Characterizing industry payments to ophthalmologists before and after onset of the COVID-19 pandemic

Abstract Purpose The COVID-19 pandemic had profound effects on many different aspects of our healthcare system and the relationship between industry and physicians was no exception. The present database study evaluates industry payments to ophthalmologists in order to identify whether there are significant differences in industry payments to ophthalmologists before and after onset of the pandemic. Methods The Centers for Medicare & Medicaid Services Open Payments Database was queried for all ophthalmologists who received industry payments between 2018 and 2021. Pre-Covid was defined as 2018–2019 while post-Covid was defined as 2020–2021. Payment date, value, type, company making payment, and state of recipient were recorded. The top ten companies and states in terms of payment value were included in analysis. Generalized Estimating Equations (GEE) modeling was used to assess significance. Results There were 729,263 industry payments to 20,832 ophthalmologists totaling $817,892,867.54 included for analysis in this study. We found that there was a significant increase in the mean value of research payments and a significant decrease in the mean value of general payments after the onset of the pandemic (both p < 0.001). We also report significant changes in industry payments to ophthalmologists based on the company making the payment and the state in which the ophthalmologist practices. Conclusions Our results suggest that significant differences exist in industry payment patterns to ophthalmologists following onset of the COVID-19 pandemic. Understanding underlying reasons for the observed differences may improve our understanding of the relationship between industry and clinical ophthalmology.


A. Introduction
The short-term effects of the pandemic on both pharmaceutical industry corporations and healthcare workers are well documented [1,2].Given the extensive impact of the pandemic on both groups, of interest is characterizing industry payments to physicians, speci cally ophthalmologists, before and after the COVID-19 pandemic.Inoue et al. found that, in the months of April to December of 2020, there was a signi cant decrease in industry payments to physicians relative to the months and years prior.Of note, the types of industry payments with the greatest decreases observed were predominantly in categories requiring physical contact, such as meals or travel [3].
The analysis of industry payments was only made possible a little over a decade ago when the Physician Payments Sunshine Act was passed into law in 2010 with the intention of increasing transparency of nancial transactions between physicians and corporations [4,5].The national Open Payments Database, sponsored by the Centers for Medicare & Medicaid Services, exists as a direct product of this legislation, where all industry payments to physicians are recorded, including but not limited to the nature of payment, the corporation making the payment, and the value of payment [6].
As a result, the literature is extensive in ophthalmology regarding industry payment trends.Just recently in fact, Kalva et al. characterized industry payments to ophthalmologists for research from 2014 to 2020 [7].Gender disparities and a lack of representation for female ophthalmologists receiving industry payments have been highlighted previously [8].Despite this, it seems that no study has been published to date looking speci cally at differences in industry payments to ophthalmologists and physicians following the onset of the COVID-19 pandemic.Hence, in this investigation we look to assess if signi cant discrepancies exist for industry payments made in 2020 and 2021 to ophthalmologists relative to payments made before the COVID-19 pandemic in 2018 and 2019.

B. Methods
The Centers for Medicare & Medicaid Services Open Payments Database was queried for all ophthalmologists who received industry payments between 2018 and 2021.Pre-Covid was de ned as 2018-2019 while post-Covid was de ned as 2020-2021.Payment date, value, type, company making payment, and state of recipient were recorded.The top ten companies and states in terms of payment value were included in analysis.Generalized Estimating Equations (GEE) modeling was used to assess signi cance.

