Pandemic-Related Disruptions and Hepatocellular Carcinoma Surveillance in Safety-Net Settings

Key Points

Question

Were the COVID-19 pandemic disruptions associated with declines in hepatocellular carcinoma (HCC) surveillance among patients with cirrhosis?

Findings

In this cohort study of 6940 patients with cirrhosis across 5 US safety-net health systems, 30.8% underwent guideline-recommended HCC surveillance within 6 months after diagnosis from March 1, 2018, to February 29, 2020. Following onset of the COVID-19 pandemic (March 1, 2020, to February 28, 2022), HCC surveillance declined to 21.1% and did not rebound, remaining at 22.3% from March 1, 2022, to February 29, 2024.

Meaning

These findings suggest that among US safety-net populations with cirrhosis, pandemic-related declines in HCC surveillance remained even up to 4 years after the onset of the COVID-19 pandemic, with fewer than 1 in 4 patients undergoing guideline-concordant HCC surveillance.

This cohort study examines contemporary data on hepatocellular carcinoma (HCC) surveillance utilization from before the COVID-19 pandemic to 4 years after onset of the pandemic among safety-net populations with cirrhosis.

Abstract

Importance

Pandemic-related disruptions in cirrhosis care resulted in major gaps and delays in surveillance for hepatocellular carcinoma (HCC). Whether these initial declines improved and rebounded to prepandemic levels remains unclear.

Objective

To evaluate contemporary clinical practice data on HCC surveillance utilization from before the COVID-19 pandemic to 4 years after the onset of the pandemic among safety-net populations with cirrhosis.

Design, Setting, and Participants

This retrospective cohort study was conducted at 5 safety-net health systems in the US. Adults with cirrhosis were evaluated longitudinally across 3 time periods: March 1, 2018, to February 29, 2020 (pre–COVID-19 period), March 1, 2020, to February 28, 2022 (COVID-19 era), and March 1, 2022, to February 29, 2024 (post–COVID-19 period).

Main Outcomes and Measures

The primary outcome was undergoing HCC surveillance identified using Current Procedural Terminology codes for ultrasonography, computed tomography, and magnetic resonance imaging, and corresponding International Statistical Classification of Diseases, Tenth Revision, Clinical Modification diagnosis codes for indication. Comparisons of HCC surveillance across time periods used paired t tests, and comparisons of HCC surveillance between subgroups within the same time period used χ² tests.

Results

Among 6940 patients with cirrhosis, 4001 (57.7%) were men (median [IQR] age, 58 [52-64] years), 206 (3.0%) were Asian, 1720 (24.8%) were Hispanic, 1672 (24.1%) were non-Hispanic Black or African American, and 3081 (44.4%) were non-Hispanic White. The proportion who underwent HCC surveillance within 6 months after diagnosis was 30.8% (1940 patients) in the pre–COVID-19 era, which declined to 21.1% (1468 patients) in the COVID-19 era, and remained at 22.3% (1405 patients) in the post–COVID-19 era. Consistent trends were observed among men and women and among all age and race groups, except for Asian individuals, for whom there was an observed increase in the post–COVID-19 era. Similar trends of low HCC surveillance post–COVID-19 were observed across insurance types but was particularly concerning among uninsured or indigent care covered patients, among whom only 116 of 997 (11.9%) underwent surveillance in the most recent period.

Conclusions and Relevance

In this observational study of US safety-net populations with cirrhosis, rates of HCC surveillance following pandemic-related declines remained persistently low even up to 4 years after the onset of the COVID-19 pandemic, with fewer than 1 in 4 patients having undergone guideline-concordant HCC surveillance.

