key: cord-0927497-stbryeat
authors: Ungaro, Ryan C; Chou, Bonnie; Mo, Jason; Ursos, Lyann; Twardowski, Rachel; Candela, Ninfa; Colombel, Jean-Frederic
title: Impact of COVID-19 on Healthcare Resource Utilization among Patients with Inflammatory Bowel Disease in the USA
date: 2022-04-09
journal: J Crohns Colitis
DOI: 10.1093/ecco-jcc/jjac056
sha: 91661c44a8892f4f36fe75b0b53a03ae6817530e
doc_id: 927497
cord_uid: stbryeat

BACKGROUND AND AIMS: The impact of the COVID-19 pandemic on patients with inflammatory bowel disease [IBD] is largely unknown. We characterized the impact of COVID-19 on IBD care by conducting an analysis of US healthcare claims data. METHODS: We obtained de-identified, open-source health insurance claims data, from January 2019 to December 2020, from the Symphony Health Integrated Dataverse for US adults with IBD and measured the rates, per 1000 patients, of five outcomes: colonoscopies; new biologic or small molecule treatment initiations or treatment switches; new biologic or small molecule treatment initiations or treatment switches in patients who had a colonoscopy within the previous 60 days; IBD-related surgeries; and telehealth consultations. RESULTS: For 2019 and 2020, 1.32 million and 1.29 million patients with IBD, respectively, were included in the analysis. In March–April 2020, the rates of colonoscopies [17.39 vs 34.44], new biologic or small molecule treatment initiations or switches in patients who had a colonoscopy within the previous 60 days [0.76 vs 1.18], and IBD-related surgeries [2.33 vs 2.99] per 1000 patients were significantly decreased versus January–February 2020; significant year-on-year decreases versus 2019 were also observed. Telehealth utilization increased in March 2020 and remained higher than in 2019 up to December 2020. CONCLUSIONS: Reduction in colonoscopies and subsequent initiation/switching of treatments during the COVID-19 pandemic suggest lost opportunities for therapy optimization that may have an impact on longer-term patient outcomes. Increased utilization of telehealth services may have helped address gaps in routine clinical care.

In late December 2019, Chinese health authorities reported a cluster of cases of pneumonia of unknown etiology in Wuhan, Hubei Province. 1 Confirmation that these cases were caused by a novel coronavirus, initially known as 2019 novel coronavirus [2019-nCoV] and subsequently renamed severe acute respiratory syndrome coronavirus 2 [SARS-CoV-2], 2 was provided on January 7, 2020. 1 Soon after, epidemiologic data indicated person-to-person transmission of the novel pathogen 3 and on January 20, 2020 a 35-year-old man presenting to a clinic in Snohomish County, Washington became the first confirmed case of SARS-CoV-2 infection in the USA. 3, 4 On March 11, 2020, the outbreak of coronavirus disease 2019 , the disease caused by SARS-CoV-2 infection, was declared a pandemic by the World Health Organization [WHO] . 5 According to the WHO interactive COVID-19 dashboard, there have been approximately 384 million SARS-CoV-2 infections and 5.6 million deaths globally as of February 3, 2022. 6 As the COVID-19 pandemic has progressed, it has had a dramatic impact on healthcare systems in affected countries, following a pattern observed in previous infectious disease epidemics including the SARS outbreak in Ontario, Canada in 2003 and the 2014 Ebola outbreak in West Africa. [7] [8] [9] [10] As well as direct effects caused by increasing numbers of COVID-19 patients requiring hospitalization and other medical care, behavioral interventions implemented by governments to mitigate virus transmission [e.g. lockdowns and social distancing measures], updates to clinical procedure guidelines, and changes in public behavior have produced indirect effects on non-COVID-19 related healthcare resource utilization. 11, 12 A systematic review of healthcare utilization from 81 studies across 20 countries including the USA, UK, Germany, China, and Brazil found a median reduction of 37% in overall health service use during the early phase of the pandemic which included reductions of 42% for clinical visits and 31% for diagnostic procedures 7 . In the USA in particular, significant decreases in non-COVID-19-related healthcare use, outpatient visits and visits to emergency departments were reported during the early phase of the COVID-19 pandemic. [13] [14] [15] [16] A c c e p t e d M a n u s c r i p t Manuscript Doi: 10 .1093/ecco-jcc/jjac056 6 In a study by Whaley and colleagues, a relative reduction in colonoscopy use of 69.6% between March-April 2019 and March-April 2020 was reported in the general patient population [46-64 years of age] in the USA; a year on year reduction of 92.9% when restricted to April alone. 15 However, little is known about the specific impact of the COVID- 19 In this study, we investigated the effects of the COVID-19 pandemic on the rate of colonoscopies, new biologic or small molecule treatment initiations or switches, and IBD-related surgeries in patients with IBD in the USA. We also analyzed the monthly rate of telehealth use to understand how patients adopted alternative forms of healthcare when in-person care was affected by COVID-19.

