A 13-year nationwide analysis of outcomes of non-variceal upper gastrointestinal bleeding in post-bariatric surgery patients

Introduction

Upper gastrointestinal bleeding (UGIB) is defined as bleeding above the ligament of Treitz and is most commonly caused by peptic ulcer disease (PUD), erosive esophagitis, and esophageal varices (1). UGIB occurs in approximately 50–150 per 100,000 individuals in the United States annually (2,3). PUD comprises about 50–60% of UGIB cases, making it the most common cause of non-variceal UGIB (NVUGIB) (3). In contrast, variceal UGIB accounts for 4–16% of cases (3). Obesity has been linked to increased morbidity in NVUGIB patients (4). Obesity increases intra-abdominal pressure and can change gastric mucosal integrity, which contributes to an increased risk of bleeding episodes (5). A standard solution to obesity is weight loss via bariatric surgery in patients with a body mass index (BMI) greater than 40 kg/m² or a BMI greater than 35 kg/m² with various comorbidities (6). There are multiple types of bariatric surgeries, the most common being sleeve gastrectomy (SG) (65% of bariatric surgeries) and Roux-en-Y gastric bypass (RYGB) (17% of bariatric surgeries) (7,8). These surgeries also provide preventative measures for a variety of comorbidities, which include type 2 diabetes mellitus (T2DM), hyperlipidemia (HLD), sleep apnea, and cardiovascular disease (CVD) (8). Despite the increasing prevalence of bariatric surgeries and their potential for comorbidities, limited research exists on post-bariatric surgery patients (PBSPs) and their risk of mortality and morbidity when admitted for NVUGIB. Hypothesize that PBSPs will have better outcomes since obese NVUGIB patients were shown to have increased morbidity.

Our study aims to evaluate the outcomes of PBSPs admitted with NVUGIB over a 13-year span. We identified patients over 18 years old admitted for NVUGIB using International Classification of Disease (ICD) codes from the National Inpatient Sample (NIS) and compared outcomes between those with and without a history of bariatric surgery. By analyzing patient demographics, comorbidities, and clinical outcomes, we intend to provide valuable insights into the outcomes of PBSPs in the context of NVUGIB, which will help improve patient care in this population. We present this article in accordance with the STROBE reporting checklist (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-100/rc).

Methods

Data source

A retrospective cohort study was performed using the NIS from 2008 to 2020. The Healthcare Cost and Utilization Project (HCUP) provides the NIS dataset (9). The NIS database contains healthcare claims and related data from multiple insurance and non-insurance holders from the USA, which is maintained by the Agency for Healthcare Research and Quality (AHRQ) (9). Annually, it comprises over seven million unweighted records and over 35 million weighted hospital encounters (9). The data provide estimates on a national level after re-organization by an algorithm supplied by HCUP, which processes initially unweighted data (9). The data were also de-identified, so the Institutional Review Board (IRB) was not required to conduct this study. Also, the data are publicly available. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013).

Study population

The NIS includes a 20% random sample of all inpatient hospitalizations from over 45 states and contains one primary diagnosis and up to 39 secondary diagnoses using the ICD, 10^th revision (ICD-10), and 29 secondary diagnoses with the ICD, 9^th revision, (ICD-9) codes. Groups were defined based on the history of bariatric surgery and demographics and comorbidities. Demographics were age, gender, race (White, Black, Hispanic, other). Also, the incidence of comorbidities, which were coronary artery disease, HLD, hypertension (HTN), T2DM, congestive heart failure (CHF), anemia, end-stage renal disease (ESRD), obesity, smoking, gastroesophageal reflux disease, PUD, liver cirrhosis, alcoholic use disorder, insurance status (Medicare, Medicaid, self-pay), were compared. Again identified by ICD codes, outcomes were compared between the two groups, and odds ratios (ORs) were calculated using weighted multivariate two-stage logistic regression. ORs were adjusted for common co-founders such as age, gender, race, and Charlson comorbidity index (CCI). Patients with a new or prior diagnosis of bariatric surgery (ICD-9 code: V45.86; ICD-10 code: Z98.84) were identified as the subject population of 28,167 patients over the 13 years. Then, those without bariatric surgery with NVUGIB (ICD-9 code: 578.9; ICD-10 code: K92.2) were the control population of 2,203,659 patients in this study. Our primary endpoints were odds of adverse outcomes, all-cause in-hospital mortality, shock, acute myocardial infarction (AMI), acute kidney injury (AKI), and composite outcomes. Secondary endpoints were a length of stay (LOS) and hospital charges.

Statistical analysis

The Pearson Chi-squared and Student’s t-test assessed categorical and continuous variables. The linear-by-linear association test analyzed the trends in the frequency of NVUGIB in bariatric surgery in hospitalized patients. After adjusting for baseline characteristics and comorbidities to account for confounding variables, a two-step hierarchical multivariate regression model was used, emphasizing variables with P<0.05. These variables included age, gender, race, CCI, and insurance payer status. Stata version 17 by StataCorp LLC (College Station, TX, USA) was utilized for all statistical analyses.