Introduction

Hepatocellular carcinoma (HCC) remains a leading cause of cancer-related morbidity and mortality.^1,2,3 Routine HCC surveillance among patients with cirrhosis is recommended at 6-month intervals, which is associated with earlier tumor stage at diagnosis and improved patient outcomes.^4,5 Delays in HCC diagnosis lead to advanced tumor stage at diagnosis, contributing to worse outcomes.^5,6,7,8 Existing studies^{5,9,10,11,12,13} have continued to demonstrate suboptimal HCC surveillance in patients with cirrhosis. For example, a meta-analysis¹¹ inclusive of 29 studies and a total of 118 799 patients with cirrhosis observed a pooled estimate of 24.0% for HCC surveillance utilization.

Safety-net populations have a high burden of chronic liver disease in the US,^{14,15,16,17,18,19,20} and these populations experience multifactorial barriers to timely cirrhosis care.^{21,22,23,24,25,26} Prior studies^{12,13,27,28,29,30,31} in safety-net populations report low HCC surveillance among patients with cirrhosis.

The onset of the COVID-19 pandemic was associated with major disruptions in the traditional delivery of health care. Cirrhosis care—in particular, HCC surveillance—was severely disrupted because of limitations of in-person visits during the early pandemic period.^{32,33,34,35,36,37} For example, Kim et al³² evaluated HCC surveillance rates among veterans with cirrhosis in the 6 months before and after the onset of the COVID-19 pandemic and observed a 44% decline, from 39% (September 1, 2019, to February 29, 2020) to 22% (April 1, 2020, to September 30, 2020).

In 2023, the World Health Organization and the US Department of Health and Human Services declared an end to the Public Health Emergency designation of the COVID-19 pandemic. Although health care visits have largely returned to normal, it remains unclear whether the initial decline in HCC surveillance observed during the early onset of the pandemic has returned to prepandemic levels. The current study focuses on understanding whether HCC surveillance has rebounded from the initial COVID-19–related disruptions in care among safety-net health populations given that these vulnerable populations were especially affected during the pandemic.

Methods

This cohort study was approved by the institutional review boards of each respective institution and health system with a waiver of informed consent. We followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guidelines for cohort studies.

Adults with cirrhosis who were receiving routine care (eg, at least 1 health care encounter annually) at 1 of 5 safety-net health systems in California, Florida, Louisiana, Ohio, and Texas were identified from March 1, 2017, to February 28, 2019, and followed up longitudinally through February 29, 2024. The sites included San Francisco Community Health Network and Zuckerberg San Francisco General Hospital, Ochsner Health System, Parkland Health and Hospital System, Jackson Memorial Health System, and MetroHealth System. The diagnosis of cirrhosis was based on established definitions used in electronic health record–based studies: 1 or more cirrhosis or cirrhosis-related complications International Statistical Classification of Diseases, Tenth Revision, Clinical Modification (ICD-10-CM) codes on 2 separate clinical encounters.^13,38,39,40 Patients with history of HCC (based on ICD-10-CM codes) at the time of cirrhosis identification were excluded. Undergoing HCC surveillance was evaluated using Current Procedural Terminology codes corresponding to abdominal imaging with ultrasonography, computed tomography, or magnetic resonance imaging scans, as well as the corresponding ICD-10-CM diagnosis codes associated with each imaging examination. Although abdominal ultrasonography is the guideline-recommended HCC surveillance modality, in actual clinical practice, there may be variations such that practitioners may order other imaging tests (eg, computed tomography or magnetic resonance imaging of the abdomen) for HCC surveillance, which would provide similar clinical benefit.⁴¹ This was our rationale for including the aforementioned imaging modalities when accompanied by appropriate ICD-10-CM diagnosis codes that were consistent with HCC surveillance examinations (eTable in Supplement 1).

Patients in our cohort received a diagnosis of cirrhosis between March 1, 2017, to February 28, 2019, and had continuous follow-up through February 29, 2024. The primary outcome was the proportion of patients who underwent HCC surveillance within 6 months following cirrhosis diagnosis during the pre–COVID-19 period (March 1, 2018, to February 29, 2020), within the first 6 months immediately following onset of the COVID-19 pandemic (March 1, 2020, to February 28, 2022), and within the first 6 months in the subsequent period from March 1, 2022, to February 29, 2024. We performed a sensitivity analysis evaluating the proportion of patients who underwent HCC surveillance within 12 months of study entry and within the aforementioned time periods (ie, annual surveillance).

