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a r c h s o c e s p o f t a l m o l .

2 0 2 2;9 7(2):63–69

ARCHIVOS DE LA SOCIEDAD
ESPAÑOLA DE OFTALMOLOGÍA

www.elsevier.es/oftalmologia

Original article

COVID-19 pandemic: Impact on the rate of viral


conjunctivitis夽

Y. Conde Bachiller, B. Puente Gete, L. Gil Ibáñez, G. Esquivel Benito, M. Asencio Duran ∗ ,
J.V. Dabad Moreno
Servicio de Oftalmología, Hospital Universitario La Paz, Instituto de Investigación Sanitaria del Hospital la Paz (IDIPAZ), Madrid, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Objective: The COVID-19 pandemic led Spain to order a state of alert with the cessation of
Received 6 February 2021 non-essential activities on 14 March 2020, and to implement public health interventions
Accepted 17 March 2021 (such as home confinement) and other health recommendations to prevent the spread of
Available online 31 January 2022 the SARS-CoV-2 virus (hand washing and the obligation to wear face-masks). These factors
could have influenced the rate of viral conjunctivitis.
Keywords: Method: In this retrospective, noninterventional, descriptive study, the incidence of viral
Viral conjunctivitis conjunctivitis in an emergency department of a national hospital is compared over two
Adenoviral conjunctivitis distinct time periods: pre-COVID (13 March-30 September 2019, one year before the start of
Respiratory infection the pandemic) and COVID (13 March-30 September 2020).
Pandemic Results: In the first period there were 436 cases of conjunctivitis, of which 168 (38.5%) were
COVID-19 confirmed cases of viral conjunctivitis 168 (38.5%), while in the second period there were
121 recorded cases, of which the most frequent were allergic and traumatic (23 cases; 19%
each group), bacterial (15 cases; 12.3%) and viral (15 cases; 12.3%). The diagnosis of viral
conjunctivitis is the one that suffered the most significant relative reduction (48.5%), while
other types of conjunctivitis hardly changed their relative frequency between these two
periods of time.
Conclusions: Viral conjunctivitis is the most frequent infectious disease of the eye and has
a transmission rate similar to that of coronavirus, so the measures implemented could
positively affect its incidence.
© 2021 Sociedad Española de Oftalmologı́a. Published by Elsevier España, S.L.U. All rights
reserved.


Please cite this article as: Conde Bachiller Y, Puente Gete B, Gil Ibáñez L, Esquivel Benito G, Asencio Duran M, Dabad Moreno JV.
Pandemia COVID-19: impacto sobre la tasa de conjuntivitis virales. Arch Soc Esp Oftalmol. 2022;97:63–69.

Corresponding author.
E-mail address: masedur@hotmail.com (M. Asencio Duran).
2173-5794/© 2021 Sociedad Española de Oftalmologı́a. Published by Elsevier España, S.L.U. All rights reserved.
64 a r c h s o c e s p o f t a l m o l . 2 0 2 2;9 7(2):63–69

