Ocular Surface Changes Associated With Face Masks in Healthcare Personnel During COVID-19 Pandemic
Ocular Surface Changes Associated With Face Masks in Healthcare Personnel During COVID-19 Pandemic
Ocular Surface Changes Associated With Face Masks in Healthcare Personnel During COVID-19 Pandemic
Article
Ocular Surface Changes Associated with Face Masks in
Healthcare Personnel during COVID-19 Pandemic
Filippo Tatti 1 , Lorenzo Mangoni 1 , Simone Pirodda 1 , Giuseppe Demarinis 1 , Claudio Iovino 1,2 ,
Emanuele Siotto Pintor 1 , Germano Orrù 3 , Luigi Isaia Lecca 4 , Marcello Campagna 4 , Gloria Denotti 5
and Enrico Peiretti 1, *
1 Department of Surgical Sciences, Eye Clinic, University of Cagliari, 09124 Cagliari, Italy
2 Multidisciplinary Department of Medical, Surgical and Dental Sciences, Eye Clinic, University of Campania
Luigi Vanvitelli, 80131 Naples, Italy
3 Molecular Biology Service Lab, Department of Surgical Science, University of Cagliari, 09124 Cagliari, Italy
4 Division of Occupational Medicine, Department of Medical Sciences and Public Health, University of Cagliari,
09042 Monserrato, Italy
5 Department of Surgical Science, Institute of Dentistry, University of Cagliari, 09124 Cagliari, Italy
* Correspondence: [email protected]
Abstract: The aim of this study was to investigate ocular surface changes associated with face mask
(FMs) use of healthcare personnel during the COVID-19 pandemic. We prospectively evaluated
200 eyes of 100 individuals during working hours and 40 eyes of 20 individuals during their rest
days as a control group. Dry eye symptoms were assessed with the Ocular Surface Disease Index
(OSDI) and McMonnies questionnaire. The clinical investigation included the best corrected visual
acuity (BCVA), corneal fluorescein staining (FS), break-up time (BUT), and Schirmer test I before
and after a 7-h work shift with a continuative use of surgical or N95 masks. The control group was
Citation: Tatti, F.; Mangoni, L.;
evaluated similarly twice a day, at 8:00 a.m. and at 3:00 p.m. In the study group, BCVA, FS, BUT,
Pirodda, S.; Demarinis, G.; Iovino, C.;
Siotto Pintor, E.; Orrù, G.; Lecca, L.I.;
and Schirmer test were investigated and there was a significant negative variation at the end of the
Campagna, M.; Denotti, G.; et al. shift. On the contrary, the control group did not show significant variations of any clinical feature.
Ocular Surface Changes Associated Furthermore, no significant changes in clinical parameters were observed during the use of surgical
with Face Masks in Healthcare or N95 masks. In conclusion, FMs continuative use resulted in daily ocular surface modifications
Personnel during COVID-19 specifically in healthcare personnel.
Pandemic. Life 2022, 12, 1491.
https://doi.org/10.3390/ Keywords: COVID-19; face mask; dry eye; mask-associated dry eye
life12101491
mask [15–17] would wrap around the corneal surface, creating conditions that may acceler-
ate corneal tear film evaporation and lead to a new clinical entity called mask-associated
dry eye (MADE) [11,13]. A recent study identified other co-risk factors implicated in
DED pathogenesis in the COVID era including digital devices misuse, unbalanced diet,
insufficient hydration, sleep deprivation, and the psychological repercussions of pandemic
restrictions [5].
Under this light, considering the WHO recommendations on wearing FMs (N95, FFP2,
or FFP3) in healthcare settings [18] and the work shifts of health workers (about 7 h/day in
Italy), these individuals may potentially be at high risk for the occurrence or worsening
of DED. Moreover, even though mask-associated dry eye has already been demonstrated,
information on daily ocular surface modifications still remains unknown. Therefore, the
aim of this study was to investigate FMs-related ocular surface changes in healthcare
personnel, using questionnaires and clinical examinations.