Baseline characteristics were evaluated during the 12 months before date of cirrhosis identification. Clinical characteristics including risk factors and comorbidities were identified using ICD-10-CM codes and laboratory data. Race and ethnicity were self-reported and included Asian, Hispanic, non-Hispanic Black or African American, non-Hispanic White, or other (which includes American Indian or Alaska Native, multiple races or ethnicities, or unknown). Data on race and ethnicity are included in this study because we wanted to understand and describe differences in receipt of HCC surveillance among different racial and ethnic groups.

Statistical Analysis

Descriptive statistics of the cirrhosis cohort were presented as frequencies and proportions for categorical variables and median and IQR or mean and SD for continuous variables. The proportion of patients who underwent HCC surveillance was stratified by demographics and clinically relevant characteristics. Comparisons of HCC surveillance across time periods used paired t tests. Comparisons of HCC surveillance between subgroups within the same time period used χ² tests. Statistical significance was met with a 2-tailed P < .05. Patients who died or were lost to follow-up were excluded from each subsequent analytic time period. Adjusted multivariable logistic regression models were used to evaluate for factors associated with successful HCC surveillance within 6 months or 12 months of cirrhosis diagnosis during March 1, 2022, to February 29, 2024. Variables that had a P < .10 in the univariable model were selected for inclusion in the multivariable model. Statistical analyses were performed using SAS Studio version 3.6 on SAS version 9.4 (SAS Institute). Statistical significance was met with a 2-tailed P < .05.

Results

A total of 6940 patients with cirrhosis were identified (median [IQR] age, 58 [52-64] years), among whom 4001 (57.7%) were men, 206 (3.0%) were Asian, 1720 (24.8%) were Hispanic, 1672 (24.1%) were non-Hispanic Black or African American, and 3081 (44.4%) were non-Hispanic White, and 261 (3.0%) were other races and ethnicities (Table 1). The characteristics of the cohort, including insurance status, cause of liver disease, and other comorbidities, are presented in Table 1. The cumulative incidence of HCC was 2.63 per 100 persons from March 1, 2018, to February 29, 2020, 2.05 per 100 persons from March 1, 2020, to February 28, 2022, and 2.41 per 100 persons from March 1, 2022, to February 29, 2024.

Table 1. Baseline Characteristics of the Study Cohort.

Characteristic	Patients, No. (%) (N = 6940 [100.0%])
Follow-up time, mo
Mean (SD)	75.1 (10.4)
Median (IQR)	78.8 (67.9-83.5)
Sex
Male	4001 (57.7)
Female	2939 (42.3)
Age, y
Mean (SD)	57.7 (10.9)
Median (IQR)	58 (52-64)
Race and ethnicity
Asian	206 (3.0)
Hispanic	1720 (24.8)
Non-Hispanic Black or African American	1672 (24.1)
Non-Hispanic White	3081 (44.4)
Unknown or othera	261 (3.8)
Primary language
English	5231 (75.4)
Other languages	1626 (23.4)
Primary insurance
Medicare	2141 (30.9)
Medicaid	1603 (23.1)
Commercial	1455 (21.0)
Other	650 (9.4)
None or indigent care	1091 (15.7)
Risk factors and comorbidities
Alcohol use	2331 (33.6)
Drug use	1001 (14.4)
HIV	946 (13.6)
Cardiovascular disease	5893 (84.9)
Hypertension	4860 (70.0)
Diabetes	2700 (38.9)
End-stage kidney disease	246 (3.5)
Mental health or psychiatric diagnoses	4469 (64.4)
Non–hepatocellular carcinoma cancer	2036 (29.3)
Causes of liver disease
Hepatitis B	438 (6.3)
Hepatitis C	2850 (41.1)
Metabolic dysfunction-associated steatotic liver disease	1190 (17.1)
Alcohol-related liver disease	2132 (30.7)
Cirrhosis complications
Ascites	2049 (29.5)
Hepatic encephalopathy	435 (6.3)
Variceal bleeding	347 (5.0)
Hepatorenal syndrome	88 (1.3)
≥1 Cirrhosis-related complication	2325 (33.5)
Model for End-Stage Liver Disease–Sodium score
Mean (SD)	15.1 (3.2)
Median (IQR)	14.8 (12.6-17.0)

