Enhanced long-term outcomes with laparoscopic bariatric surgery in patients with severe obesity and metabolic dysfunction-associated steatotic liver disease: a retrospective cohort study

Introduction

Metabolic dysfunction-associated steatotic liver disease (MASLD) is associated with end-stage liver disease as well as non-liver complications such as cardiovascular disease (CVD), chronic kidney disease (CKD) and other non-liver cancers (1-3). MASLD affects approximately 30% of people globally with increasing incidence and prevalence that is forecasted to reach 55% by 2040 (4). Such trends are due to the rapid increase of metabolic disorders such as obesity and type 2 diabetes (5).

There are currently limited pharmacological therapies approved specifically for MASLD. Weight loss through lifestyle modifications and use of some weight loss drugs like semaglutide remain the major treatments but are limited by poor adherence over time (6). European Association for the Study of the Liver (EASL)-European Association for the Study of Diabetes (EASD)-European Association for the Study of Obesity (EASO) Clinical Practice Guidelines suggested that patients with MASLD and class II or III obesity [body mass index (BMI) ≥35 kg/m²] can consider bariatric surgery if lifestyle interventions or pharmacological therapy do not work well on weight loss (7). Bariatric surgery for severe obesity (class II or III obesity) can offer an effective and durable alternative for weight loss, especially with increasing use of laparoscopic surgery such as laparoscopic sleeve gastrectomy (SG) as opposed to open Roux-en-Y operation (8,9). Weight loss following bariatric surgery is associated with improvements in liver steatosis, inflammation, and fibrosis (10,11) as well as reduced risk of adverse liver and non-liver events and mortality (12-14). Additionally, a recent randomized trial found that bariatric surgery resolved steatohepatitis more effectively than lifestyle modifications (15). In addition, bariatric surgery may offer the potential for achieving hepatic recompensation in MASLD-related cirrhosis and is getting increasing attention (16).

Prior studies generally found that laparoscopic surgery as compared to open surgery was associated with a reduced risk of postoperative mortality, infections, and other complications as well as reduced length of stay and hospital charges, but higher reoperation rates after surgery (17-21). However, most studies mainly focused on short-term postoperative complications or mortality. As a result, data comparing long-term complications of laparoscopic vs. open bariatric surgery are sparse, particularly among patients with MASLD and severe obesity. Therefore, we aimed to compare long-term liver- and non-liver complications and healthcare utilization and costs in patients with MASLD and severe obesity who underwent laparoscopic vs. open bariatric surgery. We present this article in accordance with the STROBE reporting checklist (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-529/rc).

Methods

Data source

We conducted a retrospective cohort study using the Merative™ Marketscan^® Research Databases housed in the Population Health Science Center at Stanford University, Palo Alto, California (22,23). The Marketscan^® database is a large national administrative claims database with data on approximately 250 million Americans with private health insurance and Medicare supplemental insurance in the United States (U.S.) between January 2007 and December 2022.

Study population

We first identified adult patients with at least one inpatient or two outpatient diagnoses for MASLD. According to the 2023 MASLD guideline of American Association for the Study of Liver Diseases (AASLD) (24), MASLD patients are those who have hepatic steatosis and at least one of five cardiometabolic risk factors. We further restricted the study population to patients with severe obesity (BMI ≥35 kg/m²) to be consistent with the indications for bariatric surgery on individuals with a BMI ≥35 kg/m², with or without coexisting comorbidities in clinical guidelines (25). To avoid misclassification, only patients with bariatric surgery that performed after the first MASLD diagnosis were included. Patients with diagnosis of hepatocellular carcinoma (HCC), cirrhosis or liver transplant, or history of other cancers prior to the first MASLD diagnosis date were also excluded. Patients were followed until the occurrence of liver or non-liver outcomes, withdrawal from insurance or last follow-up date (12/31/2022), whichever came first.

