Pediatric Cholecystectomy Case Volume and Complexity Following the COVID-19 Pandemic Free

Historically, biliary disease was considered rare in children, but more recent studies highlight increased cholecystectomy rates.^1–6 During the COVID-19 pandemic, many adults scheduled for elective surgery experienced delays in care, with notable increases in inpatient admissions for biliary disease.^7–11 Although we continue to learn more about COVID-19 infection, little is known about the collateral and downstream effects of the COVID-19 pandemic in children. Delays in elective surgery, emergency department and hospital avoidance, mandatory stay-at-home policies, and transfer patterns between adult and pediatric hospitals may impact utilization of pediatric surgical care.

For children, in addition to surgical delays, stay-at-home policies may have limited access to regular exercise and healthy meals. Multiple studies demonstrate a decrease in physical activity and significant changes in diet associated with an increase in childhood obesity during the pandemic.^12–22 These epidemiologic findings are notable as increased weight and poor dietary habits are associated with biliary disease. A recent single-center study from a Western Pediatric Surgery Research Consortium (WPSRC) member hospital noted a significant increase in pediatric cholecystectomy during the COVID-19 pandemic.²³ However, it is unknown whether this increase in the need for cholecystectomy is occurring within the larger pediatric population.

Our goal was to examine the effects of the COVID-19 pandemic on pediatric biliary disease requiring cholecystectomy. We hypothesized that the number of pediatric cholecystectomies performed and the complexity of biliary disease cared for at children’s hospitals increased after the start of the COVID-19 pandemic.

A multi-institutional, retrospective cohort study was conducted for children ages 18 years and younger who underwent cholecystectomy from January 1, 2016, to July 31, 2022, at 10 children’s hospitals within WPSRC. Each institution’s electronic medical record (EMR) was queried for the following Current Procedural Terminology codes for cholecystectomy: 47 562, 47 563, 47 564, 43 260, 43 261, 43 263, 43 264, 43 265, 43 274, 43 275, 43 276, 43 277, and 43 278. Children who underwent cholecystectomy for congenital biliary anomalies (including biliary atresia), gallbladder polyps, or oncologic resections or during liver transplantation were excluded (Figure 1). The beginning of the pandemic was defined as March 19, 2020, when the first statewide mandatory stay-at-home policies went into effect. The prepandemic group included patients who underwent cholecystectomy from January 1, 2016, to March 19, 2020, whereas the during-pandemic group was from March 20, 2020, to July 31, 2022. January 1, 2016, was selected as the start date to ensure adequate years to establish prepandemic trend and patterns. The study was individually approved by each WPSRC site’s institutional review board.

The demographic and clinical factors of the patients collected from review of the EMR included age, race and ethnicity, sex, body mass index (BMI), insurance/payer status, Area Deprivation Index (ADI), and chronic medical conditions (obesity defined as BMI higher than 30, sickle cell anemia, beta thalassemia, hereditary spherocytosis, other anemia, cystic fibrosis, and cardiac disease). Surgical indication was determined by review of the operative report, surgeon’s description of findings, and diagnosis. All those classified as “acute cholecystitis” had findings of gallstones. Patients with “acalculus cholecystitis” did not have gallstones. Additional factors regarding the surgical encounter were collected including endoscopic retrograde cholangiopancreatography (ERCP) performed (Y/N), magnetic resonance cholangiopancreatography (MRCP) performed (Y/N), laparoscopic vs open surgery, inpatient vs outpatient surgery, and transfer status. Transfer status was defined as patients who underwent interfacility transfer for inpatient surgery.

Race and ethnicity are recognized as social constructs and were included as certain minoritized groups have experienced disproportionately higher rates of COVID-19 infection, hospitalization, COVID-19–related mortality, and unemployment during the pandemic.^24,25 Including race and ethnicity facilitated our ability to evaluate the unequal burden the COVID-19 pandemic placed on patients from marginalized populations. Race and ethnicity categories were defined according to availability in individual hospitals’ EMR. Each hospital reported race and ethnicity data for each visit according to institutional practices and thus may include parent/guardian reporting at time of admission. Patients with missing race and/or ethnicity data were categorized as “unknown/not reported,” separate from the “other” category.