^a Other race and ethnicity includes American Indian or Alaska Native, multiple races or ethnicities, or unknown.

Surveillance Within 6 Months

The proportion of patients with cirrhosis who underwent HCC surveillance within 6 months after diagnosis was 30.8% (1940 patients) from March 1, 2018, to February 29, 2020, which declined to 21.1% (1468 patients) from March 1, 2020, to February 28, 2022, and remained at a similar level of 22.3% (1405 patients) from March 1, 2022, to February 29, 2024 (Figure 1). Similar trends were observed among subgroups. For example, across the aforementioned 3 time periods and among both men and women, HCC surveillance within 6 months declined from March 1, 2018, to February 29, 2020, to March 1, 2020, to February 28, 2022, and remained low during March 1, 2022, to February 29, 2024 (Figure 2). When evaluated by age groups, patients aged 60 to 69 years had the highest HCC surveillance receipt, but across all age groups, HCC surveillance declined during the early years of the COVID-19 pandemic and did not rebound to prepandemic levels in the post–COVID-19 era (Figure 2). When stratified by race and ethnicity, HCC surveillance among non-Hispanic White, Black or African American, and Hispanic individuals demonstrated similar trends of declining HCC surveillance after the pandemic onset, which has not rebounded to prepandemic levels in the post–COVID-19 era. However, HCC surveillance among Asian patients initially declined between March 1, 2018, to February 29, 2020, and March 1, 2020, to February 28, 2022, but rebounded in the post–COVID-19 period. In the prepandemic period, HCC surveillance was significantly higher among English-speaking patients vs those speaking other languages (1729 of 5231 patients [33.1%] vs 185 of 978 patients [18.9%]). After onset of the pandemic, HCC surveillance among English-speaking patients declined, whereas HCC surveillance among patients speaking other languages remained stably low, and in the post–COVID-19 era, HCC surveillance among both English-speaking patients and those speaking other languages were both low and did not significantly differ. Across all time periods, HCC surveillance was highest among patients with commercial insurance. Except for other insurance, patients experienced a decline in HCC surveillance following onset of the pandemic, which did not rebound to prepandemic levels. In fact, among patients who were uninsured or covered by indigent care, HCC surveillance declined from 241 of 1058 patients (22.8%) in the pre–COVID-19 era to 157 of 1091 patients (14.4%) during COVID-19, and further declined to 116 of 977 patients (11.9%) in the post–COVID-19 era (Figure 2). On multivariable regression analysis evaluating factors associated with undergoing HCC surveillance within 6 months after diagnosis in the post–COVID-19 period, no significant differences were observed by sex, age, or race and ethnicity (Table 2). Compared with commercially insured patients, Medicare-insured patients had a lower odds ratio (OR) of HCC surveillance within 6 months (OR, 0.82; 95% CI, 0.68-1.00; P = .06), but the difference was not statistically significant. Significantly lower odds of HCC surveillance were observed among patients with comorbid mental health or psychiatric conditions (OR, 0.73; 95% CI, 0.61-0.87), whereas greater odds of surveillance were observed among patients with cirrhosis-related complications (OR, 1.31; 95% CI, 1.09-1.56) (Table 2).

