Key Messages
  • What is already known?

The COVID-19 pandemic caused a worldwide disruption in healthcare utilization, including inflammatory bowel disease (IBD) care.

  • What is new here?

We observed a mitigation of the initial reduction of IBD-related procedures after the first COVID-19 wave, illustrating the rapid adaptation of the national IBD healthcare system during the second year of the pandemic

  • How can this study help patient care?

Our study implies that strategies that were taken, such as telemedicine and improved patient triage, were adequate in mitigating the reduction in IBD-related procedures but also poses questions on how these strategies can be used in the future.

Introduction

The COVID-19 pandemic has profoundly impacted gastroenterology healthcare, with a considerable reduction in scheduled healthcare in the early phase of the pandemic.1-3 Inflammatory bowel disease (IBD) healthcare depends on frequent outpatient monitoring, including regular endoscopic follow-up and surgical procedures in case of IBD complications.4 In a previous study, we showed a net reduction of colonic dysplasia diagnoses and endoscopic procedures after the first COVID-19 peak in 2020 as a result of insufficient healthcare recovery.1

As COVID-19 continued to disrupt IBD healthcare utilization and distribution during subsequent peaks, measures were taken, including telemedicine and improved triage of procedures.4,5 However, it is unknown if these adaptations restored IBD healthcare utilization as measured by the volume of IBD procedures and diagnoses. This is especially relevant for IBD patients with delayed or missed indefinite for dysplasia (IND) and low-grade dysplasia (LGD) diagnoses because these lesions may progress to advanced neoplasia with subsequent morbidity and mortality. In addition, continued delay of endoscopic and surgical procedures might have resulted in suboptimal disease assessment and treatment.

In this nationwide study, we aimed to determine the impact of consecutive COVID-19 waves on healthcare utilization deficits, including IBD-related diagnoses and procedures during the first 2 years of the COVID-19 pandemic. We also assessed whether IBD healthcare utilization recovered in the second year of the pandemic.

Methods

Data Source

For this nationwide retrospective cohort study, we searched the Dutch nationwide pathology databank (PALGA)6 to identify IBD patients who underwent an IBD-related procedure between March 1, 2018, and February 28, 2022. The PALGA registry contains pseudonymized data with unique identifiers linked to individual patients and has had nationwide coverage since 1991.6 We repeated the PALGA search from our previously published study,1 using the same terms for IBD: “ulcerative colitis,” “Crohn’s disease,” and “chronic inflammatory bowel disease.” In addition, pathologists’ report conclusions were searched using similar terms. Data on the number of COVID-19 hospital admissions were extracted from the Dutch Patient Coordination Center.7

Definitions

The procedure type (endoscopic vs surgical) was based on pathology results from either intestinal biopsy or resection specimens. IBD diagnosis was considered new in the absence of a historical pathology report. Because the first COVID-19 case in the Netherlands started on February 27, 2020, the prepandemic period was defined as March 2018 to February 2020, and the pandemic period was defined as March 2020 to February 2022.

Eligibility Criteria

All patients with a new or existing IBD diagnosis (eg, ulcerative colitis, Crohn’s disease, and IBD unclassified) were eligible for inclusion. Patients with a missing PALGA IBD diagnosis and the absence of IBD diagnosis in pathologists’ reports were excluded from our study.

Data Collection

Variables extracted from PALGA included procedure date, type, neoplasia grade (IND, LGD, high-grade dysplasia [HGD], or colorectal cancer [CRC]), and new IBD diagnosis. We screened all individual histology records to exclude any false positive IBD-related diagnoses.

Statistical Analysis

We determined the absolute incidence of IBD-related endoscopic and surgical procedures and neoplasia diagnoses (IND, LGD, HGD, and CRC) during the first and second years of the COVID-19 pandemic in the Netherlands (March 2020 to February 2021 and March 2021 to February 2022). The mean incidence of the previous 2 years (March 2018 to February 2020) served as a comparator. We used SPSS version 25 (IBM Corporation) to assess incidence rates. Confidence intervals and P values were not displayed. By using complete nationwide data, we avoided sampling error when interpreting our results for the Netherlands. With regard to other countries affected by COVID-19, sampling error is likely to be small compared with major incidence influencing factors like differences in confinement measures and healthcare policies.

Ethical Considerations

This study was approved by the scientific committee of PALGA (lzv-2020-123a).

Results

Our PALGA search yielded a total of 103 322 IBD-related procedures. After applying exclusion criteria, we included 89 401 (94.2%) endoscopic and 5462 (5.8%) surgical procedures.