Bariatric surgery cohort

We categorized 46,476 patients with MASLD and severe obesity into laparoscopic surgery (n=39,190) and open surgery group (n=7,286). The index date was defined as the bariatric surgery date. All bariatric surgeries were defined using the Current Procedural Terminology (CPT), International Classification of Diseases, Ninth and Tenth Revision, Clinical Modification (ICD-9-CM and ICD-10-CM) procedure codes recommended by the American Society for Metabolic and Bariatric Surgery including laparoscopic/open Roux-en-Y gastric bypass (RYGB), laparoscopic/open SG, laparoscopic/open vertical-banded gastroplasty (VBG), laparoscopic/open adjustable gastric banding (AGB), open biliopancreatic diversion-duodenal switch (BPD/DS) (Table S1).

Study outcomes

The study outcomes were the incidence of (I) adverse liver outcomes, including HCC, cirrhosis, and liver decompensation; and (II) adverse non-liver outcomes, including CVD, CKD, and primary obesity-related cancers. Any liver-related outcomes were a composite outcome of HCC, cirrhosis, and/or liver decompensation.

Healthcare use and costs

All-cause healthcare use was reported as the annual number of claims per patient for inpatient admissions, emergency department (ED) visits, outpatient visits, and pharmaceutical prescriptions. We also assessed the prevalence of having at least one inpatient admission, ED visit, outpatient visit, and pharmaceutical prescriptions following the index date. Similarly, all-cause inpatient, ED, outpatient, and pharmaceutical healthcare costs were reported as annual costs per patient adjusted to 2021 U.S. dollars (USD), where all dollar estimates were inflated to 2021 dollars using the Medical Care Component of the Consumer Price Index (CPI).

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study protocol was reviewed and approved by the institutional review board of Stanford Research Compliance Office at Stanford University, California (approval No. 13927), and individual consent for this retrospective analysis was waived because anonymous and de-identified information was used for the analyses.

Statistical analysis

Descriptive statistics included mean and standard deviation (SD) or median [interquartile range (IQR)] reported for continuous variables, counts with percentages reported for categorical variables. Continuous variables of two independent groups were compared by Student’s t-tests or Wilcoxon signed-rank test; categorical variables were analyzed by Pearson’s Chi-squared or Fisher’s exact tests, where appropriate.

To adjust for potential confounding variables and bias for adverse liver and non-liver outcomes between laparoscopic and open surgery, we used propensity score matching (PSM) and a nearest-neighbor 1:1 matching scheme to match these two groups, with the logit of the propensity score (PS) within 0.2 SD. The PS was developed from a logistic regression model using age, sex, geographic region, insurance type, provider specialty, year of MASLD diagnosis, year of bariatric surgery, Charlson Comorbidity Index (CCI), the presence of diabetes, hypertension, hyperlipidemia, asthma, obstructive sleep apnea, obesity hypoventilation syndrome and use of metabolic medications. For continuous variables, we did not have missing data on age and CCI. For categorical variables, sex (female/male), geographic region (Northeast, North central, South, West, and unknown), insurance type [health maintenance organization (HMO), preferred provider organization (PPO), and others], provider specialty [non-gastroenterologist (GI)/endocrinologist (Endo), GI/Endo], year of MASLD diagnosis (2007–2011, 2012–2016, and 2017–2022), year of bariatric surgery (2007–2015 and 2016–2022), the presence of comorbidities (yes/no) and use of metabolic medications (yes/no) also did not show any missing data in the database (Appendix 1). Thus, no missing data need to be addressed for these variables. For healthcare use and costs, we additionally matched for the two groups among those who had complete healthcare use and cost records in the Marketscan^® database. Incidence analyses of adverse liver and non-liver outcomes excluded patients who had specific outcomes at baseline. The Kaplan-Meier method was used to examine the cumulative incidence of liver and non-liver outcomes in the two groups, with log-rank test for comparison. Cox proportional hazard model was used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs) of adverse liver and non-liver outcomes. We did not perform competing risks model adjusting for non-liver outcomes (e.g., CVD or cancer) but analyzed non-liver outcomes independently because several studies have found that when patients develop CVD, CKD, or non-liver cancer, they still have possibility to develop cirrhosis or HCC during their lifetime (26-29).

