Introduction
The coronavirus disease (COVID)-19 pandemic drastically affected the delivery of medicine around the world. The presence of a highly contagious respiratory virus presented an unprecedented challenge to neuro-ophthalmology. In response to the pandemic, the American Academy of Ophthalmology (AAO) issued a statement in March 2020 for ophthalmologists to “cease any treatment other than urgent or emergent eye care immediately.” 1 One month later, however the AAO issued another statement calling for a cautious re-opening of ophthalmic services.
A typical comprehensive ophthalmology exam (including neuro-ophthalmology) requires the neuro-ophthalmologist to be less than 2 m from a patient for much longer than 1–2 minutes. This requirements of the typical eye exam qualify as a prolonged patient exposure according to the Centers for Disease Control and Prevention. Reference Wan, Huang, Young and Lam2 Also, non-contact tonometry has been shown to be a micro-aerosol generating procedure because of tear film disturbances, potentially further increasing transmission risks. Reference Tang and Li3 Due to the risks imposed by the constraints of the eye exam and close proximity to the patient, we conducted a survey of the impact of COVID-19 on neuro-ophthalmology in the United States.
Methods
Data Collection
This study was approved by the Institutional Review Board at University of Nevada, Reno. A 14-question survey was emailed to neuro-ophthalmologists using a survey program (Momentive Inc., San Mateo, United States). Our survey was approved by and then emailed via the North American Neuro-ophthalmology Society (NANOS) listserv (NANOSNet) to its society members. Our survey was open from August 26, 2021, until October 9, 2021, for 68 days. A total of 30 neuro-ophthalmologists responded to our survey from three different countries; however, only responses from neuro-ophthalmologists practicing in the United States were included (two responses excluded).
Results
Twenty-eight neuro-ophthalmologists practicing in the United States responded to our survey. This represents 6% of neuro-ophthalmologists in the United States. In our survey, 64% of respondents were male (n = 18) and 36% were female (n = 10). The average age of a respondent was 55 years old. Respondents were distributed throughout the United States (Figure 1).
Geographic heat wave schematic of survey respondents by state within the United States.
Neuro-ophthalmologists that responded to our survey tended to be practicing in very large cities, with an average population of 1,018,000 people. Only three respondents to our survey were practicing in a city with a population of under 125,000 people. The majority of survey respondents worked in a university, public, or government hospital 61% (n = 17) while 39% worked in private practice, either in a group or solo (n = 11). The relatively low response rate of our survey (6%) may have resulted in a non-representative sampling of the population of United States neuro-ophthalmologists.
Prior to the COVID-19 pandemic, telemedicine was rarely used in neuro-ophthalmology practice (Figure 2). Pre-pandemic, the surveyed use of telemedicine was only 19%, which increased to 78% post-pandemic.
The adoption of telemedicine in neuro-ophthalmology greatly increased post-pandemic.
The adoption of telemedicine varied by age group (Figure 3). Adoption in telemedicine was 100% for neuro-ophthalmologists below 40 years of age. The lowest use of telemedicine usage was seen in the 40–49 years age group, which may have been a result of the low number of neuro-ophthalmologists in this age group responding to our study (n = 2). The remaining age categories showed very similar levels of usage of telemedicine.
The usage of telemedicine in neuro-ophthalmology by age groups.
After the first stay-at-home orders, 68% of the neuro-ophthalmologists in our study temporarily stopped seeing all patients (Figure 4). This period with no patient consultations varied widely, from less than a week (11%), more than a week but less than a month (36%), more than a month but less than 3 months (18%). 32% did not stop seeing patients at all, while 4% had to self-quarantine during this time.
Schematic of the amount of time that neuro-ophthalmologists stopped seeing patients after stay-at-home orders.
Neuro-ophthalmic patient volume varied widely throughout the pandemic (Figure 5).
Neuro-ophthalmic patient volume after the start of the COVID-19 pandemic.
For the first month of the pandemic, patient volume significantly declined, with many reporting almost no patients. Two months into the pandemic, the majority of neuro-ophthalmologists reported a significantly lower patient volume. After 6 months, patient volume tended to be similar to pre-pandemic levels. One year after the start of the pandemic, patient volume has increased significantly.
A variety of neuro-ophthalmic diseases were reported to have increased in severity during the pandemic by 77% of survey respondents (Figure 6). Of these conditions, idiopathic intracranial hypertension was reported to have worsened the most, followed by compressive optic neuropathies. Twenty-three percent (23%) of responding neuro-ophthalmologists reported no difference in disease severity.
Neuro-ophthalmic diseases reported to have worsened after the COVID-19 pandemic.
