and
random blood sugar levels were both normal at the time of ocular
manifestation. During follow-upon in Bangladesh on 6 October 2021,
visual acuity 6/6. indicating that his eye clinical condition had
improved There was no further occurrence of hemorrhage after this
follow-up.

\textbf{Discussion:}

According to our knowledge this might be first cases in Bangladesh
presented with this rare condition of post-COVID-19 retinal hemorrhage.
Though a straightforward clear correlation could not be established
regarding study configuration, as male patient may develop ocular
consequences that may have influenced retinal changes as a result of
post-Covid consequences or 43 days after receiving a Live-virus vectored
based COVID-19 vaccine (AstraZeneca vaccine). Theoretical
pathophysiology of COVID-19 inactivation-related ocular inflammation is
unknown. Respectively molecular mimicry and antigen-specific cellular
and antibody-mediated immune system disorders have been suggested as
possibilities (17-19). The discovery of COVID-19 viral RNA in the retina
is significant. In addition, a new host cell entrance route involving
the receptor CD147 has been identified (20), CD147 is present at
moderate-to-high levels throughout all cell types of the human retina,
particularly in retinal ganglion cells (GCs), in contrast to ACE2 (21).
Furthermore, positive RT-PCR findings have been published in human
retinal biopsies, implying that the viral proteins is invading retinal
nerves specifically (4). Certain coronavirus variants can invade retinal
cells in other vertebrate species both in situ and in retinal cultured
cells (22) and in vivo following viral proteins were injected
intravitreally(23) producing experimental coronavirus
retinopathy(ECOR)(24, 25). Three out of 14, RB samples were positive for
SARS-CoV-2 RdRp-gene, E-gene, and Orf nCoV-gene-specific sequences in
the retina in one research in Germany (4). Most notably, retinal
microangiopathy exhibited as cotton wool patches (diagnostic and
therapeutic sign related with nerve fiber ischaemia) was seen in 6 out
of 27 outpatients evaluated by retinal fundoscopic, B-scan OCT(Optical
Coherence Tomography), and Optical Coherence Tomography Angiography
angiography (OCT-A) at a mean of 43 days following COVID-19 disease
onset in Spain (26). Retinal hemorrhages were identified in 9\% of
COVID-19 victims even during acute phase of infection, cotton wool
patches in 7\%, dilated veins in 28\%, and twisted vessels in 13\% in a
study in Italy (27). With no complaints or indicators of intraocular
inflammation, four patients out of 12 patients showed with mild cotton
wool patches and microhemorrhages across the retinal apartment(7). In
terms of our own experience, we had a similar case of retinal
hemorrhage. There is no intraocular inflammation or discomfort in the
eyes. In COVID-19 individuals, there are at minimum two basic ways that
vascular injury can occur: The first is a prothrombotic state, similar
to disseminated intravascular coagulation (DIC)(28) and secondly, due to
spontaneous viral infection of the vascular endothelium and widespread
endothelial dysfunction, a vasculitis-like reaction starts(29). Retinal
hemorrhages that represent the outcomes in retinopathy related to blood
dyscrasias may be a connection with SARSCoV-2 in the perspective of a
coagulopathy evoked by the pathogen in the utter lack of arterial
hypertension, no symbols of diabetic retinopathy, and the total lack of
other cardiovascular risk, as well as the improvement after the COVID-19
regimen, as well as the betterment after the COVID-19 medical therapy.
Retinal hemorrhages (subretinal, subhyaloid, or intraretinal), capillary
tortuosity, and cotton balls patches are all ophthalmic symptoms of
blood dyscrasia. Hype viscosity and prolonged arteriovenous passage time
are assumed to be the reasons(30). Our case was a subhyaloid subtype of
retinal hemorrhage. In, Abu Dhabi(12), Scleritis and episcleritis were
detected in 4 of 9 instances, on average 5 days after the first dose of
the vaccination. After compiling all of the data from our report and the
other assessment research, we discovered that several clinical findings
are in accordance across all of these patients, such as the nature of
the retinal hemorrhage or abnormalities pertaining to the covid19
complication and vaccination, but our case was unique in that it was
post covid retinal hemorrhage or late COVID-19 vaccine induced retinal
hemorrhage. The baseline retina record from validated COVID-19 patients
who had been immunized for COVID-19 and were later admitted for ocular
treatment of extreme and urgent condition was a major strength of our
study. Patients with subhyaloid hemorrhage were more likely to show with
systemic hypercoagulopathy and cytokine storm during retina evaluation.
There are certain limitations to our research. First, our case only
included young, healthy men, limiting the generalizability of our
findings. Second, complications occur at different/long times and we
don't obtain a definitive answer, whether it's for post COVID-19 or
vaccine-related issues. Third, no supplemental hematological and
biochemical analyses/studies, such as D-dimer and prothrombin time,
bleeding time, clotting time would be suitable to alternative way of
COVID-19 hyper-coagulopathy as a biological process for the retinal
signboards, as well as laboratory levels of serum, such as C reactive
protein, to link the retinal outcomes to correlating systemic
inflammation. Also, while there was no massive distinction between
patients with and without increased blood pressure, it could still be a
significant contributor.

