The Impact of COVID-19 Pandemic on Ophthalmic Referrals within a Tertiary Academic Center in Oman.

PURPOSE: To investigate the impact of coronavirus infection disease-19 (COVID-19) pandemic on ophthalmic referrals within an academic tertiary center in Oman.
METHODS: Retrospective chart review of internal referrals received and evaluated by the ophthalmology department between March 1and August 31, 2020 (COVID-19 period) compared to a corresponding period in 2019 (pre COVID-19). Data included patient demographics, referral details, ocular diagnosis, intervention, and discharge plan.
RESULTS: Referral volume significantly decreased by 58.2%; from 2019 prepandemic to 510 (P = 0.001), with the lowest in April and May 2020. Patient demographics did not differ significantly, but "urgent" referrals reduced by 96.2% (P < 0.001). Main reasons for referrals were reduced vision and screening in both periods. During pandemic, referrals for screening purposes increased from 30.3% to 37.9% (P = 0.013) and for reduced vision decreased from 30% to 23.3% (P = 0.021). Dry eye syndrome increased in frequency during 2020 (from 2.9% to 7.3%, P = 0.002) but cataracts and conjunctivitis both decreased (from 4.7% to 2.1%, P = 0.046 and from 2.3% to 0.3%, P = 0.013, respectively). Ocular trauma remained stable (from 0.8% to 0.3%, P = 0.456), but the proportion of chemical injuries increased by 13.7% (P = 0.025). There was a drastic decrease in interventions from 37% to 26.1% (P < 0.001) and an increase in discharge rate from 61.2% to 75.8% (P < 0.001).
CONCLUSION: The impact of COVID-19 pandemic on ophthalmic referrals within a tertiary academic centre in oman referral reductions and changes in pattern and characteristics as an epiphenomenon of COVID-19 reflect the extent of impact specifically in an Omani context. This information is vital for planning proper resource utilization, the adoption of innovative care delivery, and improving referral system pathways. Copyright:

Introduction

The coronavirus infection disease-19 (COVID-19) pandemic has challenged health systems across the world. Since the pandemic was declared on the of March 11, 2020, almost every country (90%) reported disruptions to health services according to a WHO global survey.[1]

The situation in the Sultanate of Oman was no exception since it registered its first two cases of novel coronavirus on of February 24, 2020.[2] Oman, like many other countries, has adopted several strict measures to fight coronavirus. These precautionary measures have affected the normal operations of several sectors including the health sector.

Health-care utilization has decreased by about a third showing considerable variation and greater reductions among people with less severe illness.[3] Ophthalmic services were disproportionately impacted when redistribution of resources was made toward more essential services. The Commonwealth Fund reported ophthalmology as the most affected subspecialty with a 79% reduction in patient flow.[4]

One of the two largest public medical facilities in Muscat, Oman is Sultan Qaboos University Hospital (SQUH) which is also an academic medical center. Its department of ophthalmology has a triple mission of clinical care, teaching, and research. Like many other institutions, it was forced to implement practice changes to adapt to the new circumstances imposed by the pandemic. Routine clinical care practically ceased by deferring elective surgeries and outpatients’ appointments. In view of the witnessed contracted volumes of ophthalmic outpatient visits, admissions, and nonurgent surgical interventions in the department, we hypothesized that ophthalmic referrals were among the areas affected as well. The aim of this study was to evaluate the impact of the pandemic on the referrals to the ophthalmology service at a tertiary teaching hospital in the country in terms of its magnitude and pattern over a course of 6-month.

Methods

We performed a retrospective analysis of data of all internal hospital referrals to the department of ophthalmology at SQUH in Muscat, Oman during a 6-month period of the pandemic from March 1 to August 31, 2020 (COVID-19 period). This was compared with a corresponding period in the year preceding the pandemic, 2019 (pre-COVID-19 period). This study was approved by the Medical Research Ethics Committee at the College of Medicine and Health Sciences in SQU and conformed to the provisions of the Declaration of Helsinki. Consent was waived due to the retrospective nature of the review; while the privacy of data was maintained with confidentiality.

All internal referrals originated from one of the following: inpatient wards, emergency department (ED), or outpatient clinics which include outpatient specialty clinics and outpatient staff/student primary care clinics. The primary outcome of our study was to determine the impact of COVID-19 on the volume of internal SQUH referrals to the ophthalmology service compared to a control period from a year earlier. Our secondary outcomes were to draw comparisons of patient demographics, characteristics of referrals, and summary of ophthalmologist's assessments of these referrals between the two above-mentioned periods.

Patients of all age groups from the adult and pediatric population referred internally and who were assessed by an ophthalmologist during the study period were included. External referrals originating from outside the hospital, rejected referrals and patients with incomplete hospital records were excluded.