IBD-Related Procedures

We calculated a net reduction of 2.9% (1391 IBD procedures) after the first 2 years of the COVID-19 pandemic compared with the 2 prepandemic years. This net reduction consists of a decrease in endoscopic procedures (−3.1% [n = 1409]) (Figure 1), while a small increase in surgical procedures was observed (+0.7% [n = 18]) (Figure 1). We found the highest net reduction during the first peak of the pandemic in April 2020 (−59.1% [n = 1166]), compared with the mean incidence of April 2018 and April 2019. For both endoscopic and surgical procedures, an initial net decrease after the first pandemic year was followed by a net increase after the second year (−6.2% [n = 1413] vs +0.02% [n = 4] and −1.3% [n = 18] vs +2.7% [n = 36], respectively).

Total (A) inflammatory bowel disease (IBD)–related endoscopic procedures, (B) surgical procedures, (C) indefinite for dysplasia (IND) and low-grade dysplasia (LGD) diagnoses, (D) and new IBD diagnoses. The gray bars represent the mean number of hospital beds occupied by COVID-19 patients in the Netherlands per month.7
Figure 1.

Total (A) inflammatory bowel disease (IBD)–related endoscopic procedures, (B) surgical procedures, (C) indefinite for dysplasia (IND) and low-grade dysplasia (LGD) diagnoses, (D) and new IBD diagnoses. The gray bars represent the mean number of hospital beds occupied by COVID-19 patients in the Netherlands per month.7

New IBD Diagnoses

A net reduction of 0.9% (n = 54) in new IBD diagnoses was observed after the first 2 years of the COVID-19 pandemic, with a net decrease of 0.8% (n = 24) and 1.0% (n = 30) after the first and second pandemic years, respectively.

IBD-Related Neoplasia

A net reduction of 1.9% (n = 74) in IND/LGD diagnoses was observed after the 2-year pandemic period. We observed a net decrease of 10.9% (n = 213) in IND/LGD diagnoses in the first pandemic year vs an increase of 7.1% (n = 139) in the second year. No net decrease was seen for HGD and CRC diagnoses.

Discussion

In this nationwide cohort study, we found a net reduction in IBD-related procedures of approximately 3% after the first 2 years of the COVID-19 pandemic, including a net reduction in endoscopic procedures, new IBD diagnoses, and IND/LGD diagnoses. However, no decrease in surgical procedures and HGD/CRC diagnoses was found. Importantly, we observed that IBD healthcare utilization was restored to prepandemic volumes in the second pandemic year.

The net decrease of 2.9% in IBD procedures after the 2-year pandemic period is most likely the result of delayed or cancelled endoscopic procedures, with even a small increase in surgical procedures (0.7%). This modest increase may result from delayed (but inevitable) surgical procedures and suboptimal treatment of inflammation or neoplasia, leading to more frequent surgical interventions.

Nearly 6 out of 10 IBD-related procedures were canceled or postponed during the first peak of COVID-19 in 2020.1 Our present update shows that during the subsequent COVID-19 peaks, the decline in IBD-related procedures and diagnoses was mitigated. This could be the result of more effective healthcare utilization and higher prioritization of necessary IBD healthcare.8 In addition, improved patient education and COVID-19 vaccination strategies might have resulted in less delayed care-seeking behavior.4,9 In line with a Dutch study showing gastroenterology procedure volumes returned to reference levels during the second wave, this trend suggests that our healthcare system is fast adapting to overcome COVID-19 hurdles.10

In contrast, we found a decrease in new IBD diagnoses for both pandemic years. Because the decrease was very small for both years (≤1%), one could hypothesize that this is a reflection of natural fluctuation in new IBD diagnoses over the years or, alternatively, that changed lifestyle factors due to the pandemic impacted this reduction.

We found a decrease in IND and LGD diagnoses during the first pandemic year, with a subsequent increase in the second year. By contrast, this was not observed for HGD and CRC diagnoses. One could hypothesize that high-risk or symptomatic patients suspected of HGD or CRC receive a higher prioritization, which corroborates with previous studies that show that the initial decrease was smallest in urgent interventions.1,3,10

Our study has several strengths. To our best knowledge, this is the first study to assess the impact of the COVID-19 pandemic during 2 consecutive years on IBD-related endoscopic and surgical procedures and new IBD and neoplasia diagnoses in the Netherlands. This allowed us to detect changes in procedures and IBD-related disease outcomes during the first pandemic peak and the second year of the pandemic. By using a nationwide pathology database, we were able to analyze a large cohort covering the first 2 years of the COVID-19 pandemic compared with incidences from the 2 prepandemic years. Limitations of our study include unavailable data on type of endoscopy (surveillance or nonsurveillance) and mortality. In addition, we could not include procedures without tissue sampling because these are not available in the pathology database.