Pandemia COVID-19: impacto sobre la tasa de conjuntivitis virales

r e s u m e n

Palabras clave: Objetivo: La pandemia COVID-19 condujo a España al decreto de estado de alarma con cese de
Conjuntivitis viral actividades no esenciales el 14 de marzo de 2020 y a intervenciones de salud pública, como
Conjuntivitis adenovírica el confinamiento domiciliario y otras recomendaciones sanitarias para evitar la propagación
Infección respiratoria del virus SARS-CoV-2: la higiene de manos y la obligatoriedad de portar mascarillas. Estos
Pandemia factores podrían haber influido en la tasa de conjuntivitis virales.
COVID-19 Método: En este estudio descriptivo retrospectivo no intervencionista se compara la inci-
dencia de conjuntivitis virales en un servicio de urgencias de un hospital nacional sobre
dos periodos de tiempo: pre-COVID (13 de marzo a 30 de septiembre de 2019, un año antes
del inicio de la pandemia) y COVID (13 de marzo a 30 de septiembre de 2020).
Resultados: En el primer periodo hubo 436 conjuntivitis, de las cuales 168 (38,5%) fueron
casos confirmados de conjuntivitis viral 168 (38,5%), mientras que en el segundo periodo
hubo 121 registros, de los cuales los más frecuentes fueron las conjuntivitis alérgicas y
las traumáticas, con 23 casos (19% cada grupo); las conjuntivitis bacterianas, con 15 casos
(12,3%), y las conjuntivitis virales, con 15 casos (12,3%). El diagnóstico de conjuntivitis viral
es el que experimenta una reducción relativa más importante (48,5%), mientras que otros
tipos de conjuntivitis apenas cambian su frecuencia relativa entre estos dos periodos de
tiempo.
Conclusiones: La conjuntivitis viral, como patología infecciosa más frecuente del ojo, tiene
una transmisión similar a la del coronavirus, por lo que las medidas implantadas podrían
afectar positivamente a su incidencia.
© 2021 Sociedad Española de Oftalmologı́a. Publicado por Elsevier España, S.L.U. Todos
los derechos reservados.

bronchiolitis, common cold or seasonal flu processes during


Introduction the epidemic has been published4,5 . In addition, the decrease
in the incidence of conjunctivitis associated to these processes
In late December 2019, patients with viral pneumonia
or standalone has been observed, albeit empirically.
due to an unidentified microbial agent were reported in
At ocular level, one of the most frequent infections is
Wuhan, Hubei Province, Central China. This disease outbreak,
viral conjunctivitis (1% of all primary care visits and emer-
called COVID-19, increased substantially and was declared a
gencies). Viral conjunctivitis is the most frequent cause of
pandemic by the WHO on March 11, 20201 . The causal microor-
conjunctivitis, representing up to 80% of all cases. Most are
ganism is a type 2 coronavirus, a positive single-stranded RNA
caused by adenoviruses (especially subtypes 7, 11 and 18),
virus that originates the severe acute respiratory syndrome,
and produce two of the clinical entities commonly associated
SARS-CoV-2. Transmission pathways between humans is sim-
to viral conjunctivitis: pharyngoconjunctivitis and epidemic
ilar to that of other coronaviruses, through infected people’s
keratoconjunctivitis6. Viral conjunctivitis can appear as an
secretions; mainly respiratory droplets, hands or fomites con-
isolated disease or associated with systemic viral infections,
taminated with secretions, followed by contact to the mouth,
such as upper respiratory tract infections (URTIs) and measles.
nose or eyes’ mucous membrane2 .
Most infections are caused indirectly after respiratory inhala-
After its arrival in Spain (estimated date, February 14, 2020),
tion, while the conjunctiva rarely serves as a virus entry
there was a significant COVID-19 progression that led to pub-
point for the guest7 , and in these cases local infection can
lic health interventions. The state of emergency and closure
be initiated through direct inoculation after ophthalmolog-
of schools and non-essential activities was decreed on March
ical procedures (tonometry and other ocular explorations),
14, 2020 confining the population in their homes3 . No previous
by contact with secretions of an infected patient, or in cer-
public health intervention can compare to the magnitude of
tain locations with higher viral concentration (for example,
restriction established by this epidemic. Compulsory outdoors
swimming pools)8 . After an incubation period of 5–15 days,
mask mandates and other recommendations such as social
the patient exhibits red eyes, itching, burning, a foreign body
distancing and maintaining hand hygiene, washing them with
sensation and often secretion and ocular discomfort that per-
water and soap or hydroalcoholic gel, were implemented.
sist from 5 to 15 days7 . Under slit lamp exploration, most
Reports show that this unusual situation in Spain could be
patients have unilateral or bilateral acute follicular conjunc-
associated with a strong decrease in both pediatric and adult
tivitis, and unilateral cases frequently become bilateral a few
infectious diseases, which are usually spread in social gather-
days later. Preauricular lymphadenopathy might be present,
ings through respiratory and contact pathways. In this sense, a
and a history of URTIs is common. The symptomatic picture
decrease in both incidence and prevalence of diseases such as
is usually acute and self-limiting, although very contagious.
a r c h s o c e s p o f t a l m o l . 2 0 2 2;9 7(2):63–69 65