2.2. Questionnaire
All subjects were evaluated for DED at baseline with the Ocular Surface Disease Index
(OSDI) and the McMonnies questionnaire. The OSDI is a 12-item scale created to assess
subjective dry eye symptoms and the effects of the disease on vision-related activities of
daily living within the previous week. The total OSDI score ranges from 0 to 100 points
and positively correlates with DED severity, with a cut-off value of 13 for a diagnosis
of DED [19]. The McMonnies questionnaire is a 12-item instrument for the screening
of dry eye disease. Each question is individually scored and the McMonnies index is
calculated by individually summing them up (perfect score = 45). The severity of dry eye
symptoms correlates with this index, with 14.5 points as the cut-off value for a diagnosis of
DED [19]. All participants were also asked about other co-risk factors, such as exposure to
air-conditioning and the use of visual display terminals (VDTs) [9].
folding a Schirmer paper strip at the notch and hooking the folded end over the temporal
one-third of the lower lid margin. The score is then measured as the length of wetting from
the notch after 5 min with the eyes gently closed. In accordance with previous studies, we
considered as pathological a cut-off of 10 s and 10 mm/5 min for BUT and Schirmer test I,
respectively [21].
3. Results
A total of 200 eyes of 100 health workers (44 men and 56 women) who wore FMs at
work were included. Their mean age was 44.56 years (±14.87). The study participants were
evaluated by the OSDI and McMonnies questionnaire to make an accurate assessment of
DED. An amount of 33 subjects exceeded the cut-off value of 13 for the OSDI screening,
whereas 19 subjects showed positive results (score > 14.5) on the McMonnies questionnaire.
The control group of 40 eyes of 20 subjects (8 males and 12 females) showed a mean age of
40.9 (±13.93). All demographic data of the study participants are summarized in Table 1.
Table Parameter
2. Clinical parameters collected
Before Workbefore SD
and at theEnd
endofofWork
the work shift.
SD p-Value
Shift Shift
Parameter Before Work Shift
Mean BCVA (LogMar) 0.05 SD0.09 End 0.07
of Work Shift
0.10 SD<0.001p-value
Mean BCVA (LogMar) Mean Schirmer test value0.05 0.09 0.07 0.10 <0.001
16.16 8.90 14.04 9.70 <0.001
Mean Schirmer test value (mm) (mm) 16.16 8.90 14.04 9.70 <0.001
Mean BUT (seconds) Mean BUT (seconds) 9.15 9.15 2.67
2.67 7.497.49 2.53 2.53<0.001<0.001
Mean FS (OGS) Mean FS (OGS) 0.10 0.10 0.35
0.35 0.510.51 0.66 0.66<0.001<0.001
BCVA, best corrected
BCVA, visual acuity;
best corrected visualBUT, break-up
acuity; BUT,time; FS, Fluorescein
break-up staining;
time; FS, OGS, Oxford
Fluorescein Grading
staining; Scale;
OGS, SD,
Oxford
standard deviation.
Grading Scale; SD, standard deviation.
(a) (b)
(c) (d)
Figure
Figure 1. Variations
1. Variations in break-up
in break-up time
time (BUT)
(BUT) of aof50-year-old
a 50-year-old female
female health
health worker.
worker. Representative
Representative
slit-lamp frames are from a BUT video of case 44. The first examination (08:05) shows (a) (a)
slit-lamp frames are from a BUT video of case 44. The first examination (08:05) shows stable
stable tear
tear
film after blinking at the start of the measurement area and (b) the development of dark
film after blinking at the start of the measurement area and (b) the development of dark areas at 7 s. areas at 7
s. The second examination (14:05) shows (c) stable tear film at the start of the measurement area and
The second examination (14:05) shows (c) stable tear film at the start of the measurement area and
(d) the development of bigger dark areas at 5 s (d).
(d) the development of bigger dark areas at 5 s (d).
There
There were
were notnot
anyany significant
significant differences
differences between
between thethe pre-shift
pre-shift clinical
clinical parameters
parameters
of the control group and the pre-shift clinical parameters of the study group (all (all
of the control group and the pre-shift clinical parameters of the study group p>0.05)
p > 0.05)
(Table
(Table 3). 3).
Table
Table 3. Clinical
3. Clinical parameters
parameters collected
collected at 8:00
at 8:00 a.m. AM
in the in the
control control
group group
and in andgroup.
the study in the study
group.
p-Value
Pre-Shift Parameter Pre-Shift Parameter
Control GroupControl Group Study Group
Study Group p-value
Mean BCVA (LogMar)Mean BCVA (LogMar) 0.025 0.025 0.05
0.05 0.06 0.06
Mean(mm)
Mean Schirmer Test Value Schirmer Test Value (mm)
18.68 18.68 16.16
16.16 0.12 0.12
Mean BUT (seconds) 10.38 9.15 0.24
Mean FS (OGS) 0.15 0.1 0.22
BCVA, best corrected visual acuity; BUT, break-up time; FS, Fluorescein staining; OGS, Oxford Grading Scale; SD,
standard deviation.