Figure 1. Bar Graph of Proportion of Patients With Cirrhosis Undergoing Hepatocellular Carcinoma Surveillance Within 6 and 12 Months After Diagnosis Before, During, and After the COVID-19 Pandemic.

Error bars represent the upper limit of 95% CIs.

Figure 2. Bar Graphs of Proportions of Patients With Cirrhosis Undergoing Hepatocellular Carcinoma Surveillance Within 6 Months of Diagnosis Across 3 Time Periods, by Demographic Group.

Error bars represent the upper limit of 95% CIs.

Table 2. Factors Associated With Undergoing HCC Surveillance Within 6 Months of Cirrhosis Diagnosis in the Post–COVID-19 Era, March 1, 2022, to February 29, 2024.

Variable	OR (95% CI)a	P value
Sex
Male	1 [Reference]	NA
Female	1.14 (0.97-1.34)	.10
Age, y
<40	1 [Reference]	NA
40-49	1.00 (0.66-1.53)	.99
50-59	1.23 (0.85-1.76)	.27
60-69	1.27 (0.88-1.83)	.21
≥70	1.14 (0.74-1.74)	.55
Race and ethnicity
Asian	1.51 (0.70-3.27)	.29
Hispanic	1.11 (0.75-1.65)	.60
Non-Hispanic Black or African American	0.88 (0.73-1.07)	.19
Non-Hispanic White	1 [Reference]	NA
Unknown or otherb	1.02 (0.57-1.83)	.94
Language
English	1 [Reference]	NA
Other languages	1.29 (0.73-2.28)	.38
Insurance status
Commercial	1 [Reference]	NA
Medicare	0.82 (0.68-1.00)	.06
Medicaid	0.83 (0.67-1.04)	.11
Other	0.45 (0.21-0.99)	.05
None or indigent care	0.64 (0.36-1.14)	.13
Risk factors and comorbidities
Alcohol use	1.32 (1.09-1.60)	.004
Drug use	0.94 (0.73-1.21)	.64
HIV coinfection	1.20 (0.94-1.53)	.14
Cardiovascular disease	1.15 (0.84-1.57)	.38
Hypertension	0.95 (0.76-1.19)	.65
Diabetes	1.02 (0.86-1.20)	.82
Mental health or psychiatric diagnosis	0.73 (0.61-0.87)	<.001
Non-HCC cancer	1.15 (0.98-1.35)	.10
Cirrhosis complication	1.31 (1.09-1.56)	.003
Model for End-Stage Liver Disease–Sodium score	0.97 (0.95-0.99)	.003
>1 Gastroenterology or hepatology clinic visit	1.09 (0.92-1.21)	.12

Abbreviations: HCC, hepatocellular carcinoma; NA, not applicable; OR, odds ratio.

^a Model adjusted for site, sex, age, race and ethnicity, primary language, insurance status, cause of liver disease, cirrhosis complications, risk factors and comorbidities, and whether patient had at least 1 gastroenterology or hepatology clinic visit.

^b Other race and ethnicity includes American Indian or Alaska Native, multiple races and ethnicities, or unknown.

Surveillance Within 12 Months

When evaluating annual HCC surveillance, 2426 patients (40.6%) underwent surveillance in the pre–COVID-19 era, which declined to 2066 patients (31.4%) during the COVID-19 era, and remained similarly low at 1807 patients (30.1%) in the post–COVID-19 era (Figure 1). Patterns of HCC surveillance within 12 months among subgroups were similar to those observed for 6-month HCC surveillance (eFigure in Supplement 1). Notably, HCC surveillance within 12 months declined among non-Hispanic White patients and remained low in the most recent period analyzed, whereas HCC surveillance among Black or African American and Hispanic patients initially declined at the onset of the pandemic and continued to decline in the post–COVID-19 era (eFigure in Supplement 1). Similar to 6-month surveillance, HCC surveillance within 12 months among Asian patients initially declined from March 1, 2018, to February 29, 2020, to March 1, 2020, to February 28, 2022, but rebounded in the post–COVID-19 period. Notably, HCC surveillance within 12 months among uninsured or indigent care patients declined from 326 of 1024 patients (31.8%) in the pre–COVID-19 period to 239 of 1054 patients (22.7%) during the COVID-19 pandemic, and further declined to 160 of 954 patients (16.8%) in the post–COVID-19 period (eFigure in Supplement 1). On multivariable regression analysis, the associations seen for receiving HCC surveillance within 12 months generally were similar those that were observed for the 6-month surveillance analysis (Table 3).