Treatment is merely a support and aimed at improving patient epidemiological survey, regional lymph nodes exploration by
discomfort6 . The most important element is infection spread palpation and slit lamp ocular exploration of both eyes with
prevention. To achieve this, doctors should wear gloves while anesthetic eye drops and fluorescein instillation performed by
examining infected patients and practice frequent and care- the emergency ophthalmologist.
ful hand wash. Any equipment and instruments used during
exploration must be cleaned with disinfectant solutions such
as 10% sodium hypochlorite, hydrogen peroxide or alcohols Results
such as 70% isopropyl alcohol9 . Furthermore, patients and
their families have to be instructed to act with caution at The first analysis was carried out with the 436 before COVID
home, washing their hands often and keeping the patient’s period records and the 121 COVID period records.
towels and bed sheets separated from the rest. Children must Out of the 436 before COVID period conjunctivitis records,
be kept out of schools from 5 to 7 days since the onset of 168 (38.5%) remained as confirmed cases of viral conjunctivi-
symptoms. tis, the second most frequent type being allergic with 64 cases
In this work, the hypothesis of possible reduction of viral (14.5%), bacterial with 25 cases ( 5.7%), irritant with 23 cases
conjunctivitis cases in the national emergency system during (5.25%), traumatic with 20 cases (4.6%), inflammatory with 11
the COVID-19 pandemic is considered, and attempts to relate cases (2.5%), herpetic with 10 cases (2, 3%) and phlyctenular
this fact to the use of the hygienic-social measures mandated with 2 cases (0.5%); the rest were diagnostic errors (subcon-
during the pandemic. junctival bleeding, uveitis, keratitis, etc.) (Table 2).
In the 121 COVID period conjunctivitis records, the most
frequent types were allergic and traumatic with 23 cases in
Methods each group (19%), viral and bacterial with 15 cases (12.3%
each), irritant with 12 cases (9.9%), herpetic with 10 cases
A retrospective, non-interventional descriptive study that (8.3%), inflammatory with 7 cases (5.8%) and phlyctenular with
compares the incidence of viral conjunctivitis in an emergency 2 cases (1.65%); the rest were diagnostic errors. It should be
room service admission from a third-level Spanish hospital noted that out of the 121 cases of conjunctivitis, 4 of them
over two different periods of time: before COVID (March 13 to were confirmed cases of COVID-19, but only one of them man-
September 30, 2019, a year before the pandemic) and COVID ifested acute follicular conjunctivitis; the remaining 3 cases
(March 13 to September 30, 2020) is presented. A search on did not manifest follicles and could not be confirmed viral
the hospital Electronic Clinical History Application (Hcis, DXC- conjunctivitis (Table 2).
HCIS® ) within the emergency listings from both adults and If the worldwide emergency activity of the year 2020 com-
children, including diagnoses (ICD-10)10 generally used in clin- pared to 2019 is estimated based on these data, the number
ical trials to describe this pathology (Table 1) by the emergency of ophthalmology emergency consultations suffered a drop
ophthalmologist, in both written and coded diagnostic boxes from 2019 to 2020 of 72.24%, which affected all diagnoses,
was performed. i.e., the number of patients with a viral, allergic, etc. con-
As a result, two spreadsheets were obtained (Microsoft junctivitis diagnosis, was theoretically decreased by 72.24%
Office Excel® 2007), one corresponding to the 13/03-30/09/2019 due to home confinement and other pandemic-related effects.
period and another corresponding to the 13/03-30/09/2020 However, viral conjunctivitis diagnosis is the type that experi-
period, generated by the program and called Excel diagnóstico ences the greatest drop in absolute numbers of all possible
2019 and Excel diagnóstico 2020, that contained the clinical his- conjunctivitis diagnoses during the analyzed COVID period
tory number, patient name, date of birth, age, emergency room (153 less cases than the previous year), the second diagno-
admission date and diagnosis. sis in numerical decrease being allergic conjunctivitis (41 less
To avoid the loss of cases without ICD-10 diagnosis by this cases in 2020 compared to 2019). If this absolute numer-
system, a decision to expand the search within these emer- ical value is relativized in relation to the global decrease
gency listings also selecting reason for consultation was made in ophthalmological visits in emergency care numbers (315
(which is found in 100% of patients, since it is mandatory less patients attended in 2020 compared to 2019) the diag-
data for Manchester staging and subsequent filtering for the nosis with the most important percentage drop remains
emergency specialist). As reasons for consultation, the most viral conjunctivitis, with 48.5% less emergency consulta-
frequently used by the triaging emergency staff were cho- tions. In second place, other diagnostic errors cataloged as
sen: red eye, ocular secretion, rheum, conjunctivitis, ocular conjunctivitis in a first screen is observed, with 31.4% less
infection and ocular swelling. Two other new Excel® sheets prevalence, and in third place allergic conjunctivitis, with a
generated by the program were obtained, called Excel motivo de 13% less.
consulta 2019 and Excel motivo de consulta 2020 that contained To avoid the influence of diagnostic errors mistaken with
the same basic data. The two spreadsheets of each year were conjunctivitis (which constitute up to 25.9% of Excel fusión
merged in a third Excel sheet called Excel fusión (one for 2019 2019 and 11.5% of Excel fusión 2020), a second screen of the
and another for 2020). A total of 436 conjunctivitis records were spreadsheets was performed, so that in all cases obtained by
obtained for the 2019 analyzed period (before COVID) and 121 searching reason for consultation, the final diagnoses given
records for the 2020 analyzed period (COVID). to the patient by the ophthalmologist were all confirmed one
In this study, no samples of conjunctival exudate or by one (which was written in the free text space of the emer-
serology were collected for the determination of causal micro- gency discharge report in the clinical history itself but it did not
biological diagnosis. Diagnosis was based on anamnesis, the appear in the written diagnostic boxes as a coded diagnosis),
66 a r c h s o c e s p o f t a l m o l . 2 0 2 2;9 7(2):63–69