We performed subgroup analyses stratified by index year (2007–2012 and 2013–2021), age (<50 and ≥50 years) and sex to investigate the association between bariatric surgery types and the risk of adverse liver and non-liver outcomes. Index year, age, and sex were not adjusted for in subgroup analyses stratified by each of these specific respective factors. To confirm the robustness of findings, we performed sensitivity analyses: (I) we excluded patients with viral hepatitis or other hepatobiliary diseases; and (II) we excluded adverse outcomes within 1 year after the index date. To detect residual bias from unmeasured confounding, we performed negative control analyses including anemia and hemiplegia without known association with bariatric surgery types. Statistical significance was defined as a two-tailed P value <0.05. All statistical analyses were performed using R software version 4.3.3 (R Foundation for Statistical Computing, Vienna, Austria).

Results

Patient characteristics

We identified 922,914 patients with MASLD diagnosis between 2007 and 2022. After excluding patients aged <18 years, those without severe obesity, those with significant alcohol use, and history of HCC, cirrhosis, liver transplant or other cancers prior to the first MASLD diagnosis date, 46,476 eligible patients with MASLD and severe obesity (BMI ≥35 kg/m²) were included in the analysis (Figure S1). Compared to those with open surgery (n=7,286), patients with laparoscopic surgery (n=39,190) were younger (44.72 vs. 54.84 years), less likely to be male (23.5% vs. 38.6%) and to have comorbidities including DM, hypertension, hyperlipidemia, CVD, CKD, non-liver cancers, asthma and obesity-related comorbidity at baseline (Table 1). After 1:1 PSM, a total of 5,629 matched pairs of patients with laparoscopic surgery and open surgery were similar across demographic and clinical characteristics.

Utilization trend, patient characteristics, and postoperative complications by bariatric surgery procedure types

Among all bariatric surgeries performed, RYGB was the dominant surgery procedure prior to 2012 then declined to 30% after, whereas SG became the dominant procedure accounting for more than half of bariatric surgeries after 2012 (Figure 1). Other procedures including ABG, VBG, and BPD/DS were rarely performed throughout the study period.

Figure 1 Percentage of bariatric surgery types in MASLD and severe obesity patients from 2007 to 2022. AGB, adjustable gastric banding; BPD/DS, biliopancreatic diversion-duodenal switch; MASLD, metabolic dysfunction-associated steatotic liver disease; RYGB, Roux-en-Y gastric bypass; SG, sleeve gastrectomy; VBG, vertical-banded gastroplasty.

Within each time period 2007–2015 or 2016–2021, patients with laparoscopic surgery were younger, less likely to be male and had less comorbidities (Table S2). In regard to <30-day postoperative complications, there were no significant differences between laparoscopic and open surgery in the frequency of incisional hernia and intestinal obstruction, but laparoscopic surgery group had more gastrointestinal bleeding (0.18% vs. 0.03%) and nausea/vomiting (1.48% vs. 0.10%) than open surgery group (Table S3). In regard to medium-term complications, laparoscopic surgery group had lower rates of gastroesophageal reflux disease (0.80% vs. 2.44%), incisional hernia (0.20% vs. 0.81%), chronic diarrhea (0.63% vs. 1.48%), and reoperation rate (0.51% vs. 2.74%), but had a higher rate of dumping syndrome (0.24% vs. 0.03%) than open surgery group.

Association between bariatric surgery types and adverse liver outcomes

In the PSM cohort, during a mean follow-up duration of 3.72 and 4.04 years of laparoscopic and open surgery, 331 (4.0%), 20 (0.2%), 330 (4.0%), and 266 (2.9%) patients developed any liver-related outcomes, HCC, cirrhosis and liver decompensation, respectively. Cumulative incidence of any liver-related outcomes was significantly lower for patients with laparoscopic surgery compared to those with open surgery at 5 years (3.7% vs. 6.7%) and 10 years (6.0% vs. 11.3%, P<0.001; Figure 2A). Similar findings were observed in the outcome of cirrhosis and liver decompensation (Figure 2B,2C). Because PSM has effectively balanced the relevant baseline characteristics of the study groups, we did not further adjust for these variables in multivariable analysis. Patients with laparoscopic surgery had a 47% lower risk of any liver-related outcomes [adjusted HR (aHR) =0.53; 95% CI: 0.42–0.67; P<0.001] and cirrhosis (aHR =0.53; 95% CI: 0.42–0.66; P<0.001), and 32% reduced risk of liver decompensation (aHR =0.68; 95% CI: 0.53–0.87; P=0.002) compared to those with open surgery (Table 2). There was no statistically significant difference in the risk of HCC between laparoscopic and open surgery.