Table 3. Factors Associated With Undergoing HCC Surveillance Within 12 Months of Cirrhosis Diagnosis in the Post–COVID-19 Era: March 1, 2022, to February 29, 2024.

Variable	OR (95% CI)a	P value
Sex
Male	1 [Reference]	NA
Female	1.10 (0.94-1.29)	.23
Age, y
<40	1 [Reference]	NA
40-49	0.79 (0.53-1.18)	.25
50-59	1.06 (0.76-1.49)	.73
60-69	1.04 (0.73-1.46)	.84
≥70	0.79 (0.53-1.19)	.26
Race and ethnicity
Asian	1.34 (0.62-2.91)	.46
Hispanic	1.18 (0.80-1.74)	.40
Non-Hispanic Black or African American	0.88 (0.73-1.06)	.17
Non-Hispanic White	1 [Reference]	NA
Unknown or otherb	1.41 (0.80-2.50)	.24
Language
English	1 [Reference]	NA
Other languages	1.31 (0.75-2.29)	.35
Insurance status
Commercial	1 [Reference]	NA
Medicare	0.90 (0.74-1.09)	.27
Medicaid	0.82 (0.66-1.02)	.08
Other	0.70 (0.36-1.35)	.29
None or indigent care	0.55 (0.32-0.97)	.04
Risk factors and comorbidities
Alcohol use	1.37 (1.13-1.65)	.001
Drug use	0.84 (0.66-1.07)	.16
HIV coinfection	1.24 (0.98-1.58)	.07
Cardiovascular disease	1.07 (0.79-1.45)	.65
Hypertension	0.91 (0.73-1.14)	.41
Diabetes	1.07 (0.91-1.26)	.39
Mental health or psychiatric diagnosis	0.72 (0.60-0.86)	<.001
Non-HCC cancer	1.13 (0.96-1.32)	.13
Cirrhosis complication	1.30 (1.09-1.55)	.003
Model for End-Stage Liver Disease–Sodium score	0.96 (0.94-0.98)	<.001
>1 Gastroenterology or hepatology clinic visit	1.03 (0.86-1.31)	.23

Abbreviations: HCC, hepatocellular carcinoma; NA, not applicable; OR, odds ratio.

^a Model adjusted for site, sex, age, race and ethnicity, primary language, insurance status, cause of liver disease, cirrhosis complications, risk factors and comorbidities, and whether patient had at least 1 gastroenterology or hepatology clinic visit.

^b Other race and ethnicity includes American Indian or Alaska Native, multiple races and ethnicities, or unknown.