Life 2022, 12, 1491 5 of 11
As shown in Table 4, the control group showed no significant variation (p > 0.05) of
any clinical parameter (BCVA, BUT, Schirmer test, and FS).
Table 5. Study group for the dry eye disease assessment. In brackets, tests results are expressed in
mean (±SD).
In both groups,
In both therethere
groups, was awas
significant difference
a significant between
difference clinical clinical
between parameters collectedcol-
parameters
before
lected before and after the shift (p < 0.05). We also performed a comparative between
and after the shift (p < 0.05). We also performed a comparative analysis analysis be-
the tween
groupstheforgroups
BCVA,for Schirmer, BUT, andBUT,
BCVA, Schirmer, OGS and
score variance
OGS after working
score variance with FMs
after working with
(Figure 2).
FMs (Figure 2).
(a) (b)
Figure 2. Variations in clinical parameters after continuative use of surgical mask or respirators
Figure
during 2. Variations
work. in clinical
The bar graph parameters
(a,b) illustrates after
values continuative
of clinical use of(Schirmer,
parameters surgical mask or respirators
BUT, BCVA and
during work. The bar graph (a, b) illustrates values of clinical parameters (Schirmer, BUT, BCVA
OGS); bars represent mean values and standard errors (SE) in surgical mask group (green) and N95
and OGS); bars represent mean values and standard errors (SE) in surgical mask group (green) and
group (blue) as indicated in Table 7.
N95 group (blue) as indicated in Table 7.
Table 7. Variations
Table in clinical
7. Variations parameters
in clinical after continuative
parameters use of surgical
after continuative mask or N95
use of surgical maskduring
or N95work.
during
work.
Variations in Clinical Parameters
Schirmer (mm)
Variations
BUT (s)
in Clinical Parameters
BCVA (LogMar) FS (OGS)
FACE
Schirmer (mm) BUT (s) BCVA (LogMar) FS (OGS)
MASK PRE- POST-
SE PRE-
PRE-
SE POST- SE PRE-
POST-
SE
PRE-
SE
POST-
SE
PRE-
SE
POST-
SE
FACE MASK
WS WS WS WS POST- WS PRE- WS POST- WS PRE- WSPOST-
TYPE SE SE SE SE SE SE SE SE
Surgical
TYPE WS WS WS WS WS WS WS WS
16.14 0.94 13.05 1.02 8.86 0.28 7.06 0.25 0.06 0.01 0.07 0.01 0.1 0.04 0.43 0.07
Surgical Mask 16.14 0.94 13.05 1.02 8.86 0.28 7.06 0.25 0.06 0.01 0.07 0.01 0.1 0.04 0.43 0.07
Mask
N95 16.18 0.85 14.70 0.92 9.34 0.26 7.78 0.24 0.04 0.01 0.06 0.01 0.1 0.03 0.55 0.06
N95 16.18 0.85 14.70 0.92 9.34 0.26 7.78 0.24 0.04 0.01 0.06 0.01 0.1 0.03 0.55 0.06
BCVA, best corrected visual acuity; BUT, break-up time; FS, Fluorescein staining; OGS, Oxford Grading Scale; WS,
work shift.
As shown in Table 8, no significant differences between surgical masks and N95s were
observed (p > 0.05).
Life 2022, 12, 1491 7 of 11
Table 8. ANOVA with repeated measures analysis shows a statistically significant difference between
variables pre/post continuative use of FMs (p < 0.001). Face mask type (surgical or respirator) had no
statistically significant effect on clinical parameters after work (p > 0.05).
3.4. Correlations
Multiple regression analysis between demographic and clinical variations was per-
formed, with weakly significant results (Table 9). The analysis of variance showed that
BCVA variation was negatively correlated with age (R = −0.23; p = 0.0047) and OSDI score
(R = −0.20; p = 0.0303), and positively correlated with male sex (R = 0.15; p = 0.0187). BUT
variation was weakly correlated with time of VDT use (R = −0.08; p = 0.0469). All other
correlations were not significant.
4. Discussion
Although the continuative use of FMs is essential to control the COVID-19 pandemic’s
spreading, it may influence ocular surface health owing to air leaking around the mask’s
edge during inhalation and exhalation [8,11,13,14,22].
In our study, we investigated ocular surface changes through standard tests, including
BCVA, BUT, Schirmer test, and FS [9,23]. In particular, we analysed the variations in these
parameters in healthcare workers after a 7-h shift with continuous use of FMs.