The ADI was determined for each patient and deidentified using the University of Wisconsin School of Medicine and Public Health website.²⁶ The ADI ranks neighborhoods based upon 17 indicators from the American Community Survey, which encompasses information on socioeconomic domains including education, economic, housing, social, food security, and transportation.^27–29 The ADI score correlates with access to pediatric surgical care and was used as a proxy for socioeconomic disadvantage.^30,31 ADI national rankings (0–100) were reported as median/IQR and divided into tertiles (low, moderate, and high) with the highest tertile representing greater socioeconomic disadvantage.

The primary outcome of interest was cholecystectomy case volume defined by number of cholecystectomies performed per month. The secondary outcomes included surgical indication as indication of complexity of biliary disease and transfer status. Postoperative outcomes were also evaluated, including length of stay (days), postoperative complications (pancreatitis, common bile duct injury, retained stone, cholangitis, pneumonia, deep venous thrombosis [DVT], urinary tract infection [UTI], bleeding), readmissions within 30 days of discharge, and indication for readmission (superficial surgical site infection, intraabdominal abscess, bowel injury, cholangitis/retained stone, common bile duct injury, pneumonia, UTI, DVT, bile leak, bleeding, pain control). All variables were obtained via a standardized manual chart review of the EMR at all sites.

Continuous variables were described using median and IQR, and Wilcoxon-Mann-Whitney tests were used to compare the groups. Categorical variables were described using frequencies and percentages with χ² or Fischer’s exact tests used to compare the groups. Nonparametric tests were used for data that were not normally distributed. The total monthly number of cholecystectomies performed was compared between the prepandemic and pandemic groups, with trends evaluated by interrupted time series (ITS) analysis using the autoregressive integrated moving average model to account for the correlated observations taken over time.^32,33 ITS modeling is a robust method for evaluating interventions or critical events at a population level by accounting for underlying trends, autocorrelation, and seasonality, although patient-specific variables are not included in the model.³⁴ The ITS analysis was selected to determine whether the case volume trends observed in the analysis significantly deviated from those that would have been expected before the COVID-19 pandemic. The impact of the COVID-19 pandemic was evaluated by the change in the level (immediate step change) and trend of the monthly number of cholecystectomies performed. As a sensitivity analysis, the ITS was repeated with a subgroup of the cohort excluding patients who were transferred from a referring hospital for inpatient surgery. A P value of less than .05 was considered significant. Data analysis was performed using SAS software version 9.4 (SAS Institute Inc).

The cohort consisted of 4282 patients: 2122 in the prepandemic group and 2160 in the pandemic group. Most patients were female (74.5%), Hispanic (57.6%), and publicly-insured (64.6%) with a median age of 15 years (IQR, 13.0–16.0 years). Children and adolescents who underwent cholecystectomy during the pandemic had significantly higher BMI values than those undergoing cholecystectomy before the pandemic (26.0 kg/m² vs 27.1 kg/m²; P < .001). The distribution of race and ethnicity differed between the 2 groups (P = .009; Table 1). Notably, although Hispanic patients made up the majority of prepandemic and during-pandemic groups, the proportion of Hispanic patients increased during the pandemic (55.0% vs 60.1%; Table 1). Irrespective of group, most patients fell into the least-disadvantaged ADI tertile (score: 0–39), and the proportion between ADI tertiles differed by pandemic period (P = .01; Table 1). The number of patients with chronic medical conditions predisposing to biliary disease, including sickle cell anemia (3.5% vs 2.3%; P = .02), beta thalassemia (0.3% vs 0%; P = .02), hereditary spherocytosis (3.7% vs 2.0%; P = .001), and cystic fibrosis (0.5% vs 0.1%; P = .02), decreased during the pandemic. Obesity was more common during the pandemic (30.8% vs 37.4%; P < .001; Table 1).