Figure 2 Cumulative incidence of (A) any liver-related outcomes, (B) cirrhosis, (C) liver decompensation, (D) CVD, (E) CKD, (F) obesity-related cancer in MASLD and severe obesity patients with laparoscopic surgery or open surgery. CKD, chronic kidney disease; CVD, cardiovascular disease; MASLD, metabolic dysfunction-associated steatotic liver disease.

Association between bariatric surgery types and adverse non-liver outcomes

For non-liver outcomes, 671 (7.8%), 481 (5.5%), and 163 (1.5%) patients developed CVD, CKD, and obesity-related cancers, respectively. Patients with laparoscopic surgery had lower cumulative incidence of CVD, CKD and obesity-related cancers than those with open surgery at 5 and 10 years (Figure 2D-2F). In multivariable analysis, patients with laparoscopic surgery had a 67% reduced risk of CVD (aHR =0.33; 95% CI: 0.28–0.40; P<0.001), 56% reduced risk of CKD (aHR =0.44; 95% CI: 0.36–0.54; P<0.001), and 42% reduced risk of obesity-related cancers (aHR =0.58; 95% CI: 0.42–0.80; P<0.001), compared to those who had open surgery (Table 2). We further investigated specific obesity-related cancers. Patients with laparoscopic surgery had lower cumulative incidence of colorectal cancer, pancreatic cancer and female-specific cancer than those with open surgery (Figure S2A-S2C). After multivariable adjustment, laparoscopic surgery group was associated 71% lower risk of pancreatic cancer (aHR =0.29; 95% CI: 0.12–0.71; P=0.007), 35% lower risk of female-specific cancer (aHR =0.65; 95% CI: 0.43–0.98; P=0.041) and a trend of lower risk of colorectal cancer (aHR =0.57; 95% CI: 0.30–1.09; P=0.09) (Table 2).

Healthcare use and costs between bariatric surgery types

After PSM for two bariatric surgery types among those who had complete healthcare use and cost records, we included 1,880 matched pairs of patients with laparoscopic surgery and open surgery. Patients with laparoscopic surgery had less frequent all-cause annual inpatient admissions (0.04 vs. 0.06, P=0.04), ED visits (0.03 vs. 0.08, P=0.01) and outpatient visits (2.09 vs. 2.63, P=0.01; Table 3). Compared to open surgery group, laparoscopic surgery group had a lower prevalence of having at least one ED visit (3.1% vs. 8.0%, P<0.001) and outpatient visit (54.7% vs. 71.5%, P<0.001), but higher prevalence of having at least one pharmacy claims annually (64.7% vs. 59.7%, P=0.002). Patients with laparoscopic surgery had higher annual outpatient costs ($1,249 vs. $922, P<0.001) but lower pharmacy costs ($21,766 vs. $24,353, P<0.001) compared to those with open surgery (Table 4). However, there was no significant difference in the annual costs of inpatient admissions or ED visits between the two surgery types.

Subgroup and sensitivity analysis

Consistent findings were observed in subgroup analyses stratified by index year (2007–2012 and 2013–2022), age (<50 and ≥50 years), and sex (Tables S4-S6 and Figure S3A-S3C). The results of sensitivity analyses were also consistent with our main findings. When excluding patients with viral hepatitis or other hepatobiliary diseases and excluding adverse outcomes within 1 year after the index date, laparoscopic surgery was still associated with risk reductions in liver-related outcomes, CVD, CKD, and obesity-related cancers (Tables S7,S8). In negative control analyses, observed risks of anemia and hemiplegia without known association with bariatric surgery were similar across patients with laparoscopic and open surgery, showing no obvious residual bias from unmeasured confounding for the comparison (Table S9).

Discussion

To our knowledge, this is the first study to compare the long-term clinical outcomes to include both liver and non-liver adverse events, as well as healthcare utilization and costs between laparoscopic surgery and open surgery in patients with MASLD and severe obesity. In this population-based study, laparoscopic surgery was associated with reduced risks of adverse liver outcomes and non-liver outcomes including CVD, CKD, and obesity-related cancers, as well as lower healthcare use and pharmacy costs, compared with open surgery among patients with MASLD and severe obesity.