To assess changes in healthcare use during the early phase of the COVID- 19 7 different payer types including commercial healthcare plans, Medicare Part D and co-pay assistance programs. We obtained data for claims between January 2019 and December 2020.

Eligible patients were 18-80 years old and had at least one IBD diagnosis, including CD [ICD-9-CM: 555.xx; ICD-10-CM: K50.xx] or UC [ICD-9-CM: 556.xx; ICD-10-CM: K51.xx], in the 36 months prior to the month in which one of the specified outcome measures was first achieved. IDV ® does not include patient insurance enrollment data and therefore the number of active IBD patients was used as a proxy for the number of enrollees to calculate health care utilization rates. Active patients with IBD were defined by having at least one claim activity during the study period including in person or virtual clinic visits or pharmacy refills [including mail-in orders]. Patients whose geographical location, age or sex were not known were excluded from the analysis.

We assessed the effects of the COVID-19 pandemic on health care utilization by comparing monthly or bimonthly rates of specified outcome measures. Monthly rates, per 1000 patients with IBD, were calculated by dividing the number of events for each outcome per month by the total number of patients with IBD during the specified month and multiplying by 1000. For bimonthly comparisons, we calculated the rates for each two-month period [January-February, March-April, May-June, July-August, September-October, November-December] as the mean of the rates for individual months. To compare the rates of the specified outcomes during the COVID-19 pandemic with pre-pandemic time, two analyses were performed. First, we determined changes in outcome rates across 2020 by comparing the bimonthly rates during 2020 to the rate observed in January-February 2020, an appropriate baseline period immediately prior to the onset of the COVID-19 pandemic in the US. Second, to account for potential seasonal effects in health care utilization, we 3) New treatment initiations or treatment switches in patients who had a colonoscopy in the previous 60 days were defined as patients who had a new treatment initiation or treatment switch identified as previously described and who had a colonoscopy, identified using CPT codes, in the 60 days prior to treatment initiation or switch.

Measurements for this outcome were performed up to October 2020 to allow for the 60-day look-forward window until the end of our analysis period in December 2020. 

For colonoscopies, new treatment initiations or treatment switches, new treatment initiations or treatment switches in patients who had a colonoscopy in the previous 60 days, and IBD-related surgeries, we calculated rate ratios to compare rates between pandemic and pre-pandemic timeframes. The sample population event distribution was visually inspected for type of IBD diagnosis, age group, sex, and US region. The distributions showed an excess of zero counts [no event] with only a small fraction of patients having more than one event during the measured time interval. Consequently, we used zero-inflated Poisson regression to model the distribution and to calculate 95% confidence intervals [CI] and statistical significance for the rate ratios. 20, 21 We modelled the number of events as the outcome and created a binary dummy variable [COVID-19] to represent the exposure of interest, adjusting for type of IBD diagnosis [UC or CD], patient age group, sex, and region. We report the estimated adjusted rate ratio [aRR], 95% CI for the estimated aRR, and p-value. Monthly and yearly average event rates are reported as mean ± standard deviation.

To evaluate the overall net impact of the COVID-19 pandemic [up to December 2020] on healthcare resource utilization by patients with IBD, we performed an interrupted time series [ITS] analysis using segmented regression. We used the following segmented regression model:

where Y t is the healthcare utilization rate for outcome measures 1-4 at time t, T is the time elapsed in months since the first measurement [T = 0], X t is a binary variable to distinguish pre-[coded 0] and post-intervention time [coded 1], β 0 is the baseline healthcare utilization rate at time T = 0, β 1 T is the rate of change [slope] for each outcome measure that represents the underlying trend over the 24month study period that would have been expected to occur in the absence of any intervention, β 2 X t is the level change in healthcare utilization rate associated with the intervention, and β 3 TX t is the rate of change for each outcome measure in the period following the intervention. In the case of the

A c c e p t e d M a n u s c r i p t Manuscript Doi: 10.1093/ecco-jcc/jjac056

10 of scheduled hospital-based procedures] were considered as the policy change variable [X t ] for the analysis. Despite many of the policy changes being implemented at individual state level in the US, the majority were introduced during March 2020 and, therefore, this month was considered as the anchor point for the policy change across the USA.

All analyses were conducted in SAS version 9.4. PROC GENMODE with ZIP distribution was used to model zero-inflated Poisson regression. PROC AUTOREG with Newey-West standard errors 22,23 was used to account for autocorrelation and heteroskedasticity. Statistical significance was set at p < 0.05 and marginal significance was set at p < 0.10.