Changes in surgical indication for cholecystectomy were observed between the prepandemic and during-pandemic groups (Table 2). Symptomatic cholelithiasis (56.1 vs 45.6%; P < .001) and biliary dyskinesia (6.2% vs 4.3%; P = .005) as an indication for cholecystectomy decreased during the pandemic, and an increase in cholecystectomy for complicated biliary disease was observed. Significant increases in cholecystectomy for acute cholecystitis (12.2% vs 17.3%; P < .001), choledocholithiasis (12.8% vs 16.5%; P = .001), and chronic cholecystitis (1.4% vs 3.2%; P < .001) occurred during the pandemic. Although not statistically significant, a higher proportion of gallstone pancreatitis was reported during the pandemic (10.6% vs 12.4%; P = .06). Although MRCP utilization increased in the during-pandemic group (14.3% vs 17.7%; P = .003), there was no significant difference in the proportion of ERCPs performed (18.0% vs 18.8%; P = .53) (Table 2).

During the pandemic, a greater proportion of patients were transferred from a referring hospital for inpatient cholecystectomy during the same hospitalization (21.3% vs 28.5%; P < .001). There was also a significant difference in the type of surgical encounter (outpatient vs inpatient) between the groups, with an increased proportion of inpatient encounters (49.1% vs 60.3%; P < .001) (Table 2). There was no significant difference in the proportion of cholecystectomies performed laparoscopically vs open during the pandemic (99.5% and 99.3%; P = .36).

The median length of stay of both prepandemic and pandemic groups was 2 days (prepandemic IQR, 2.0–4.0; pandemic IQR, 1.0–4.0) with the pandemic group skewed to a slightly shorter length of stay (P = .003) (Table 2). Fewer postoperative complications were reported before the pandemic (no postoperative complications: 93.4% vs 83.8%; P < .001). However, on individual examination of common complications after cholecystectomy, such as retained stone, cholangitis, common bile duct injury, pancreatitis, and bleeding, there were no significant differences between groups (Table 2). Among patients who had a readmission within 30 days, there was a decrease in the proportion of patients with readmission reason secondary to pain control during the pandemic (34.7% vs 18.3%; P = .006) (Table 2).

Raw cholecystectomy case counts increased after the start of the pandemic at each institution (Supplemental Table 1). When evaluating cholecystectomy case volume via ITS analysis, there were significant differences in the prepandemic and pandemic groups (Table 3; Figure 2). Before the pandemic, the average monthly cholecystectomy case count was 40.08 (95% CI, 36.32–43.85) and there was no significant change in month-to-month case volume trend over time (0.08; 95% CI, −0.05 to 0.21; P = .19). Immediately following March 19, 2020, the monthly case count increased by 4.32 (95% CI, −2.12 to 10.75). After the start of the pandemic period, the month-to-month case volume trend significantly increased by 1.69 (95% CI, 1.36–2.01; P < .001). To determine whether the significant increase in cholecystectomies was secondary to a change in transfer patterns from adult to children’s hospitals, a sensitivity analysis excluding transferred patients was performed. Even when excluding patients transferred for cholecystectomy, a significant increase in case volume during the pandemic remained (Table 3; Figure 3; P < .001). Finally, when stratified by individual children’s hospital, cholecystectomy case volume increased at each institution during the pandemic (Figure 4).

Our study demonstrates a considerable and continuing increase in the month-to-month case volume of cholecystectomies for children during the first 2.5 years of the COVID-19 pandemic. Additionally, children undergoing cholecystectomy were more likely to present with complicated biliary disease and were more likely to undergo MRCP imaging. Consistent with national trends, children undergoing cholecystectomy during the pandemic had significantly higher BMIs and increased rates of obesity.^12–22 Finally, the significant increase in case volume persisted even when excluding children transferred for inpatient surgery. These findings may represent broader shifts in the epidemiology of pediatric biliary disease and lasting changes in health care utilization that occurred during and persisted after the COVID-19 pandemic.