In a retrospective study of patients with biopsy-proven MASH and obesity, bariatric surgery was associated with a significantly lower risk of incident major adverse liver outcomes and cardiovascular events compared with the nonsurgical group (12). Another nationwide study from the U.S. showed that bariatric surgery was associated with significant risk reduction in any cancer and obesity-related cancers in patients with MASLD and severe obesity compared to those who did not undergo bariatric surgery (14). Recent evidence from a decision analysis study by Rouhi et al. found that surgical weight loss was associated with a reduction in the progression of MASH, thereby reducing the need for liver transplant (30). The results of this decision analysis align with our study’s findings by underscoring the benefit of bariatric surgery on the long-term outcomes with the reduction of end-stage liver disease and liver transplant. Our study adds to the current knowledge by providing long-term outcome data for patients undergoing bariatric surgery by the types of surgery. We found that patients with laparoscopic surgery had more favorable long-term outcomes than those with open surgery. These significant findings may be interpreted by that patients who underwent laparoscopic surgery might be less sick, have less complications and proves to achieve better quality of life after surgery compared to those with open surgery (31). In addition to data on several liver and non-liver adverse events, we provided data for specific obesity-related cancers including colorectal cancer, pancreatic cancer and female-specific cancer which reduced risks with laparoscopic surgery as compared to open surgery.

Laparoscopic bariatric surgery has been associated with more favorable liver outcomes in terms of liver enzyme normalization, liver histology improvement, and overall liver function recovery, possibly due to the less traumatic nature of the surgery and reduced stress and inflammatory response on the liver during recovery compared with open surgery (32). Consistent with our study, a prior randomized controlled trial compared laparoscopic and open gastric bypass surgery in morbidly obese patients with MASLD and found that the laparoscopic group had more significant reductions in weight loss, liver fat content, and improved liver function when compared to open surgery group (31). Our study also provided important data for the association between laparoscopic surgery and non-liver complications, which may be partly due to the less invasive nature of the procedure, quicker recovery, fewer complications and better control over cardiovascular risk factors such as diabetes and obesity (33,34). Prior studies have reported fewer long-term complications related to CVD in patients undergoing laparoscopic surgery as compared to open operation (35,36). However, data comparing laparoscopic vs. open bariatric surgery on the long-term outcomes of extrahepatic cancer risk are sparse. Regardless, weight loss achieved through both types of surgery is known to reduce the incidence of certain cancers and laparoscopic surgery tends to have a better long-term recovery and less inflammation response, which may help reduce the likelihood of developing cancer, but further studies are needed (37,38).

The U.S. national trend of laparoscopic surgery dramatically increase over time, paralleled by a substantial decrease in open surgery from 2006 to 2015 (8). Our study also demonstrated that laparoscopic surgery was preferred for better outcomes compared to the open approach. In this study, among different bariatric surgery types, we further showed SG was more prevalent over RYGB in U.S. since 2016, which may be attributed to the simpler procedure, improvement of surgical techniques, shorter operation time and lower morbidity and mortality rates observed with SG (39). Our subgroup analyses also supported that laparoscopic surgery was associated with lower risk of liver and non-liver outcomes than open surgery regardless of index year, age and sex.

A 6-year follow-up of bariatric surgery and control cohorts found that total costs including inpatient, outpatient and pharmacy costs in the first two years postoperative for patients with laparoscopic surgery were significantly lower than those with open surgery, but these differences did not persist in subsequent periods (40). This study was limited by the shorter follow-up for the newer procedures during 2002–2008. Banka et al. reported that patients who underwent open surgery had longer median lengths of inpatient stay (3.5 vs. 2.4 days) and higher inpatient costs ($35,018 vs. $32,671) than those who had laparoscopic surgery using the 2005–2007 Nationwide Inpatient Sample from the U.S. (18). However, this retrospective study only reported inpatient utilization and costs but did not investigate ED, outpatient and pharmacy use and costs. In our study, we provided evidence that patients with laparoscopic surgery had less frequent inpatient, ED and outpatient visits, and had lower pharmacy costs compared to those with open surgery, which suggests patients with laparoscopic surgery may achieve better health state and quality of life after surgery.