Table 1 – Most used diagnoses in the study to describe acute viral conjunctivitis according to the International Catalog of
Diseases Version 10 (ICD-10)10 .
Diagnosis at discharge Reason for consultation

Code (ICD-10)

H10.01 Acute follicular conjunctivitis Red eye


H10.22 Pseudomembranous conjunctivitis Eye discharge
H10.3 Acute non-specified conjunctivitis Rheum
H11.43 Conjunctival hyperemia Conjunctivitis
H16.2 Keratoconjunctivitis Ocular infection
B30 Viral conjunctivitis Ocular swelling
B30.0 Adenovirus Keratoconjunctivitis
Epidemic keratoconjunctivitis
B30.1 Conjunctivits by adenovirus
Adenovirus acute follicular conjunctivitis
B30.2 Viral pharyngoconjunctivitis
B30.3 Acute epidemic hemorrhagic conjunctivitis (enterovirus)
Enterovirus conjunctivitis
Coxsackie virus conjunctivitis
Hemorrhagic (acute) (epidemic) conjunctivitis
B30.8 Other viral conjunctivitis
Newcastle virus conjunctivitis
B30.9 Viral conjunctivitis, unspecified

Table 2 – Most frequently diagnosed conjunctivitis in emergencies (prior to ICD-10 coding) in the period before COVID
(March 13 to September 30, 2019) and during COVID (March 13, 2020 to September 30, 2020).
Emergency diagnosis Before COVID COVID % of change from before Absolute change % relative change
COVID to COVID (regarding in patient (absolute
total number of patients in numbers change/total
the period) absolute change)