In the past, pediatric biliary disease necessitating cholecystectomy was uncommon and primarily associated with hemolytic disorders.³ In recent decades, an increase in the incidence of pediatric cholecystectomy has been observed.^1–6,35 Historically, the increase in volume in the United States was thought to be driven by increases in biliary dyskinesia.^6,36–38 More recent literature shows that symptomatic cholelithiasis from nonhemolytic gallstones is now most common, which is largely attributed to the obesity epidemic in children.^5,6,39 Although not the focus of the present study, regional practice patterns may also be indicated by our findings as the definition of biliary dyskinesia is heterogeneous.⁴⁰ Although the rise in case volume noted in our study may reflect the natural progression of these trends seen over the last few decades, the changes in surgical indication reported in our study deviate from those previously described. During the pandemic, we observed that the number of children undergoing cholecystectomy for symptomatic cholelithiasis, biliary dyskinesia, or hematologic disorders decreased during the pandemic. More complicated biliary disease, including acute cholecystitis, choledocholithiasis, and chronic cholecystitis, increased. Additionally, our study’s findings are not consistent with ongoing national trends,^35–38 and instead demonstrate that after the onset of the COVID-19 pandemic, the cholecystectomy case volume increase was abrupt and statistically significant. Adult studies examining the impact of delayed cholecystectomy during the COVID-19 pandemic demonstrated a similar increase in the severity of biliary disease presentations and inpatient admissions.^7–11 The increases in complicated biliary disease as surgical indications for cholecystectomy may explain why more cases were performed during a period of halting elective operations. Additionally, we report a decrease in readmissions related to pain control, which may be further indicative of health care avoidance during the COVID-19 pandemic.

In addition to the effects of health care avoidance and delayed surgical intervention, mandatory stay-at-home policies for COVID-19 may have impacted key risk factors for the development of pediatric biliary disease. Multiple studies have shown that the COVID-19 lockdown led to increased screen time, reduced physical activity, and dietary changes among children.^{12,13,15–22} Moreover, existing literature points to an increase in pediatric BMI and the prevalence of obesity in the United States.^12–16 A retrospective study using data from Kaiser Permanente Southern California revealed significant weight gain during the pandemic, particularly in 5- to 11-year-old children.¹² A Centers for Disease Control and Prevention study on over 400 000 children and adolescents across the United States reported that the monthly rate of BMI increase doubled between the prepandemic and pandemic periods.¹³ Additionally, pediatric patients who were overweight before the pandemic experienced higher monthly rates of BMI increase compared with children of healthy weight before the pandemic.¹³ In line with current literature, our study reports a rise in BMI and a higher prevalence of obesity among patients undergoing cholecystectomy during the pandemic at children’s hospitals across the western United States. Furthermore, our patient population was predominantly female and of Hispanic ethnicity. Although not surprising as increased BMI, female sex, and Hispanic ethnicity are all well-documented risk factors for gallstone disease,^5,39 our findings allow for the development of targeted interventions for vulnerable subpopulations.

Ten years before the COVID-19 pandemic, 70% of pediatric inpatient admissions and 40% of pediatric general surgery operations took place in adult general hospitals.^6,41 Therefore, the rise in cholecystectomy case volume could be due to increased transfer of pediatric patients from adult hospitals to alleviate the burden COVID-19 put on inpatient bed availability, similar to those reported in pediatric trauma centers.⁴² Indeed, we report an increase in the proportion of patients transferred from a referring hospital to 1 of the 10 participating children’s hospitals for inpatient surgery. Furthermore, transfer status does not capture changes in referral patterns across a large region nor does it account for existing patterns of regionalization of pediatric inpatient care over the last decade. Since 2008, pediatric inpatient units in the United States decreased by 19.1% and inpatient unit beds decreased by 11.8%, with rural areas seeing the sharpest declines.⁴³ Pediatric beds are increasingly concentrated at children’s hospitals, with inpatient unit beds increasing 12.1% at children’s hospitals and decreasing 18.4% at adult general hospitals.⁴³ Additionally, closures of pediatric inpatient units increased during and after the COVID-19 pandemic due to the need for adult beds and drive for increased profits.⁴⁴ The pandemic acutely exacerbated and accelerated shifts that were already under way with respect to where pediatric care is delivered in the United States. Importantly, however, when transfer patients were excluded from the analysis, the sharp increase in month-to-month trend persisted, indicating that our results are likely multifactorial and cholecystectomy case counts cannot be explained by the changes in pediatric health care delivery alone.