Discussion

In this large retrospective cohort study of patients with cirrhosis across 5 US safety-net health systems, the initial declines in HCC surveillance observed following onset of the COVID-19 pandemic did not rebound and remained alarmingly low. In our analysis of data up to 4 years after the onset of the pandemic, fewer than 1 in 4 patients with cirrhosis underwent guideline-recommended semiannual HCC surveillance, and fewer than 1 in 3 patients underwent annual HCC surveillance. These observations are particularly concerning given that adherence to guideline-recommended HCC surveillance is associated with improved long-term patient outcomes. For example, a 2022 meta-analysis⁵ observed that HCC surveillance was associated with improved early-stage detection (risk ratio, 1.86; 95% CI, 1.73-1.98), receipt of potentially curative treatment (risk ratio, 1.83; 95% CI, 1.69-1.97), and overall survival (hazard ratio, 0.67; 95% CI, 0.61-0.72). Early data following the pandemic have already shown some signs of potential detrimental impact of gaps and delays in HCC surveillance.^42,43,44 For example, Li et al⁴³ observed a nearly 50% decline in the proportion of patients with HCC who were eligible for surgical resection at diagnosis from 20% prepandemic to 11% in the first 6 months of the pandemic. Liang et al⁴² observed that age-adjusted incidence rate of HCC in 2020 was 12.2% lower than the expected, with the greatest discrepancy observed among patients from minoritized ethnic groups and patients with located HCC. These data suggest that the lower-than-expected incidence may be due to delays in timely HCC diagnosis directly resulting from persistent gaps and delays in HCC surveillance. Some of the longer-term detrimental impacts (eg, more advanced tumor stage at diagnosis and worse patient survival) of continued gaps and delays in HCC surveillance may be forthcoming; hence, urgent action is needed to address the persistently low HCC surveillance, particularly among vulnerable safety-net populations.

The pandemic-related decline and continued persistently low HCC surveillance was seen among men and women and across all age groups. When stratified by race and ethnicity, non-Hispanic White patients had the highest rate of HCC surveillance within 6 months in the prepandemic period (Figure 2). Following the pandemic, HCC surveillance declined among all racial and ethnic groups. However, in the most recent post–COVID-19 period, although HCC surveillance remained low among non-Hispanic White, Black or African American, and Hispanic patients, HCC surveillance among Asian patients rebounded, surpassing than of prepandemic levels. However, Asian patients represented only 3.0% of our entire cirrhosis cohort and sample size was relatively small; hence, although notable, these trends were not statistically significant.

In the prepandemic period, HCC surveillance was significantly higher in English-speaking patients vs those speaking other languages (March 1, 2018, to February 29, 2020: 33.1% vs 18.9%). The lower HCC surveillance rates among patients speaking other languages may have reflected lower health literacy, which has been associated with lower cancer screening utilization in prior studies.⁴⁵ However, after onset of the pandemic, HCC surveillance among English-speaking patients declined and remained low, whereas surveillance among patients speaking other languages remained essentially unchanged. As a result, in the most recent time period, HCC surveillance was similarly low among both English-speaking patients and those speaking other languages. Although the surveillance trends among English-speaking patients mirror what was observed among the overall cohort, the trends among patients speaking other languages may suggest that a subset of such patients may have been more resilient and better able to adapt to the disruptions in cirrhosis care. It is also possible that patients speaking other languages more often rely on their family or community support networks, which may have helped to mitigate the decline in HCC screening after COVID-19. Another possibility is that among some sites, many patients who were Spanish speaking were able to receive care from Spanish-speaking practitioners, which allowed language-concordant care.

Although HCC surveillance in the prepandemic period was highest among commercially insured patients, patients across all insurance types, with the exception of other, experienced declines in HCC surveillance after onset of the pandemic. However, trends in HCC surveillance among uninsured or indigent care patients with cirrhosis are particularly alarming. This group had one of the lowest HCC surveillance rates in the prepandemic period (22.8% surveillance within 6 months), which declined to 14.4% during the early years of the pandemic, and continued to decline into the most recent post–COVID-19 period (March 1, 2022, to February 29, 2024), when only 1 in 9 patients underwent guideline-concordant HCC surveillance. These observations highlight the urgent need for novel and effective interventions to improve HCC surveillance particularly among underinsured safety-net populations.