From January to December 2019 and January to December 2020, 1.32 million and 1.29 million adult patients with IBD, respectively, were included in the analysis. The study populations had similar characteristics in terms of age, sex, geographical location, IBD diagnosis, and use of 5aminosalicylic acid, corticosteroids, or immunomodulators in each year [ Table 1 and September-October 2020 [aRR: 1.10, 95% CI: 1.08-1.11, p < 0.0001] the rate of colonoscopies had recovered, with a modest increase observed compared with the rate in January-February 2020.

Overall, between July and December 2020, the rate of colonoscopies was comparable to that recorded in 2019, before the onset of the COVID-19 pandemic [ Figure 1A , Figure 2B ]. 12 In patients with an inadequate response, loss of response or intolerance to conventional treatments or to a first-line biologic treatment, the decision to initiate a new treatment is typically made based upon a clinical assessment of disease activity that includes endoscopic findings. 24 Therefore, to determine if pandemic related effects on colonoscopies specifically affected rates of new treatment initiations or treatment switches we measured the rates of treatment initiations or treatment switches that occurred within 60 days of a previous colonoscopy. In 2019, the mean monthly rate of new treatment initiations or treatment switches in patients with IBD who had a colonoscopy in the previous 60 days was 1.06 ± 0.09 per 1000 patients. In March-April 2020, the rate fell to 0.76 per 1000 patients with IBD [ Figure 1C ], a significant reduction versus January- Table 2 ]. However, we found that the policy interventions adopted in the US to mitigate the effects of COVID-19 (e.g., lockdown) were associated with a significant drop in the level of colonoscopies performed, with a reduction of approximately 17 colonoscopies per 1000 patients with IBD between pre-and post-pandemic time [ Table 2 ]. However, in the period following the pandemic onset (post-March 2020) the colonoscopies performed recovered at a rate of 2.308 procedures per 1000 patients with IBD per month [Table 2, Figure 1A ]. Overall, new treatment initiations and treatment switches were not affected by the pandemic; a small, but not significant, increase was observed during the pandemic versus pre-pandemic time [1.479 procedures per 1000 patients with IBD per month; Table 2 ]. For new treatment initiations or treatment switches that occurred within 60 days of a previous colonoscopy we observed a non-significant reduction between pandemic and pre-pandemic time [−0.278 per 1000 patients, Table 2 ]; the rate of change of new treatment initiations or treatment switches that occurred within 60 days of a previous colonoscopy was significantly increased during the period after the pandemic onset [0.081 per 1000 patients with IBD per month, Table 2 patients per month between July and December 2020, a level which remained markedly higher than prior to the pandemic onset [ Figure 3 ].

The COVID-19 pandemic and associated government actions to mitigate its effects on the population have had a marked impact upon healthcare systems in the USA and worldwide. 7 Using a crosssectional and time-series analysis of patient healthcare claims records, we have shown that the onset of the COVID-19 pandemic in early 2020 was associated with significant impacts on IBD care that may have long-term effects.

In patients with IBD in the USA, we found that colonoscopy procedures were significantly disrupted by the pandemic during spring 2020. Between January [35.2 per 1000 patients] and April [8.4 per 1000 patients] 2020 there was a 76.2% reduction in colonoscopies performed. During the early phase of the pandemic, although routes of SARS-CoV-2 transmission were not fully understood, it was considered highly likely that the virus could be spread via aerosolized particles, droplets and stool. Consequently, colonoscopy procedures were considered high risk for exposure to patients and clinical staff. 18, 25 Our findings suggest that during the early phase of the pandemic many planned growing COVID-19 case numbers, healthcare resources, in particular healthcare workers, were increasingly diverted away from elective procedures to inpatient care. However, after the initial shock to the healthcare system in March and April 2020, our analysis shows that the rate of colonoscopies in patients with IBD recovered relatively quickly to pre-pandemic levels; by July and August 2020 the rate was similar to that observed in January-February 2020 and throughout 2019.

The reasons for this are likely two-fold. First, as public health interventions began to take effect the level of COVID-19 in the population fell significantly relieving the overall pressure on healthcare systems imposed by the very high case numbers in the early months of the pandemic. Second, as global understanding of the SARS-CoV-2 virus and its transmission improved, bodies including national gastroenterology and endoscopy societies and the World Endoscopy Organization released updated recommendations on performing colonoscopies in a COVID-19 safe manner. 18, 25 Our new analysis reveals that the COVID-19 pandemic also had an impact upon the decision to initiate new treatments or to switch treatment in patients in the USA with IBD. We found that in March-April 2020 there was a significant drop in the rate of new treatment initiations or treatment switches in patients who had recent colonoscopies. However, the rate of new treatment initiations or treatment switches between May and October 2020 was significantly increased when compared with 2019. This suggests that IBD flares may have been undertreated during the early phase of the pandemic, but that treatment was delayed rather than missed altogether. This possibly resulted from reluctance among healthcare professionals to initiate new therapies or switch therapies during the early phase of the pandemic out of concern that it could aggravate COVID-19 outcomes.