C. Results
There were 729,263 industry payments to 20,832 ophthalmologists totaling $817,892,867.54included for analysis in this study.Research-based payments composed of 9.07% of the number of payments and 71.40% of the total monetary amount of payments (Table 1).Among the non-research payments, food and beverages composed of the majority of payments (78.35% of total number of payments made), but represented only 2.53% of the monetary amount.After research payments, faculty or speakers was the classi cation with the greatest percentage of dollar amount paid (10.11%).Overall, the median payment was $22.21, and median research payment was $900.00.
Carl Zeiss was the company with the greatest mean value of payments made ($5,507.32)pre-COVID and Genentech had the greatest mean value post-COVID ($12,813.70) of all companies (

D. Discussion
The relationship between physicians and industry is a major source of public distrust in the American healthcare system.A 2016 survey of over 1,300 US adults showed that public disclosure of industry payments to physicians lowered patient trust, regardless of whether their physician had received any payments [9].In a study from Hwong et al., people were more likely to perceive physicians receiving industry payments as dishonest, with physicians receiving higher payments being perceived as more dishonest [10].Not only do industry payments to physicians seriously harm physician-patient relationships, but several studies also strongly suggest that industry payments can in uence the care a patient receives [11,12].Recognizing trends in industry payments to physicians is vital for fully understanding the in uence these payments can have both on public perception and the treatment physicians deliver.The COVID-19 pandemic is the greatest disruption the American healthcare system has seen in recent years.The pandemic has had a signi cant in uence on the American healthcare system and healthcare expenditures [13].Given this in uence, this study aims to understand what differences, if any, exist for industry payments to ophthalmologists before and after onset of the COVID-19 pandemic.Several prior publications have used the Open Payments Database to address industry payments to ophthalmologists, and we look to speci cally analyzed any changes in industry payments to ophthalmologists before and after the beginning of the COVID-19 pandemic made possible by the availability of 2021 data [4,7,[14][15][16]].This study additionally serves as an update on general research payment trends to ophthalmologists.
Total industry payments to ophthalmologists from 2018 to 2021 amounted to over $800 million paid to 20,832 ophthalmologists (Table 1).The majority (71.4%) of the $800 million was for research-related payments, which includes direct compensation to physicians for research, funding for medical studies, and payments to study participants for study-related expenses.Research-related payments made up only 9% of the total number of payments and only 8% of all ophthalmologists received any research-related payment.This indicates that the majority of all money paid to ophthalmologists by industry was made in large payments to a relatively small number of ophthalmologists for research.This is consistent with another study from Tringale et al. showing that, compared to general payments, research payments to physicians regardless of specialty were of disproportionately larger value and were paid to a relatively small number of physicians [6].Although the eld of ophthalmology is re ective of payment trends seen across all physicians, the type and distribution of industry payments are eld-dependent.For example, a study from Pakanati et al. excluded research payments when evaluating industry payments to hospitalists on the grounds that the number and value of payments were so small as to be insigni cant [17].The remainder (28.6%) of the $800 million paid to ophthalmologists by industry was in the general category (Table 1), which includes a broad range of subcategories such as consulting fees, food and beverages for work-related meetings, and gifts, among others.Within the general category, the two subcategories with the greatest value paid were consulting fees and faculty or speakers (8.59% and 10.11% of total paid, respectively), whereas the number of payments of these types made was relatively small (3.31% and 2.28% of all payments, respectively).Payments for food and beverage made up the majority of total payments made (78.35%), while being a small percentage of the total value paid (2.53%).Overall, this indicates that research payments are generally much greater than general payments, exempli ed by comparing the median values of research and general payments ($900 and $21, respectively).This is consistent with other publications evaluating industry payments to physicians using the Open Payments Database [6, 18].