Prior studies have demonstrated the success of different targeted interventions to improve HCC surveillance.¹¹ These interventions are best targeted to patient and practitioner barriers that have been associated with lower surveillance completion.²⁷ For example, Singal et al²⁷ demonstrated that implementing mailed outreach invitations plus patient navigation intervention was associated with a 33% improvement in completed HCC surveillance compared with usual care in patients with cirrhosis.⁴⁶ Improving adherence to utilizing ultrasonography Liver Imaging Reporting and Data System criteria can also improve the quality of HCC surveillance examinations.¹² Advancements in blood-based biomarkers that could be potentially used as a primary first-line modality for HCC surveillance could mitigate many of the patient-reported barriers that are associated with imaging-based modalities and improve long-term surveillance adherence.^27,47 These interventions and advancements require more research and have the potential to mitigate some of the existing gaps observed in HCC surveillance.

Strengths and Limitations

A strength of this study is that incorporating clinical practice data on HCC surveillance patterns among a diverse cohort of patients with cirrhosis across 5 safety-net health systems provides a snapshot of health care inequities among some of the most vulnerable populations in the US. Our data are further strengthened by providing contemporary data 4 years following onset of the pandemic to better understand whether health care delivery has rebounded to prepandemic levels.

However, certain limitations should be acknowledged. The utilization of ICD-10-CM codes may have introduced misclassification bias, which we attempted to minimize by using established definitions and algorithms previously validated in large database studies. Furthermore, we incorporated Current Procedural Terminology codes and corresponding ICD-10-CM codes to accurately identify HCC surveillance examinations. Given the observational nature of the study, there may have been other unmeasured confounders or factors (eg, practitioner knowledge regarding HCC surveillance, whether imaging was not ordered or ordered and not completed, and specific hurdles or challenges from the patient perspective) that could have impacted HCC surveillance. It is possible that patients in our cohort may have received care outside of study sites. However, we believe this to have had limited impact on our analyses because most safety-net populations would likely not have undergone elective HCC surveillance outside of safety-net settings owing to insurance limitations, given that HCC surveillance does not constitute acute or emergency care.^23,48,49 Although no systematic changes in HCC surveillance strategies were implemented across all sites during the study period, we acknowledge that potential site-specific variations in quality improvement studies or outreach projects may have affected site-specific rates of HCC surveillance. Diagnostic testing, including HCC surveillance, is often more likely to be completed at initial diagnosis of cirrhosis, which could have influenced HCC surveillance among patients who newly received a diagnosis during the pre–COVID-19 period. On the other hand, patients who are not candidates for HCC treatment, including liver transplant, may have been less likely to undergo HCC surveillance; the observational nature of the study limited our ability to accurately ascertain a patient’s candidacy for HCC treatment. We also acknowledge that successful implementation of effective HCC surveillance is complex, particularly following onset of the COVID-19 pandemic, and gaps and delays in surveillance likely reflect multiple patient-level, practitioner-level, and system-level factors (eg, limited radiology department capacity, lack of integrated electronic health records–based reminders, patient navigators, and patient financial and logistical barriers).^10,50,51,52 The observational nature of our study design limited the ability to assess these more granular factors potentially affecting HCC surveillance.

Conclusions

In this observational study of a multicenter longitudinal cohort of patients with cirrhosis who received care at US safety-net health systems, the onset of the COVID-19 pandemic was associated with major declines in timely HCC surveillance. It was particularly alarming that even up to 4 years following onset of the pandemic, HCC surveillance among safety-net populations had not rebounded to prepandemic levels and remained unacceptably low, with fewer than 1 in 4 patients with cirrhosis having undergone guideline-concordant HCC surveillance. Urgent action is needed to implement novel and effective interventions to improve HCC surveillance to prevent the downstream consequences of advanced tumor stage, limited treatment options, and high mortality.

Supplement 1.

eTable. ICD-10-CM Codes to Identify Imaging Indication for HCC Surveillance

eFigure. Proportion of Patients With Cirrhosis Receiving HCC Surveillance Within 12 Months Across Three Time Periods

Supplement 2.

Data Sharing Statement