Viral conjunctivitis 168 (38.5%) 15 (12.3%) –26.2 –153 –48.5


Allergic 64 (14.5%) 23 (19%) +4.5 –41 –13
conjunctivitis
Bacterial 25 (5.7%) 15 (12.4%) +6.7 –10 –3.2
conjunctivitis
Irritant 23 (5.25%) 12 (9.9%) +4.65 –11 –3.4
conjunctivitis
Traumatic 20 (4.6%) 23 (19%) +14.4 +3 +0.9
conjunctivitis
Inflammatory 11 (2.5%) 7 (5.6%) +3.1 –4 –1.2
conjunctivitis
Herpetic 10 (2.3%) 10 (8.3%) +6.0 0 0
conjunctivitis
Phlyctenular 2 (0.5%) 2 (1.65%) +1.15 0 0
conjunctivitis
Other diagnosesa 113 (25.9%) 14 (11.5%) –14.4 –99 –31.4
TOTAL 436 121 –72.24% –315 –100%

a
Diagnostic errors mistakenly cataloged as conjunctivitis in a first screening; including hyposfagma, uveitis, keratitis, stye, pterygion. etc.).

and if they did not correspond to any of those selected from to the data collection closure date on 09/30/2020, 15 diagnoses
the ICD-10 code, were deleted. After also eliminating duplicate compatible with ICD-10 standards for viral conjunctivitis,
patients, files that had basic information missing or incongru- without no cases registered during the months of March or
ous diagnoses, a total of 168 viral conjunctivitis patient records September 2020, and with a maximum number of patients
were obtained for the period 13/03-30/09/19 (Excel fusión 2019 per month in the months of May and June (the distribution of
final, before COVID period) and a total of 15 viral conjunctivi- diagnosed viral conjunctivitis cases per month in each period
tis patient records the period 13/03-30/09/20 (Excel fusión 2020 is shown in Figs. 1 and 2). This contrasts significantly with the
final, COVID period) These two new spreadsheets only include number of diagnosed and collected cases in the same time
diagnoses compatible with ICD-10 for viral conjunctivitis diag- frame from the previous year (13/03-30/09/2019), in which the
nosis (Table 1). The patient distribution by diagnosis is shown average number of patients diagnosed with viral conjunctivitis
in Table 3. was 26.5 patients (not taking the month of March into account,
This second analysis shows that during the 6-month period since it is not a complete month and therefore the average
between 13/03/2020 (COVID-19 pandemic became official) up cannot be performed).
a r c h s o c e s p o f t a l m o l . 2 0 2 2;9 7(2):63–69 67