There was a signi cant increase in the mean payment to ophthalmologists after the beginning of the COVID-19 pandemic compared to before (Table 3).Notably, the median payment decreased slightly after the onset of the pandemic, suggesting that there was a relative increase in high-value payments.This increase in high-value payments is attributable to the notable increase in the mean research-related payment, which increased by 145% after the beginning of the pandemic.The number of research-related payments also increased.Conversely, there was a 25% decrease in the mean general payment after the pandemic and the number of general payments also decreased.Concordant with our ndings, a study from Murayama et al. evaluating changes in general payments to rheumatologists pre-and postpandemic found that the total value of general payments and the number of rheumatologists receiving general payments both decreased signi cantly after the onset of the pandemic [19].Other publications reporting industry payments to plastic surgeons or infectious disease physicians before and after the onset of the pandemic show similar trends [20,21].Within the general category, the mean payment to ophthalmologists for consulting fees, education, faculty or speakers, food and beverage, gifts, honoraria, royalty or license, and travel and lodging all decreased signi cantly (p < 0.05).Social distancing and the cancellation of many in-person events explains drastic changes in payments made for food and beverage and travel and lodging, as many events moved to a virtual format.It is also likely that social distancing was the cause of changes in payments for consulting fees, education, and honoraria, as the shift to a virtual format decreased the cost of services rendered by ophthalmologists (and thus payments made to said physicians).
A study from Inoue et al. that evaluated industry payments to physicians in 2020 in the months before and after the onset of the pandemic had similar ndings.The group found that there was a signi cant decrease in the mean value of industry payments to physicians for food and beverage, travel and lodging, consulting fees, faculty or speakers, and education and honoraria.Aside from food and beverage and travel and lodging, the group avoids speculating on a speci c reason for changes in the value of payments [3].The signi cant decrease in payments to ophthalmologists made for royalty or licensing fees, which are payments based on sales of products using a physician's intellectual property, was likely due to a sharp decrease in medical device sales during the pandemic.Many hospitals redirected funding from nonessential equipment to personal protective equipment (PPE), ventilators, and other general hospital supplies [22,23].Conversely, the mean payment for entertainment increased signi cantly, although the number of entertainment-related payments dropped from over 600 to only 25 after the onset of the pandemic.This subcategory covers cost of attendance at recreational or sporting events, many of which were likely canceled or postponed after the onset of the pandemic.The increased mean payment for entertainment is likely explained by industry paying for more expensive events, which were less likely to be canceled in response to the pandemic.
Table 2 shows the top 10 companies making payments to ophthalmologists before and after the beginning of the pandemic.The median payment for all companies aside from Carl Zeiss, Genentech, and Regeneron decreased during the pandemic.The mean payment for all companies aside from AbbVie, Alcon, and Johnson and Johnson changed signi cantly during the pandemic, although there is no consistent direction of change amongst all companies.Based on these results, it seems that changes in payments made by the top 10 companies before and during the pandemic are company-dependent and followed no discernable trend.
Table 6 shows industry payments to ophthalmologists for the ten states with the highest total value of industry payments from 2018-2021.The high value of payments made to ophthalmologists in these ten states can likely be explained by each state's population.Seven of these ten states are in the top-ten largest states by population and a greater population necessitates a greater number of physicians [24].
All ten states had a lower number of payments made to ophthalmologists during the pandemic compared to before.Interestingly, the only four states that had a signi cant change in mean industry payment to ophthalmologists (California, Massachusetts, Pennsylvania, and Texas) showed an increase in mean payment.As mentioned above regarding overall shifts in industry payments, it is likely that this is due to industry making a smaller number of larger-value payments, which would cause the mean payment value to increase.
Our study analysis is limited by the data collected in the Open Payments database.As such, conclusions about the COVID-19 pandemic de nitively in uencing industry payment patterns are limited without adjusting for potential confounders, and our analysis is restricted to simply describing the patterns observed.Additionally, in ation was not accounted for.
Understanding trends in industry payments to physicians is vital for understanding how the relationship between physicians and industry can in uence public perception of the healthcare system and the way that physicians practice medicine.As one of the greatest disruptors of the American healthcare system in recent years, the onset of the COVID-19 pandemic may be associated with differences in industry payment patterns.This study evaluates changes in industry payments to ophthalmologists following onset of the COVID-19 pandemic.Future work in this eld should aim to address changes in industry payments to ophthalmologists during the global recovery from the pandemic, as well as evaluate underlying reasons for the signi cant differences observed.

Declarations
Tables

Table 1 .
Classi cation and Amount of Payments Received by Ophthalmologists

Table 2 .
Comparison of Payments Made by Top 10 Companies Types Pre-and Post-COVID *P values were not recorded for payment classi cations that did not have any value of payments either pre-or post-pandemic.

Table 4 .
Comparison of Payments by Top 10 States Pre-and Post-COVID