Conclusions

In this nationwide cohort study covering the first 2 years of the COVID-19 pandemic, we observed mitigation of the initial reduction of IBD-related procedures after the first COVID-19 wave. This finding illustrates the rapid adaptation of the national IBD healthcare system during the second year of the pandemic.

Abbreviations

    Abbreviations
     
  • COVID-19

    Coronavirus disease 2019

  •  
  • CRC

    Colorectal cancer

  •  
  • HGD

    High-grade dysplasia

  •  
  • IBD

    Inflammatory bowel disease

  •  
  • IND

    Indefinite for dysplasia

  •  
  • LCPS

    The Dutch Patient Coordination Center

  •  
  • LGD

    Low-grade dysplasia

  •  
  • PALGA

    The Dutch nationwide pathology databank

  •  
  • SPSS

    Statistical Package for the Social Sciences

Funding

No funding was obtained for this work.

Conflicts of Interest

The authors state no conflicts of interest.

Data Availability

Study materials will be shared upon reasonable request, after consultation and agreement of the authors.

References

1.

te Groen
M
,
Derks
MEW
,
Kuijpers
CCHJ
,
Nagtegaal
ID
,
Hoentjen
F.
Reduction in inflammatory bowel disease healthcare during the coronavirus disease 2019 pandemic: a Nationwide Retrospective Cohort Study
.
Gastroenterology.
2021
;
160
(
3
):
935
-
937.e1
.

2.

Rutter
MD
,
Brookes
M
,
Lee
TJ
,
Rogers
P
,
Sharp
L.
Impact of the COVID-19 pandemic on UK endoscopic activity and cancer detection: a National Endoscopy Database Analysis
.
Gut.
2021
;
70
(
3
):
537
-
543
.

3.

Theunissen
F
,
Lantinga
MA
,
ter Borg
PCJ
,
Bruno
MJ
,
Ouwendijk
RJT
,
Siersema
PD.
Impact of the COVID-19 pandemic on gastrointestinal endoscopy in the Netherlands: analysis of a prospective endoscopy database
.
Endoscopy.
2020
;
53
(
2
):
166
-
170
.

4.

Ungaro
RC
,
Chou
B
,
Mo
J
, et al.
Impact of COVID-19 on healthcare resource utilisation among patients with inflammatory bowel disease in the USA
.
J Crohns Colitis
.
2022
;
16
(
9
):
1405
-
1414
.

5.

Lees
CW
,
Regueiro
M
,
Mahadevan
U
;
International Organization for the Study of Inflammatory Bowel Disease
.
Innovation in inflammatory bowel disease care during the COVID-19 pandemic: results of a global telemedicine survey by the International Organization for the Study of Inflammatory Bowel Disease
.
Gastroenterology.
2020
;
159
(
3
):
805
-
808.e1
.

6.

Casparie
M
,
Tiebosch
AT
,
Burger
G
, et al.
Pathology databanking and biobanking in the Netherlands, a central role for PALGA, the nationwide histopathology and cytopathology data network and archive
.
Cell Oncol.
2007
;
29
(
1
):
19
-
24
.

7.

Landelijk Coördinatiecentrum Patiënten Spreiding (LCPS). Covid-19-datafeed
.
2022
. Accessed October 31, 2022. https://lcps.nu/wp-content/uploads/covid-19-datafeed.csv

8.

Kennedy
NA
,
Jones
GR
,
Lamb
CA
, et al.
British Society of Gastroenterology guidance for management of inflammatory bowel disease during the COVID-19 pandemic
.
Gut.
2020
;
69
(
6
):
984
-
990
.

9.

Allocca
M
,
Fiorino
G
,
Furfaro
F
, et al.
Maintaining the quality standards of care for inflammatory bowel disease patients during the COVID-19 pandemic
.
Clin Gastroenterol Hepatol.
2020
;
18
(
8
):
1882
-
1883
.

10.

Sonneveld
MJ
,
Hardeman
S
,
Kuipers
EJ
,
de Graaf
W
,
Spaander
MCW
,
van der Meer
AJ.
Effect of the COVID-19 pandemic on procedure volumes in gastroenterology in the Netherlands
.
Lancet Gastroenterol Hepatol
.
2022
;
7
(
7
):
595
-
598
.

Author notes

Monica E. W. Derks and Lisa M. A. van Lierop Shared first authorship.

This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected]