Impact of the Coronavirus Disease 2019 Pandemic on Gastrointestinal Procedures and Cancers in the United States: A Multicenter Research Network Study.

The coronavirus disease 2019 (COVID-19) pandemic has caused an extraordinary burden on the healthcare system and has dramatically impacted the delivery of services. Many nonurgent gastrointestinal (GI) endoscopy services and in-person clinic visits have been deferred, and patients have also avoided visiting healthcare facilities because of the risk of exposure to COVID-19. Data from the United Kingdom and Hong Kong have shown a drop in the number of patients diagnosed with various GI cancers. , However, the overall impact of the COVID-19 pandemic on common GI procedures and cancer diagnoses in the United States has not been thoroughly evaluated.

Methods

We used TriNetX (Cambridge, MA) to retrospectively analyze data from multiple healthcare organizations (HCOs) in the United States. Details of the TriNetX database are described in the Supplementary Methods and in previous studies. , We first estimated the change in the number of patients who had healthcare encounters, procedures, and diagnoses of new GI cancers at participating HCOs in the United States between March 15, 2020 and July 15, 2020 (early COVID-19 pandemic), and March 15, 2019 to July 15, 2019. The number of patients with procedures and new diagnoses of GI cancers was calculated per 100,000 patients with healthcare encounters. We further extended our analysis to study the trend later in the pandemic between July 16, 2020 and November 15, 2020, compared with the corresponding duration in 2019. Sensitivity analysis comparing the diagnosis of new GI cancers during the early COVID-19 pandemic with similar times in 2016, 2017, and 2018 was performed. Detailed methodology is provided in the Supplementary Methods.

The study was approved by Charleston Area Medical Center Institutional Review Board, (Charleston, WV). The study qualified as exempt from review. TriNetX data have also been granted a waiver from the Western Institutional Review Board because it is a federated network and only aggregated counts and statistical summaries of the deidentified information without any protected health information is received from member HCOs.

Data are available to member HCOs on the TriNetX research network platform. Data aggregated directly from the electronic health records systems of the member HCOs are provided on the TriNetX cloud-based platform. Codes for creating cohorts of patients are included in the Supplementary Methods.

Results

Between March 15, 2019 and July 15, 2019, 8,661,314 adult patients had at least 1 healthcare encounter reported from 41 HCOs. During the early COVID-19 pandemic, 6,264,995 patients had at least 1 healthcare encounter reported from 36 HCOs. Characteristics of these patients are described in the Supplementary Methods. We estimated a decline in inpatient (–42.99%), emergency department (–40.09%), and ambulatory (–22.55%) visits, whereas an increase in virtual (+4465.02%) visits per HCO was seen during the early pandemic phase (March to July 2020) compared with the same time in 2019. Similarly, a decrease in patients who underwent endoscopy (71.84%), colonoscopy (84.66%), abdominal ultrasound (35.78%), endoscopic ultrasound (73.15%), and endoscopic retrograde cholangiopancreatography (48.79%) was noticed. The new diagnoses of malignant liver and intrahepatic (34.13%), colorectal (30.91%), esophageal and gastric (26.96%), and pancreatobiliary (22.81%) cancers per 100,000 patients with healthcare encounters were also decreased during the pandemic (Figure 1 and Supplementary Table 1). The sensitivity analysis also showed a substantial decline in new diagnosis of GI cancers during the early COVID-19 pandemic compared with similar time duration in 2016, 2017, and 2018 (Supplementary Figure 1).

Figure 1

Healthcare encounters, GI procedures, and new diagnoses of GI cancers during the early phase (March 15, 2020 to July 15, 2020) and later phase (July 16, 2020 to November 15, 2020) of the COVID-19 pandemic compared with corresponding intervals in 2019.

Supplementary Table 1

Patients with Healthcare Encounters, GI Procedures, and New Diagnoses of GI Cancers During the Early Phase (March 15, 2020 to July 15, 2020) and Later Phase (July 16, 2020 to November 15, 2020) of the COVID-19 Pandemic Compared With Corresponding Intervals in 2019

	Before the Pandemic (March 15 to July 15, 2019)			During the Pandemic (March 15 to July 15, 2020)				Before the Pandemic (July 16 to November 15, 2019)			During the Pandemic (July 16 to November 15, 2020)
	Healthcare encounters
	No. of Patients	Total HCOs	Average No. of Patients/HCOs	No. of Patients	Total HCOs	Average No. of Patients/HCOs	Percentage of Change	No. of Patients	Total HCOs	Average No. of Patients/HCOs	No. of Patients	Total HCOs	Average No. of Patients/HCOs	Percentage of Change
Ambulatory visits	5,919,882	35	159,996.81	4,167,867	32	130,245.84	–22.55	6,673,161	40	166,829.03	6,042,417	39	154,933.77	–7.13
Inpatient visits	823,493	37	22,256.57	426,704	32	13,334.50	–42.99	954,633	40	23,865.83	711,368	39	18,240.21	–23.57
Emergency department visits	1,268,126	36	35,225.72	679,925	31	21,933.06	–40.92	1,426,728	39	36,582.77	1,034,873	38	27,233.50	–25.56
Virtual visits	7266	25	290.64	394,542	27	14,612.67	4465.02	10,063	28	359.39	278,852	31	8,995.23	2402.92
	Procedures (no. of patients/100,000 patients with healthcare encounters)
Upper GI endoscopy	186.38			52.48			–71.84	179.84			63.41			–64.74
Colonoscopy	299.91			46.02			–84.66	293.72			112.66			–61.64
Abdominal ultrasound	536.79			344.74			–35.78	534.12			395.52			–25.95
Endoscopic ultrasound	18.77			5.04			–73.15	18.3			4.4			–75.95
Endoscopic retrograde cholangiopancreatography	11.56			5.92			–48.79	10.29			3.93			–68.10
	New diagnoses of cancers (no. of patients/100,000 patients with healthcare encounters)
Esophageal or gastric cancer	10.57			7.72			–26.96	9.45			7.58			–19.78
Pancreas, gallbladder, and other bile duct cancer	14.38			11.1			–22.81	11.44			9.66			–15.56
Liver and intrahepatic bile duct cancer	13.8			9.09			–34.13	11.49			8.55			–25.58
Colorectal cancer	33.54			23.17			–30.91	30.16			26.62			–11.74

Supplementary Figure 1

Percentage of change in new diagnoses of GI cancers per 1,000,000 patients with healthcare encounters during the COVID-19 pandemic (between March 15, 2020 and July 15, 2020) compared with same time duration in (A) 2016, (B) 2017, (C) 2018, and (D) 2019.

Similarly, a decrease in the patient visits, procedures, and new diagnoses of cancers were also seen in the later phase of the pandemic (July to November 2020) compared with a similar period in 2019; however, the proportion of the decline was smaller compared with the early pandemic (Figure 1 and Supplementary Table 1). The decrease in new diagnoses of malignant liver and intrahepatic (25.58%), colorectal (11.74%), esophageal and gastric (19.78%), and pancreatobiliary (15.56%) cancers later in the pandemic was considerable but recovered compared with the early COVID-19 pandemic.

Discussion

Our study, including data from multiple HCOs in the United States, showed the collateral damage caused by the COVID-19 pandemic leading to potential delays in the diagnosis of major GI cancers. Patient encounters and new diagnoses of GI cancers and procedures significantly declined during the COVID-19 pandemic compared with a similar period in 2019. Our findings report trends similar to other studies that showed a reduction in all cancer-related patient encounters during the COVID-19 pandemic. , These trends may result in an increase in late-stage cancer cases and poor cancer outcomes; moreover, the cancellation of cancer-preventive GI procedures can lead to a rise in the incidence of GI cancers in the future. An increase in virtual visits was seen; however, the volume of these virtual visits was not large enough to account for the decrease in volume of ambulatory visits, and the nature of virtual visits could not replace procedures or imaging needed for cancer diagnosis.

Decreases in GI procedures is a significant disruption of practice patterns and source of revenue for gastroenterologists. Going forward, when GI endoscopy and routine healthcare services are resumed in full capacity, there will be a significant burden and demand for procedures related to cancer screening. An increase in capacity of GI procedures will be needed, and gastroenterologists will also have to carefully triage patient panels to evaluate and schedule persons at risk for malignancy sooner. Similarly, gastroenterologists will need to use all available evidence-based required tools for cancer screening. For instance, in patients needing colon cancer screening, using noninvasive screening methods such as the fecal immunochemical test, fecal-fecal immunochemical test DNA, and computed tomography colonography in addition to colonoscopy will be needed. Other experts have also suggested considering weekend and evening endoscopy sessions to meet the backlog of GI endoscopy created during the pandemic. However, this will need to be balanced by the burden on the already strained healthcare system and physician burnout. These factors will become especially crucial in a prolonged COVID-19 pandemic. This will further extend these reported trends and delay in new cancer diagnosis.

Our study has several limitations. Data derived from administrative coding systems have the inherent limitations of miscoding or data entry errors. Our study estimated procedures and diagnoses only among the patients with healthcare encounters and did not account for the patient population without healthcare encounters. Differences in cancer staging, histology, treatment modalities, and mortality were not determined. Despite these limitations, our study is the largest study to show a reduction in diagnoses of major GI cancers during the pandemic. This highlights the serious future implications that can result in an increased restraint on healthcare resources and lead to increased morbidity and mortality. Urgent policy and practice interventions will be needed, and HCOs and gastroenterologists will need to use innovative methods to meet the backlog of screening and diagnostic tests for GI cancers.

Codes to identify patient encounters, procedures, and GI cancers
Visits
Emergency department	CPT codes: 99281, 99282, 99283, 99284, 99285
	HCPS codes: G0382, G0381, G0383, G0380
Ambulatory	TNX Visit: Ambulatory
	CPT codes: 99211, 99212, 99213, 99214, 99215, 99201, 99202, 99203, 99204, 99205, 99024, 99495, 99496
	HCPS codes: G0463, G0438, G0439, T1015, G0466, G0467, G0468, G9050, G9051, G9052, G9054, G9055
Virtual	TNX Visit: Virtual
	CPT codes: 99441, 99442, 99443, 99444, 1018510, 98966, 98967, 98968, 99446, 99447, 99448, 99449, 99451, 99452, 1035156,1018515
	HCPS codes: G0406, G0407, G0408, G0509, G0425, G0426, G0427, Q3014
Inpatient	TNX Inpatient Encounter, Short Stay, Inpatient Acute, Inpatient Non-Acute, Observation Encounter
	CPT codes: 99251, 99252, 99253, 99254, 99255, 1013659, 1013660, 1013661, 1013699, 1013700, 99217, 1013675, 99231, 99232, 99233, 99234, 99235, 99236, 1013800, 99356, 99221, 99222, 99223, 1019140, 1013729, 1014309, 99291, 99292
	HCPS codes: Q5005, G0408, G0406, G0407
Procedures
Colonoscopy	CPT codes: 1022231, 45380, 45378, 45385, 45380, 45384, 45390, 45381, 45388, 45386, 44389, 44394, 1007534, 44388, 45391, 44392,
	HCPCS codes: G0105, G0121, 45393, G0120, G9935, G9936, G9933, G9937
	ICD-10 code: 0DJD8ZZ
Upper endoscopy	CPT codes: 1021431, 1007260, 43239, 43235, 43249, 43259, 1021430, 43248, 1007242, 43242, 43237, 43200, 43251, 43238, 43245, 43253, 43226, 43233, 43252, 43229, 43205, 43197, 43212, 43213, 43217, 43206
	ICD 10 codes: 0DJ08ZZ, 0DB68ZX, 0DB98ZX, 0DB58ZX, 0D968ZX, 0D958ZX, 0D998ZX
Abdominal ultrasound	CPT codes: 76705, 1010775, 76700
	ICD-10 codes: BD47ZZZ, BF4CZZZ, BF40ZZZ, BF43ZZZ, BF45ZZZ, BF46ZZZ, BF45, BF46
Endoscopic ultrasound	CPT codes: 43231, 43232, 43237, 43238, 43242, 43253, 43259, 44406, 44407, 45341, 45342, 45391, 45392
Endoscopic retrograde cholangiopancreatography	CPT codes: 1007283, 1021432, 43260, 43261, 43262, 43263, 43264, 43265, 43274, 43275, 43276, 43277, 43278
	ICD-10 codes: BF110ZZ, BF111ZZ, BF11YZZ
Diagnoses
GI cancers	Malignant neoplasm of esophagus (C15), Malignant neoplasm of stomach (C16), Malignant neoplasm of pancreas (C25), Malignant neoplasm of gallbladder (C23), Malignant neoplasm of other and unspecific parts of the biliary tract (C24), Malignant neoplasm of liver and intrahepatic parts of the biliary tract (C22), Malignant neoplasm of colon (C18), Malignant neoplasm of rectosigmoid (C19), Malignant neoplasm of rectum (C20) (colorectal cancer).