Discussion
COVID-19 stay-at-home orders created significant barriers to neuro-ophthalmic care in the United States. Based on our survey, we believe that the likely pent-up demand for neuro-ophthalmic care after the pandemic will increase significantly. Neuro-ophthalmology is one of the most outpatient-oriented areas of medicine. The thousands of canceled neuro-ophthalmic visits at the start of the pandemic likely led to the delay of treatment that may have potentially led to significant preventable loss of vision. This is particularly concerning due to the relatively low number of neuro-ophthalmologists relative to the United States population. The waitlist for a new appointment in neuro-ophthalmology in most parts of the country was already long pre-pandemic, and we believe that the pandemic shutdowns and restrictions likely further increased the difficulty to promptly access neuro-ophthalmic care. Reference DeBusk, Subramanian, Scannell Bryan, Moster, Calvert and Frohman4 Debusk et al. Reference DeBusk, Subramanian, Scannell Bryan, Moster, Calvert and Frohman4 reported pre-pandemic that there are no practicing neuro-ophthalmologists in six US states. Additionally, only eight states had met the ratio of one clinical full-time equivalent for every 1.2 million individuals. This likely explains the trend of significantly increased patient volume 1 year after the start of the COVID-19 pandemic seen in our study.
A study by Stunkel et al. Reference Stunkel, Sharma and Mackay5 showed the importance of early consultations with neuro-ophthalmology, in a study of 496 consecutive adult patients seen at three different neuro-ophthalmic clinics across the United States. This study found that in 49% of these patients, the referral diagnosis was incorrect and 26% of these misdiagnosed patients experienced harm. Reference Stunkel, Sharma and Mackay5 An early referral to neuro-ophthalmology would have also prevented the need for unnecessary diagnostic imaging, laboratory testing, and treatment in many of these patients. This study shows the important of neuro-ophthalmic consultations and shows the potential danger that exists when barriers to neuro-ophthalmic care exist such as the COVID-19 pandemic.
Moss et al. Reference Moss, Ko and Mackay6 studied neuro-ophthalmic patient encounters for a 3-month-long period in 2020 and found that compared with the year prior, neuro-ophthalmic care volume decreased, the use of telemedicine increased and the proportion of consults with established patients increased. It is important to note that this study only included four neuro-ophthalmologists, located in two geographic regions; however, these findings mirror the trends seen in our study. Jin et al. Reference Jin, Canizares, El-Defrawy, Bogale and Buys7 examined the usage of telemedicine in ophthalmology in Ontario, Canada, and found a significant increase at the start of the pandemic, which later decreased. This study also found that ophthalmologists aged between 60 and 69 years were most likely to provide telemedicine services, in contrast to our study which found neuro-ophthalmologists below the age of 40 to be most likely to do so.
The COVID-19 pandemic highlighted the importance of telemedicine in neuro-ophthalmic practice. Phone visits may also be useful to discuss recent laboratory results, neuroimaging, and medication tolerance and compliance. Although less optimal than an in-person visit, video telemedicine can also be used to allow for external examinations to visualize conditions such as ptosis, strabismus, or orbital issues. Further advances are required to perform a full neuro-ophthalmic assessment, without the need for a patient to be physically present. The development of this technology would not only be useful for use during future pandemics but also allow patients in remote regions to access ophthalmic care. Our survey showed a significant lack of neuro-ophthalmologists practicing in small cities, which is a common trend in neuro-ophthalmic practice.
Additional research is needed to address the challenges to face-to-face patient care highlighted during the COVID-19 pandemic. Reference Waisberg, Ong, Zaman, Kamran, Tavakkoli and Lee8 Specifically, home-based, portable, or even “pop-up” testing sites could be a potential countermeasure to care restrictions in any future pandemic. Serious potential countermeasures considered at the home institution of one of us (AGL) included “pop-up” drive through intraocular pressure check stations, home computer-based visual acuity, color, and visual field testing applications and software, and drone-based testing for home delivery. Fortunately, the restrictions were relatively short lived and these countermeasures were never deployed. In addition, our research group is currently developing a head-mounted visual assessment device to assess subtle visual changes for astronauts in spaceflight. Reference Ong, Tavakkoli and Zaman9–Reference Waisberg, Ong, Zaman, Kamran, Lee and Tavakkoli11 This novel technology may one day be useful terrestrially to aid ophthalmologists in conducting rapid, and comprehensive visual assessments at remote sites or at the patient’s home. Reference Waisberg, Ong and Paladugu12 Having the ability to conduct an accurate visual assessment with a low-cost headset could be vital for ophthalmic monitoring in remote communities as well as in developing countries. Reference Waisberg, Ong and Paladugu13
Conclusion
To our knowledge, this study represents the largest study evaluating the impacts of COVID-19 on the subspecialty of neuro-ophthalmology. Neuro-ophthalmologists’ patient volume across the United States drastically slowed during the first two months of the pandemic, normalized around 6 months into the pandemic, and after 1 year increased significantly. We also report a significant increase in the use of telemedicine in neuro-ophthalmology.
Acknowledgements
We thank the North American Neuro-Ophthalmology Society (NANOS) for their support and for distributing this survey to NANOS members for this study.
Statement of authorship
E.W. – Study Design, Data Acquisition, Writing, Figure Development.
J.O. – Study Design, Data Acquisition, Writing, Figure Development.
N.Z. – Review, Intellectual Support.
S.K. – Review, Intellectual Support.
A.G.L. – Review, Intellectual Support.
A.T. – Study Design, Data Acquisition, Review, Intellectual Support.
Conflict of interest
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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