Data extracted from the referral records included demographic data (age, gender, and residential locality), referral details (referral date, priority of referral, reason for referral, and origin of referral request), and summary of ophthalmologists’ assessment (ocular diagnosis, intervention, and disposition). Referral priorities were categorized as routine or urgent if an ophthalmic assessment was required within 48 h to avoid negative consequences on vision. Diagnoses and interventions were documented using the International Classification of Diseases, tenth revision codes (ICD-10-CM). The list was reviewed by two ophthalmologists to ensure correct data entry and grouping.

Statistical analysis

All data were recorded, anonymized, and verified by two members of the study group for their accuracy. The data were processed and analyzed using the Statistical Package for the Social Sciences (version 20.0, SPSS Inc., Chicago, IL, USA). Descriptive statistics were used to evaluate the data. Categorical variables were analyzed by Chi-squared (χ2) test. To detect departures from the normal distribution, a Shapiro–Wilk's test was performed for all variables. Continuous variables were compared by conducting a Student's t-test for independent variables. Statistical significance of the differences between groups for qualitative variables was assessed using Fisher's exact test. A P < 0.05 was considered statistically significant.

Results

A total of 1729 charts were reviewed over the two study periods. During the COVID-19 period, from March 1 to August 31, 2020, the ophthalmology service received only 510 internal referrals compared to 1219 in the preceding year (pre-COVID-19). This represents a significant 58.2% decrease in referral volume between the two time periods (P = 0.001). The overall total referrals and their monthly trend for both periods are shown [Figure 1]. During the COVID-19 period, the month of May experienced the lowest volume of referrals (n = 50, 9.8%) followed by April (n = 65, 12.7%).

Figure 1

Monthly internal ophthalmic referrals over the two study periods; pre-COVID-19 in 2019 (blue) and during COVID-19 in 2020 (orange)

Overall, the proportion of referrals by age and gender did not differ significantly during the pandemic [Table 1]. Patient age was categorized by decade. Those younger than 10 years of age constituted the majority of referrals followed by those over 60 years in both periods. There was a slight increase in proportion of those younger than 10 years of age from 26.3% (n = 320/1219) to 30% (n = 153/510) during the pandemic and a slight decrease in those 60 years and above from 16.4% (n = 200/1219) to 13.7% (n = 70/510). However, these differences were statistically insignificant (P = 0.367). Patients residing in the capital city Muscat comprised majority of referrals in both periods with an insignificant difference pre and during COVID-19 [Table 1].

Table 1

Demographics of ophthalmic patient referrals presenting pre corona virus disease-2019 and during corona virus disease-2019 study periods

Variables	Pre COVID-19 (2019), n (%)	During COVID-19 (2020), n (%)	P
Gender
Male: female	635:584 (52, 48)	245:265 (48, 52)	0.219
Age groups (years)
<10	320 (26.3)	153 (30.0)	0.367
10-20	150 (12.3)	54 (10.6)
20-30	157 (12.9)	52 (10.2)
30-40	102 (8.4)	45 (8.8)
40-50	158 (13.0)	82 (16.1)
50-60	132 (10.8)	54 (10.6)
≥60	200 (16.4)	70 (13.7)
Residential locality
Muscat (capital city)	496 (40.7)	181 (35.5)	0.111
Outside muscat (other governorates)	723 (59.3)	329 (64.5)

COVID-19: Corona virus disease-2019

Referrals of urgent priority significantly decreased from 56% (n = 683/1219) to 5% (n = 26/510) (P < 0.001) during the pandemic period. Whereas routine referrals significantly increased from 44% (n = 536/1219) to 95% (n = 484/510) (P < 0.001). There was a reduction in volume from all originating sites but in both periods most referrals originated from inpatient wards (pre 42% vs. during 41%) followed by the ED (pre 33% vs. during 39%) and outpatient clinics (pre 25% vs. during 20%) respectively. Volume reductions were 66.6% from outpatient departments, 59.2% from inpatient wards, and 50.6% from ED. Common sources of inpatient ward referrals in descending frequency were adult hematology (pre n = 32 vs. during n = 22), pediatric neurology unit (pre n = 32 vs. during n = 18), clinical genetics (pre n = 20 vs. during n = 13), general pediatric wards (pre n = 14 vs. during n = 11) and neonatal ICU (pre n = 17 vs. during n = 8). The distribution of main reasons for referrals pre and during COVID-19 is shown in Figure 2. The most common reason for referrals was decreased vision followed by screening purposes in both periods. However, there was a significant increase in % of eyes that were referred for screening purposes (pre n = 369; 30.3% vs. during n = 193; 37.9%, P = 0.013) and a decrease in % of patients referred for reduction in vision (pre n = 365; 30% vs. during n = 119; 23.3%, P = 0.021). The other reasons for referrals did not differ significantly pre and during the pandemic. Specific screening request for diabetic retinopathy rose nonsignificantly from 11.5% pre COVID-19-15.8% during COVID-19 (P = 0.541). There was a nonsignificant difference in referral volumes requesting for posttraumatic evaluation and eye redness during the pandemic compared to the prepandemic period.

Figure 2

Distribution of common reasons for internal ophthalmic referrals in pre COVID-19 (blue) and during COVID-19 (orange)

The diagnostic categories and their frequencies both pre and during COVID-19 is shown in Table 2. According to the ICD-10 classification, the top five diagnostic groups in the pre COVID-19 period (in descending order) were normal eye exam (n = 581,47.7%), refractive errors (n = 128, 10.5%), posterior segment pathologies (n = 96, 7.9%), adnexal/orbital disorders (n = 78, 6.4%), and cataracts (n = 57, 4.7%). Whereas during the pandemic the common categories were normal eye exam (n = 329, 64.5%), dry eye syndrome (n = 37, 7.3%), posterior segment pathologies (n = 34, 6.7%), keratitis/corneal abrasion (n = 28, 5.5%), and refractive errors (n = 27, 5.3%). Some specific diagnoses significantly differed between both periods; cataracts decreased from 4.7% pre to 2.1% during COVID-19 (P = 0.046) as well as conjunctivitis cases from 2.3% pre to 0.3% during COVID-19 (P = 0.013). However, dry eye syndrome increased from 2.9% pre to 7.3% during COVID-10 (P = 0.002). Interesting to note, ocular injuries as a diagnosis did not differ significantly between both periods (from 0.8% pre to 0.3% during COVID-19, P = 0.456). Despite this, the composition of these injuries differed during the pandemic with an increase in proportion of chemical injuries than prepandemic (pre n = 6/35; 17.1% vs. during n = 4/13; 30.8%, P = 0.025).

Table 2

Diagnostic categories of internal ophthalmic referrals in pre- corona virus disease-19 and during corona virus disease-19 study periods

	Pre COVID, n (%)	During COVID, n (%)	P
Anterior segment	133 (10.9)	67 (8.2)	0.139
Cataract	57 (4.7)	11 (2.2)	0.046*
Glaucoma	21 (1.7)	5 (1.0)	0.427
Neuro-ophthalmic	46 (3.8)	21 (4.2)	0.741
Normal eye exam	581 (47.7)	329 (64.5)	<0.001*
Adnexal and orbital	78 (6.4)	20 (3.9)	0.124
Posterior segment	96 (7.9)	34 (6.7)	0.541
Refractive error	128 (10.5)	26 (5.1)	0.003*
Strabismus	38 (3.1)	4 (0.8)	0.036*
Uveitis	4 (0.3)	5 (0.9)	0.356
Endophthalmitis	1 (0.1)	0	1.000
Ocular injury	35 (2.9)	13 (2.5)	0.456

*Significant P<0.05, COVID-19: Corona virus disease-2019

Interventions drastically differed between the two time periods. Surgical therapies reduced from 4.5% to 1.8% (P = 0.027) and medical therapies from 33.8% to 24.3% (P = 0.002). Patients for follow-up care were significantly reduced during the COVID-19 period and an increase in the patient discharge rate was noted. Both differences were by 14% (P < 0.001) [Figure 3].

Figure 3

Intervention and discharge plan of internal ophthalmic patient referrals in pre COVID-19 (blue) and during COVID-19 (orange) study periods

Discussion

This study revealed a significant reduction of 58.2% in the volume of referrals during a 6-month time frame of the pandemic in comparison to a similar period in the preceding year. This is in concordance with a study that witnessed a decrease in emergency ophthalmology referrals to a Canadian tertiary academic center by 54.2%.[5] A similar impact was observed on outpatient referrals to a pediatric ophthalmology service in UK which was reduced by 50.2%.[6] In this study, the most reduction was from the outpatient department (by 66.6%), which is expected due to reduced patient volumes booked in outpatient clinics. However, numerous studies confirmed the largest fall to be from the ED, which in our study was 50.6% reduction in ED referrals alone. This impact is similar to acute ophthalmology services in Moorfields Eye Hospital where attendances to the ED reduced by >50%.[7] Several other European publications have found 65%–73% decrease in ophthalmic emergencies in 2020 in comparison to a comparable period.[8910]

The seasonal trend of referrals in the pre-COVID-19 period seems to peak in March and gradually decreases over the subsequent months as patients usually escape abroad for the Summer. However, during the pandemic, there was a shift in this trend whereby referrals showed a major dip in April and May [Figure 1]. This comes to no surprise, as the country reported its first death from the virus on April 1, 2020. This followed tighter restrictions in April with an enforced lockdown extending into May with an additional movement restriction between governorates which could explain the excessive drop in this period. Throughout the remainder of the study, referral volumes remained low despite the slight ease in restrictions.

Muscat is the most populated city in Oman and during the pandemic continued to have the highest number of confirmed cases and deaths in the country. Therefore, it is not unusual for it to constitute the majority of referrals in both pre and during COVID-19.[11] The pediatric population constituted most referrals in both periods. This is not surprising as Oman has a relatively young population structure with 30.45% under 14 years of age.[12] Although over 65 years are a minority, the ophthalmology service in the country mostly caters to patients from these extreme age groups, which are considered high-risk groups if COVID-19 is contracted. Although statistically insignificant, the relative increase in children and decrease in elderly proportions has a plausible explanation. The implementation of online learning meant children had more free time to seek medical care and it was common knowledge at the time that they were potentially less vulnerable for contracting COVID-19 and if infected were less symptomatic.[13] Governmental restrictions also advised cocooning of older patients. In addition to this, overall decline in referrals was likely due to a combination of patients’ attitudes, perception of personal risk with contracting the infection in the hospital setting and institutional guidelines resulting in a reduced department workload.

Characteristics of referrals were altered during the pandemic. Ocular and visual screening requests were increased, and the opposite occurred with decreased vision, corroborating that majority of referrals during the COVID-19 pandemic were nonurgent. Consistent with this was a significant increase in diagnoses of normal eye examinations. Despite reports of conjunctivitis as symptoms of COVID-19, conjunctivitis referrals significantly decreased in frequency during the second study period.[14] This could be due to enhanced awareness on hand hygiene, social distancing measures, and school closure contributing to the reduction in the spread of contagious diseases including infectious conjunctivitis. The change in diagnostic types of referrals reflected the change in practice patterns. There was a significant decrease in cataracts with the cancellation of elective surgeries. As for ocular traumas, their presentation remained unchanged. Contradicting reports exist in the literature with Pellegrini et al. reporting a 68.4% reduction in ocular trauma across different types of injuries during the pandemic due to stay-at-home orders and limited nonessential business or personal travel.[15] Whereas the oxford eye hospital reported an increase in the number of ocular trauma cases due to “do-it yourself” tasks.[16] Our study revealed an increase in the proportion of chemical injuries partly due to an increased number of sanitizer-related ocular injuries rather than occupation related, in keeping with recent reports in the literature.[1718] Interesting to note, there was a significant increase in dry eye syndrome. It is hypothesized that patients under lockdown are at risk of ocular surface alterations due to a number of predisposing factors. The abuse of digital devices, malnutrition, and sleep/stress disorders could be triggered. This phenomenon was recently proposed in the literature as “quarantine dry eye.”[19]

Management patterns in our study showed a decrease in interventions in keeping with the profile of patients seen during the pandemic. There was also an increase in discharges to the community as physicians had a tendency to avoid follow-up visits during this period. International and local recommendations to limit routine ophthalmic examinations and restrict in-patient evaluations to urgent and emergent ocular conditions have been implemented by deferring nonurgent follow-ups in the clinic.[20] Contrary to this, we revealed a relative increase in the composition of nonurgent referrals compared to urgent cases to the eye service from across the hospital which contradicts this recommendation. The reduction in urgent referrals could be attributed to the overall decline in ED attendances during the pandemic as well as possibly the lack of insight into the risk-to-benefit ratio of failing to seek prompt medical attention, especially in uncertain times such as during the pandemic. In addition, a US experience was dissimilar to our findings with a reduction of patient encounters with nonurgent screening requests during COVID-19 possibly due to the implementation of telemedicine. Telemedicine was advised for screening and for nonurgent patient concerns to limit unnecessary in-person evaluations.[2122] The low utility of teleconsultation in our facility could have contributed to the observed relative increase in routine referrals. This was likely attributed to cultural differences, ethical and confidentiality issues, patients’ level of education, the unfamiliarity of using technological software and their poor perceptivity of telemedicine. In addition, most of our population from the young pediatric age group, we assume, will be difficult to assess remotely and still require a face-to-face assessment.[6]

The detrimental consequences of change in volume and urgency of referrals include the inability to optimally meet the educational requirements for trainees and the reliance on alternative methods of teaching. A rebound of workload is anticipated with likely a presentation of more advanced cases that have a poorer prognosis requiring more intensive or frequent treatments.

The study's main strength is the duration covering the full first wave of the pandemic. The limitations are the exclusion of external referrals and the lack of involving a main national trauma centre which perhaps can impact the observed results especially the effect on ocular traumas.

Conclusion

Results from this study highlight the importance of improving referral pathways to decrease nonurgent referrals during a crisis, searching for innovative ways to evaluate referrals such as resorting to telehealth and developing recovery strategies for the anticipated aftermath. Future studies on the subsequent waves of the pandemic would be helpful to draw further conclusions.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.