Giannaccare et al. suggested that the role of FMs in ocular discomfort symptoms is due
to the rapid tear evaporation caused by air dispersion around the mask [11]. Considering
that DED is clinically divided into two subtypes based on tear production (deficiency of
aqueous or hypo-secretive component) or evaporation (hyper-evaporative) [9], MADE may
be included in the second category.
As previously reported, high airflow may lead to water evaporation from the pre-
corneal tear film with resulting dry spots formation [24–26]. Indeed, a significant decrease
in lower tear meniscus dimensions was shown in subjects with a baseline short BUT (<5 s)
after exposure to an airflow of 1.5 m/s [26]. On the other hand, the airflow effect in healthy
eyes is controversial. Some authors demonstrated an increase of lower tear meniscus
dimensions as a result of reflex sensory loop and tear secretion compensation induced
Life 2022, 12, 1491 8 of 11
by airflow exposure changes in the tear film [26]. In contrast, Wyon et al. reported that
an exposure of the tear film to high air velocity (1.0 m/s) for 30 min led to a significant
decrease in tear stability, as demonstrated by reduced BUT in healthy eyes [24].
Similarly, in our study, there was evidence of significant worsening of the clinical
parameters analysed in the entire cohort after wearing FMS continuously during work and
exposing the tear film to the related abnormal airflow.
Given the need to wear a FM throughout the whole shift, the ocular surface of health-
care workers’ eyes is subjected to limited airflow for a long time. This condition of chronic
ocular surface insult could lead to long-term damage of tear film stability, as demonstrated
by Mastropasqua et al. In fact, the continuative use of FMs for more than 6 h/day during a
3-month follow-up, worsened clinical indicators of ocular surface disease and increased
cellular and molecular inflammation bio-markers [14]. These signs of ocular surface dam-
age, seen in healthy subjects, were more severe in patients with DED even when they used
FMs for less than 6 h/day [14].
The present study shows daily ocular surface changes in healthcare personnel after
continuous use of FMs for about 7 h, and we supposed that these daily changes could lead
to long-term damage, as shown in the previous study by Mastropasqua et al. [14].
It is important to highlight that the analysis of clinical parameters before and after the
work shift could be affected by a physiological modification of tear film during the day,
which has been, however, a particularly controversial area of research [27–31]. Oncel et al.
reported that tear osmolarity does not have diurnal oscillations in normal subjects [27].
Similarly, no significant differences were found between morning and evening BUT mea-
surements or in tear ferning test patterns at different hours of the day [28,29]. On the
contrary, a daily decrease in tear meniscus volume by tear strip meniscometry was reported
by Ayaki et al. [30]. A study by Lira et al. [31] showed that tear film quantity, analysed by
Schirmer measurements and tear meniscus height, is unrelated to the hour it is assessed,
while there is worsening of tear film quality evaluated by BUT and non-invasive BUT. In
those studies [28–31], the authors suggested that the behaviour of tear film is different
between patients with diagnosed DED and normal subjects. This concept was in fact
confirmed by comparing visual function in the two groups. Walker et al. [32] reported that
individuals with dry eyes experience significant diurnal fluctuations in visual function
and in signs and symptoms of their condition due to an increased rate of keratitis in the
evening, whereas previous research on normal subjects demonstrated an increase in visual
function ability from morning to evening [33]. Our results are consistent with this finding,
showing a BCVA worsening at the end of the shift, with wearing FMs possibly playing a
pivotal role in that phenomenon.
Although all FMs are effective at slowing down the frontward flow and the horizontal
distance travelled by aerosol particles [15,16], a surgical mask not fitting the face tightly
causes greater air leakage around the sides during coughing [15], whereas an upward
leakage jet was described for FFP2 masks when it was not possible to seal them properly [15].
In our study, no demographic differences were found between the groups of surgical masks
and N95 wearers. Nevertheless, a worsening of the clinical parameters was found in both
the groups at the end of the work shift that we supposed to be related to an upward
dispersion of exhaled air. We suggest that the mask should be carefully shaped to the nose
to ensure a proper seal and, in turn, to reduce the airflow over the corneal surface.
Although Krolo et al. [12] observed a higher incidence of MADE in women and
subjects with a previous history of DED who wore FMs longer than 3 h/day, in the present
study, we did not find any significant correlation either between parameter variations and
demographic data nor between dry eye assessment (OSDI and McMonnies questionnaire)
and ocular surface changes. However, it is interesting to note that among the 33 healthcare
workers with dry eye symptoms, 21 showed BUT impairment (<10 s) before and after work
while 11 of them showed impairment only after work. Only one individual did not show
any homeostasis biomarker alteration.
Life 2022, 12, 1491 9 of 11
With regards to the use of goggles or eye protection devices, these were reported
to increase periocular humidity and therefore could be a protective measure for dry eye
occurrence or worsening [34,35]. However, in the present study, wearing glasses or eye
protection equipment was found to not influence the variation of parameters explored.
WHO estimates that between 80,000 and 180,000 healthcare workers died from COVID-19
between January 2020 and May 2021, converging to a medium scenario of 115,500 deaths [36].
The severity of the complications related to COVID-19 underlines the importance of using
preventive measures, especially in healthcare settings. Indeed, face masks are an essential
tool for healthcare personnel, and their use is mandatory due to the more concerning
consequences of SARS-COV-2 infection more than dry eye symptoms [18]. Neverthe-
less, long-term mask wearing has created a new problem to cope with, albeit of minor
importance.
Defining an occupational disease involves two main elements: the exposure–effect
relationship between a specific working environment and/or activity and a specific disease
effect, and the fact that these diseases occur among certain groups with a frequency higher
than the average for the rest of the population [37]. Further study is required to define
whether those criteria will be met and affect the magnitude of DED in mask wearers
worldwide.
To our knowledge, the present is the first study to focus on ocular surface daily
modifications in healthcare personnel wearing FMs. The short-term follow-up better
reflects the ocular surface damage induced by only using FMs.
Limitations of the current study include the lack of close monitoring of the subjects
during the work shift to ensure proper mask sealing. In addition, study participants
were asked about the use of video terminals, but no specific environment information
were evaluated: further study should be directed to also investigate humidity levels and
room lighting of each workday environment. Furthermore, the two study arms were
not homogeneous in terms of number: the control group of subjects not using FMs was
smaller than the study group. Another limitation was that we exclusively assessed the FMs’
influence with standard tests of DED, while a tear meniscus analysis with optical coherence
tomography, osmolarity testing, and the identification of pro-inflammatory markers may
add useful information.
Further population studies involving larger cohorts will be required to better define
the actual incidence and severity of DED in mask wearers worldwide. Given the intensive
FMs use, nowadays compulsory in many different settings, and the fact that DED often
remains unrecognized until symptoms are significantly advanced [7], a DED assessment
to evaluate the need for therapy should be performed as part of work health control. On
the other hand, healthcare personnel should observe a series of precautions to reduce the
impact of FMs on their ocular surfaces, such as ensuring the mask to be properly sealed onto
the nose reducing the airflow turbulence towards the eyes. In addition, following simple
healthy lifestyle measures, such as drinking an adequate amount of water to counteract the
drying process, may be appropriate.
Furthermore, considering the difficulty of predicting the duration of anti-pandemic
measures, a longitudinal examination of DED signs and symptoms in healthy subjects and
DED patients would be desirable to evaluate the long-term impact of these measures on
ocular surfaces.
5. Conclusions
FMs are an essential tool for healthcare personnel, and their use is mandatory to
avoid concerning consequences of SARS-COV-2 infection [18]. However, wearing them
for long-term periods, especially in work environments, has created several minor issues,
including modifications to the ocular surface and clinical signs of DED. The worsening of
clinical parameters did not correlate with the type of FM worn. Further studies are required
to avoid potential biases and identify ocular surface inflammation markers.
Life 2022, 12, 1491 10 of 11
Author Contributions: Conceptualization, F.T. and E.P.; formal analysis, F.T. and L.M.; investigation,
F.T. and S.P.; methodology, F.T., L.M., G.D. (Giuseppe Demarinis) and E.P.; supervision, G.O., M.C.,
G.D. (Gloria Denotti) and E.P.; writing—original draft, F.T., L.M. and E.P.; writing—review and
editing, G.D. (Giuseppe Demarinis), E.S.P., C.I., L.I.L. and E.P. All authors have read and agreed to
the published version of the manuscript.
Funding: This research received no specific grant from any public funding agency, or from the
commercial or not-for-profit sector.
Institutional Review Board Statement: The study was approved by the Local Institutional Review
Board on 31 March 2021 (PG/2021/5479). All procedures were performed in accordance with the
principles of the Declaration of Helsinki.
Informed Consent Statement: Written informed consent was obtained from each participant.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
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