\textbf{Conclusion:}

As COVID-19 becomes more endemic, a dedicated international registry for
tracking unusual ocular consequence following COVID-19 vaccination could
help us better understand the disease. It might be useful to figure out
which people have a high risk of suffering ocular consequence as a
result of post COVID-19 infection or immunization. Our findings point to
a possible retinal haemorrhage with an unusual trajectory, highlighting
the complexities of diagnosing and treating this event with the Covid19
vaccination. As a result of the inflammatory cytokines and
hypercoagulable conditions produced by infection with SARS-CoV-2,
ophthalmologists must be cautious of ocular vascular disorders. As the
investigation for a post covid and COVID-19 vaccine continues, we should
expect higher incidence in the frequency of ophthalmic consequence from
the various possibilities.

\textbf{Funding}

This research did not receive any specific grant from funding agencies
in the public, commercial, or not-for-profit sectors.

\textbf{Declaration of competing interest}

The authors declare that they have no competing financial interests or
personal relationships that could have appeared to influence the work
reported in this paper.

\textbf{Author contributions}

The article's first draft was written by MAA and MDH. MAA, SN, SA and
TAD contributed to the literature review and manuscript preparation. All
authors contributed to the final version by critically reviewing and
editing drafts.

\textbf{Ethical approval}

The article is about a case study. As a result, our Ethics Committee's
consent was not required.

\textbf{Consent}

The patient's written informed consent for publishing of this case
report, as well as images, was acquired.

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\textbf{Table and figure}

\textbf{Table 1. Laboratory parameters of the cases}\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
Investigation & 7\textsuperscript{th} June 2021\tabularnewline
\midrule
\endhead
S. Creatine & 0.91 mg/dl\tabularnewline
S. ALT & 49 U/L\tabularnewline
Lipid Profile &\tabularnewline
S. Cholesterol & 151 mg/dl\tabularnewline
S. Triglyceride & 291 mg/dl\tabularnewline
S.HDL & 27 mg/dl\tabularnewline
Non-HDL Cholesterol & 124 mg/dl\tabularnewline
T.Cholestero-HDL Ratio & 5.59\tabularnewline
ACR &\tabularnewline
Urine Micro-Albumin & 19.10 mg/L\tabularnewline
Urine Creatinine & 4.42 gm/L\tabularnewline
Micro-Albumin Creatinine Ration & 4.32 mg/gm\tabularnewline
Platelet count & 210000 per microliter of blood.\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 2. Medication list}\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
\textbf{Date} & \textbf{Medication received}\tabularnewline
\midrule
\endhead
On, 17\textsuperscript{th} October, 2020 & Paracetamol 500mg 1tab
8hourly, Azithromycin 500mg once at night for 5days, Deflazacort 24mg 12
hourly for 5days and Enoxaparin sodium 60mg once daily 5
days.\tabularnewline
On, 1\textsuperscript{st} December 2020 & losartan potassium 50mg at
night and bisoprolol 2.5mg at morning\tabularnewline
On, 7\textsuperscript{th} June, 2021 & Tranexenic acid 500mg and
Moxifloxacin eye on right 6hourly to continue for 7 days\tabularnewline
19 June, 2021 and 26 June, 2021 two outdoor follow up & Moxifloxacin eye
on right 6 hourly and Nepafenac eye drop on right eye 12hourly eye drop
as continue treatment\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 3. Eye examination}\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
\textbf{Date and institute} & \textbf{Examination
finding}\tabularnewline
\midrule
\endhead
On, 7\textsuperscript{th} June, 2021, Ispahani Islamia Eye Institute and
Hospital, Dhaka & On eye examination finding, VAR (Right visual acuity)-
Counting Fingers (CF) 3 feet without and VAL (Left visual acuity)- 6/9
without, Anterior Segment of Right eye(R/E): Intra ocular pressure
(IOP):14 mm hg and Left eye(L/E): Intra ocular pressure (IOP):11 mm hg
and fundus of R/E: Total vitreous hemorrhage\tabularnewline
On, 3rd August 2021, Sankara Nethralaya eye hospital, Chennai, India. &
Examination revealed attached retina with plenty of low reflective dot
and clump echos and cornea and conjunctiva of both eyes were
normal\tabularnewline
On, 16th August 2021, Sankara Nethralaya eye hospital, Chennai, India. &
Eye examination on right eye, eyelids edematous, conjunctiva chemosis at
6 o clock and 10 o clock, sclera mild congestion, cornea clear, anterior
chamber- deep, iris- normal color and pattern, pupil- dilated and fixed
, post dilated examination, pupil of R/E -7mm, lens clear and L/E- 3mm
un dilated and leans clear, fundus examination R/E -- Media clear, optic
disc size- medium size disc, optic disc -normal, blood vessel- normal,
macula-normal, Cup/Disc ratio-0.3, Fundus- retina ON. During the whole
period scenario, physician not found any significant cause of this
retinal haemorrhage\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Figure 1. Fundoscopy shows retinal haemorrhage}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

\textbf{Figure 2.} Ultrasound biomicroscopy (UBM) which showed retinal
detachment as well as complete posterior vitreous detachment and
vitreous shows multiple number of low reflective dot mobile echoes on
right eye.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure-1/Figure-1}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure-2/Figure-2}

\end{center}
\end{figure}

\selectlanguage{english}
\FloatBarrier
\end{document}