However, with increasing knowledge of the relatively low-risk for adverse COVID-19 outcomes with biologic and small molecule treatments, in particular from the SECURE-IBD registry 26-28 , clinicians were able to approach IBD treatment with renewed confidence. IBD-related surgeries were also A c c e p t e d M a n u s c r i p t Manuscript Doi: 10.1093/ecco-jcc/jjac056 16 acutely decreased in early 2020. Reassuringly, the rate of IBD-related surgeries did not increase in the later months of 2020 suggesting that the treatments that were initially delayed by the pandemic were still sufficiently effective in averting additional surgeries.

Finally, we found that the COVID-19 pandemic was associated with a dramatic increase in telehealth utilization. Our analysis showed that in patients with IBD telehealth utilization was traditionally low, with only approximately 1.5 consultations per 1000 patients per month. However, at the peak of the pandemic in the USA during April 2020, we found a 19 335% increase in telehealth use in patients with IBD compared with April 2019. This increase is consistent with significant increases in telehealth use in the general US population at the onset of the pandemic. For example, the multisite Mayo Clinic saw a 78% reduction in in-person visits between March 11, 2020 and April 20, 2020 accompanied by a 10 880% increase in video appointments with patients at home. 29 Moreover, the International Organization for the study of IBD telemedicine survey conducted by Lees and colleagues found similar increases in telehealth use in the US as well as a range of other countries including the UK, Canada, Australia and South Africa during the onset of the pandemic. 30 Interestingly, although we observed signs that some clinical services, including colonoscopies, were returning to normal levels later in 2020, the rate of telehealth consultations remained markedly higher than during pre-pandemic time. This trend probably reflects increasing patient awareness and demand for these services but is also probably the result of continuing unavailability of in-person clinical services that were not captured by our analysis.

This study is subject to certain limitations associated with claims data use. First, the presence of a claim for a filled prescription does not indicate that the medication was consumed or taken as prescribed. Furthermore, the presence of a diagnosis code on a medical claim does not necessarily indicate a positive presence of disease, because the diagnosis code may be incorrectly coded or included as rule-out criteria rather than actual disease. Finally, certain information is not readily available in claims data that could influence study outcomes, such as clinical and disease-A c c e p t e d M a n u s c r i p t are not available. However, despite the promise of using these imaging modalities to assess transmural healing in people with Crohn's disease 31 , this is not currently recommended as a formal treat-to-target diagnostic measure by the latest STRIDE-II guidelines 32 . Therefore, we believe that unavailability of data on these measures in our dataset during the COVID-19 pandemic in 2020 does not significantly detract from our findings and that the outcome measures we selected remain the most useful for determining the effects of the pandemic on IBD care.

Another limitation of the present study is the timespan. The results presented here only capture the effects of the first wave of the COVID-19 pandemic on IBD care. Our data does not capture changes that occurred as the pandemic progressed into 2021 and beyond which may have had a significant impact on the response of healthcare services to COVID-19, most critically the introduction of effective COVID-19 vaccines. The duration of our present study also precludes a thorough assessment of any direct link between impacts on healthcare resource utilization and COVID-19 case numbers. Although the greatest impacts we report in the present study occurred during the early part of 2020 when COVID-19 case numbers in the US were high we cannot distinguish whether these impacts were due to overwhelmed healthcare systems or because of caution in response to a novel pathogen. In a future analysis, it would be of value to investigate whether the impacts we observed during the first wave of the pandemic were repeated during subsequent waves, where case numbers were high, but healthcare systems were better prepared.

A c c e p t e d M a n u s c r i p t

The data found in the IDV ® database is aggregated from multiple sources, including multiple payers, health systems, pharmacies, electronic billing relay systems [i.e., billing switches], and other sources. This allows for a unique longitudinal data source that contains individual patient-level data for patients that move between health plans, as well as capturing cash payments for select services.

The downside to this methodology is the lack of a patient eligibility or monthly enrollment file that would be commonly found in administrative claims data from a single payer. To overcome this limitation, a quarterly activity variable for each patient has been generated, which provides an indication that the patient had medical or pharmacy claims activity in each quarter.

In conclusion, IBD-related care in the USA was significantly affected during the COVID-19 pandemic which may have caused lost opportunities for therapy optimization. Longer follow-up will be needed to fully address the impact of these acute changes on disease progression. M a n u s c r i p t M a n u s c r i p t M a n u s c r i p t 

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