The closing of pediatric units in general hospitals and similar shifts in the US health care system placed further strain on populations already at risk for poor access to care and may contribute to the increase in the presentation of complicated biliary disease at children’s hospitals. Notably, our results are limited to a racially and ethnically diverse group of children and adolescents, most of whom were publicly insured and cared for at institutions with large Hispanic populations. We report an increase in the proportion of Asian patients and a decrease in the proportion of Black patients treated with cholecystectomy during the pandemic at WPSRC institutions. Additionally, we report that the proportion of Hispanic patients treated with cholecystectomy increased during the pandemic at WPSRC institutions. It is important to note that Hispanic families have experienced disproportionately higher rates of COVID-19 infection, hospitalization, COVID-19–related mortality, and increased unemployment during the pandemic.^24,25 Indeed, in our study, the proportion of patients undergoing cholecystectomy with public insurance increased and the proportion of those with private insurance decreased during the pandemic. The results of this study therefore add to our understanding of the unequal burden the COVID-19 pandemic placed on children from certain populations and their families. Although we also note an increase in the median ADI for both groups, this was not statistically significant. Additionally, we report a greater proportion of children in the middle ADI tertile and a decrease in those in the highest ADI tertile during the pandemic. It could be that the movement of the highest tertile prepandemic ADI scores to more moderate ADI scores in the pandemic group is due to the American Rescue Plan, which expanded the Child Income Tax credit.⁴⁵ This law resulted in a substantial reduction in child poverty overall and marked the lowest child poverty rate on record, which may have lessened the differences seen due to ADI for this cohort as factors impacting ADI scores for the most vulnerable groups improved.⁴⁵ Furthermore, the change in the distribution of ADI tertiles may support the view that despite the unequal impact on certain populations, changes in where pediatric care is delivered in the United States is impacting all pediatric patients.

Our study has several limitations. This study was performed at multiple institutions in the Western region of the United States, and it is unknown whether the findings observed are reflective of national trends. Although anecdotally each of the participating institutions experienced closures of pediatric inpatient beds at surrounding hospitals, specifics of these closures, timing, and whether temporary related to our findings is unknown. Additionally, any readmissions to a hospital other than the institution where surgery was performed were not captured. Although the demographic composition of the West is predominantly Hispanic, the US census predicts that Hispanic children will make up 31.9% of the pediatric population by 2060.⁴⁶ Our results therefore may have future implications for pediatric health nationally. Additionally, the COVID-19 status of patients was not collected, and thus we cannot hypothesize whether infection with or exposure to the virus had any effect on our results reported. We elected not to explore the relationship between COVID-19 infection at time of cholecystectomy because of the changing accuracy of testing, emergence of new variants, inability to distinguish recent vs distant infection, and/or long–COVID-19. Although an association between COVID-19 and liver disease was identified,⁴⁷ to our knowledge there are not studies in either the pediatric or adult population reporting an effect of COVID-19 on the biliary system. Although unlikely, we acknowledge that further investigation would be needed to determine whether COVID-19 is directly linked with pediatric biliary disease. Finally, in May 2023, the World Health Organization declared that COVID-19 no longer constituted a Public Health Emergency of International Concern.⁴⁸ This retrospective study does not allow us to draw a causal link to COVID-19 pandemic alone unless a decrease in case volume to prepandemic levels was observed after the pandemic was declared over. However, cholecystectomy case volumes continued to rise even in the last 7 months of data collection in 2022 (Supplemental Table 1). Future studies are needed to determine whether the trends reported in this study represent a new baseline for pediatric health or were isolated to the COVID-19 pandemic.

Among hospitals participating in WPSRC, we observed a sharp rise in monthly cholecystectomy case volume and complexity during the COVID-19 pandemic. Children and adolescents undergoing cholecystectomy also had increased BMI and higher rates of obesity. The increase in pediatric cholecystectomy volume may be secondary to increases in childhood obesity, changes in transfer and referral patterns away from adult general hospitals, increasing the concentration of pediatric care to children’s hospitals, and other shifts in health care utilization that occurred during the COVID-19 pandemic.