Strengths and limitations

There are several strengths of this study. First, we had a large sample size with individual-level claims data from a real-world cohort that is representative of the general U.S. population with private health insurance. Second, to minimize the impact of selection bias and confounding variables in retrospective data, PSM was used to minimize confounders between the two groups. This methodological strength provides further evidence of the strong association between bariatric surgery types and long-term outcomes. Lastly, we adjusted for multiple confounding variables associated with adverse outcomes, as well as conducted multiple subgroups, sensitivity analyses and negative control analyses to further enhance the robustness of our results.

Our study also had several limitations. We did not adjust for additional potential confounders such as race, lifestyle, and socioeconomic status as they were not available in the Marketscan^® database, so future studies are needed to evaluate these factors. Also, administrative claims databases are prone to have under-coding and misclassification issues. However, as this is a large database maintained with rigorous methods, the misinterpretation of disease states may be minimized. Additionally, our study focused on short and medium-term complication rates, so further studies are needed to assess potential differences in the long-term complications of the different bariatric surgical approaches. Furthermore, the database only included insured individuals, so the findings may not apply to individuals who are uninsured or underinsured, but individuals with lesser health coverage may have more advanced disease and even higher risk for complications. Lastly, though we adjusted for as many potential confounders associated with adverse outcomes that were available, there may still be some potential unmeasured confounders that were not captured. The criteria for surgical approach selection as unmeasured confounders can vary based on the patient’s health and medical history (e.g., severe obesity-related comorbidities, high BMI, abdominal anatomy may be better suited for open surgery) and surgical experience and expertise (e.g., surgeons with extensive experience in laparoscopic techniques and facility support may prefer this method for less complications), as well as patient’s preference and risk tolerance (e.g., recovery time and cost) (25). These potential selection biases can lead to an overestimation or underestimation of the benefits of one approach over the other. For example, if laparoscopic surgeries are usually performed by more experienced surgeons or at better-equipped hospitals, the study could incorrectly attribute better outcomes to the laparoscopic approach, when in reality the differences might be due to these confounding factors. Conversely, if open surgery is performed in less experienced surgeons or in less-equipped facilities, its outcomes may appear worse than they truly are. However, we performed additional negative control analyses which suggested that our findings were robust despite the potential presence of unmeasured confounders and residual bias after PSM. In addition, entropy balancing can also be a complementary method to PSM for addressing unmeasured confounding in future studies (41).

Conclusions

In this population-based study, patients with MASLD and severe obesity who underwent laparoscopic surgery had significantly lower risk of adverse liver and non-liver outcomes including CVD, CKD, and obesity-related cancers than those who had open surgery. Patients with laparoscopic surgery were also associated with less healthcare utilization and pharmacy costs compared to those with open surgery. The present study suggests that laparoscopic surgery is a promising potential treatment for patients with MASLD and severe obesity with more favorable long-term outcomes and healthcare utilization and costs than open surgery. Although our study provides novel information, randomized clinical trials and additional cost-effectiveness analysis are needed to corroborate our findings.

Acknowledgments

Data for this project were accessed using the Stanford Center for Population Health Sciences Data Core. The Population Health Sciences Data Core is supported by a National Institutes of Health National Center for Advancing Translational Science Clinical and Translational Science Award (UL1TR003142) and from Internal Stanford funding. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-529/rc

Data Sharing Statement: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-529/dss

Peer Review File: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-529/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-529/coif). M.H.N. declares research funding from Pfizer, Enanta, Astra Zeneca, Glycotest, GSK, Delfi, Innogen, Exact Science, CurveBio, Gilead, Vir Biotech, Helio Health, National Cancer Institute, National Health Institute, Roche; and leadership or fiduciary role and consulting fees from Exelixis, Gilead, Intercept, GSK, Exact Science. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study protocol was reviewed and approved by the institutional review board of Stanford Research Compliance Office at Stanford University, California (approval No. 13927), and individual consent for this retrospective analysis was waived because anonymous and de-identified information was used for the analyses.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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