reduced by at least half, and cultural, artistic, sports and simi-


Table 3 – Number of final patients attributed to each
ICD-10 diagnosis for viral conjunctivitis in each time lar activities were suspended. All of this, added to the “fear” of
period analyzed: period before COVID (March 13 to contracting the COVID-19 disease, limited patients visits to the
September 30, 2019) and COVID period (March 13, 2020 emergency services of health centers and hospitals through-
to 30 September, 2020), after clearing the initially out Spain. This explains the decrease of patients treated in
obtained spreadsheets. emergencies in all medical specialties, including ophthalmol-
Diagnoses ICD-10 Before COVID COVID ogy. Although the data is estimated, in an ophthalmological
center similar to that of our study, patient care in the emer-
Acute follicular conjunctivitis 99 0
Pseudomembranous conjunctivitis 15 7 gency room decreased more than 70% in 2020 compared to
Acute non-specified conjunctivitis 6 3 2019.
Conjunctival hyperemia 2 0 Out of all ophthalmological pathologies, this work ana-
Keratoconjuntivitis 1 0 lyzed one of the most frequent reasons for consultation,
Viral conjunctivitis 23 1 conjunctivitis7 , and viral conjunctivitis in particular, which
Adenovirus keratoconjunctivitis 0
at the time of year analyzed (March to September) are the
Epidemic keratoconjunctivitis 2 0
most common, since its frequency is higher in spring and
Adenovirus conjunctivitis 2 0
Adenovirus acute follicular conjunctivitis 6 0 summer6 . The viruses that cause this pathology most fre-
Viral pharyngoconjunctivitis 1 0 quently, adenoviruses, share transmission mechanisms and
Acute epidemic hemorrhagic 0 0 even clinical signs very similar to those of coronavirus11 , and
conjunctivitis (enterovirus) therefore it can be assumed that measures applied to con-
Enterovirus conjunctivitis 0 0 tain the spread during the COVID-1912,13 pandemic and the
Coxsackie virus conjunctivitis 0 0
preventing recommendations from various medical organiza-
Conjunctivitis (acute) (epidemic) 1 0
hemorrhagic
tions and ophthalmological societies14–18 have also an effect in
Other viral conjunctivitis 2 0 decreasing viral conjunctivitis propagation. Despite the obvi-
Newcastle virus conjunctivitis ous case decrease due to the emergency state and home
Viral conjunctivitis, unspecified 8 4 confinement, after performing a careful data analysis it can
TOTAL 168 15 be concluded that from all the types of conjunctivitis admitted
in emergency care, viral conjunctivitis experienced the biggest
decrease. According to the relative percentage of change anal-
The only case of viral conjunctivitis that complied with
ysis (absolute change or difference in total number of patients
ICD-10 diagnostic criteria and microbiologically confirmed as
diagnosed with conjunctivitis of a given type, for example
positive for SARS-CoV-2 was a pseudomembranous unilat-
viral, in the period of 2020 relative to the period of 2019 and
eral conjunctivitis that presented follicles in ophthalmological
divided by the absolute change total or difference in number
exploration, diagnosed in May 2020.
of all conjunctivitis diagnoses in the period of 2020 compared
to 2019), viral conjunctivitis decreases by 48.5% in 2020 in con-
Discussion trast to 2019, far from the second type, allergic conjunctivitis,
that only decreased 13%. In absolute values, the number of
During the COVID-19 pandemic in Spain and mainly moti- patients attended with a final viral conjunctivitis diagnosis
vated by the state of emergency declaration, a restriction was reduced by 91% (only 15 cases in 2020 compared to 168 in
on personal and collective circulation was enforced in the 2019), while the number of patients with allergic conjunctivi-
population, limited to carrying out exclusively first necessity tis remains 64% of cases (23 cases in 2020 compared to 64 in
activities, such as attending health centers or assisting vul- 2019). Other conjunctivitis diagnoses do not present as much
nerable people. Transportation, both public and private, was variation between these two time intervals.

Fig. 1 – Number of patients that attended the emergency room diagnosed with “viral conjunctivitis” during the first 6
months of COVID-19 pandemic (March 13, 2010 to September 30, 2020).
68 a r c h s o c e s p o f t a l m o l . 2 0 2 2;9 7(2):63–69

Fig. 2 – Number of patients that attended the emergency room diagnosed with “viral conjunctivitis” during the 6
overlapping months in the COVID-19 pandemic period, but analyzed from 2019.

The reasons that could explain this marked decrease in


viral conjunctivitis compared to other types of conjunctivitis
Funding
may be in the hygiene measures implemented as a result of
the pandemic, which have affected the transmission pathway This work has not received funding from public or private
of SARS-CoV-2 and other respiratory viruses (like the aden- institutions.
ovirus that causes most viral conjunctivitis). Among these
measures, use of facial masks, washing hands, ventilation Conflict of interest
of spaces with high concentration of people and surface
disinfection with diluted bleach, chlorine or alcohol deriva- No conflicts of interests have been declared by the authors.
tives at 70% (which have also shown to be effective against
adenoviruses19,20 ). references
This study would be the first to demonstrate the benefits
of the hygienic-social measures implemented during the pan-
demic for the prevention of community propagation of viral
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