Results

A total of 2,231,826 patients admitted for NVUGIB were included in this study. Of these, 28,167 had a history of bariatric surgery. The timing of bariatric surgery and the incidence of NVUGIB cannot be determined with this database; only a documented history of bariatric surgery can be determined. PBSPs were younger, with a mean age of 55.57 years (P<0.001), while non-PBSPs (NBSPs) were 68.25 years (P<0.001). NBSPs were mostly male (53.36% male, 46.64% female, P<0.001), while PBSPs were more likely to be female (30.37% male, 69.63% female, P<0.001). PBSPs were mostly white (77.44% White, 11.96% Black, 7.17% Hispanic, 3.44% other, P<0.001), as were NBSPs (70.93% White, 13.95% Black, 8.52% Hispanic, 6.60% other, P<0.001). PBSPs were less complicated (CCI: 2.71 vs. 4.76, P<0.001), had a shorter LOS (4.07 vs. 5.09 days, P<0.001), and were less likely to be on Medicare/Medicaid than NBSPs (52.03% vs. 74.10%, P<0.001) (Table 1).

Several comorbidities were more common in PBSPs, including HTN (43.66% vs. 42.46%, P=0.07), anemia (22.61% vs. 20.46%, P<0.001), obesity (30.99% vs. 10.68%, P<0.001), smoking (16.39% vs. 16.26%, P=0.79), gastroesophageal reflux disease (26.47% vs. 22.75%, P<0.001), and PUD (1.81% vs. 1.57%, P=0.13). NBSPs were more likely to have coronary artery disease (16.20% vs. 27.98%, P<0.001), HLD (25.67% vs. 38.34%, P<0.001), T2DM (26.37% vs. 30.16%, P<0.001), CHF (6.94% vs. 15.96%, P<0.001), ESRD (2.84% vs. 5.15%, P<0.001), liver cirrhosis (2.34% vs. 5.25%, P<0.001), and alcohol use disorder (14.92% vs. 15.14%, P=0.65) (Table 1).

We found that patients admitted for NVUGIB with a history of bariatric surgery had significantly lower odds of all outcomes. All-cause mortality was 0.55% in PBSPs vs. 1.97% in NBSPs (OR =0.48; 95% CI: 0.340–0.690; P<0.001). AKI occurred in 9.16% of PBSPs vs. 19.34% in NBSPs (OR =0.71; 95% CI: 0.645–0.775; P<0.001). AMI occurred in 0.88% of PBSPs vs. 2.69% of NBSPs (OR =0.62; 95% CI: 0.469–0.824; P<0.05). Shock occurred in 4.49% of PBSPs vs. 5.97% of NBSPs (OR =0.88; 95% CI: 0.769–0.995; P<0.05). Any of these outcomes occurred in 13.36% of PBSPs vs. 24.69% of NBSPs (OR =0.77; 95% CI: 0.707–0.829; P<0.001) (Table 2).

Discussion

NVUGIB includes pathologies such as PUD, erosive esophagitis, and Malorry-Weiss tear, and vascular lesions such as Dieulafoy syndrome, vascular ectasias, and angiodysplasia (3,10,11). Limited research exists on the direct correlation between NVUGIB and obesity. Previous studies have primarily focused on the association between NVUGIB and conditions such as GERD and operative complications in obese patients (11,12).

PBSPs had fewer comorbidities, likely leading to lower morbidity and mortality rates. In contrast, NBSPs had higher incidences of coronary artery disease (CAD), HLD, CHF, T2DM, ESRD, and liver cirrhosis (P<0.05). Obesity rates were almost twice as high in the NBSPs, which carries an increase in the risk of these comorbidities. Various studies have demonstrated that weight loss, whether from bariatric surgery or other methods, decreases the prevalence of these risk factors and improves the management of T2DM, HLD, and HTN (8,13,14). Although this study did not demonstrate any statistical difference in HTN between PBSPs and NBSPs, weight reduction is a modifiable risk factor relating to HTN (15) (Table 1).

There is a lack of studies evaluating the direct long-term effects of chronic kidney disease (CKD) management in PBSPs. Evidence suggests that the weight loss and improved glycemic control associated with bariatric surgery may have protective effects (16-18). A study by Sood et al. found that patients with CKD or ESRD who are admitted with primary UGIB may face up to a threefold greater risk of all-cause in-hospital mortality (19). The significant decrease in renal disease in the PBSP group is likely attributed to weight loss leading to improvements in blood pressure, reduced systemic inflammation, and improved renal function (20). Furthermore, weight loss also improves insulin sensitivity, thereby improving T2DM (21). PBSPs have been associated with decreased admission rates for CHF exacerbation, increased left ventricular ejection fraction, and reduced cardiovascular events (22-24). Patients taking anticoagulants, low-dose aspirin, and other antiplatelet drugs demonstrate an increased risk of UGIB (25). An 11-month study showed a 1.6% increase in NVUGIB following post-percutaneous coronary artery intervention (26). There is limited research on the direct relationship between HF and NVUGIB. Still, it has been suggested that hypoxia and microperfusion from severe HF can result in mucosal lesions that progress to NVUGIB (10,27).

UGIB or nutrient deficiencies in folate, iron, or vitamin B12 can result in anemia. The absorption of these nutrients depends on the environment’s acidity and the architecture of the small intestine. Alexandrou et al. demonstrated similar iron and folate deficiencies observed post-operatively in SG and RYGB populations—around 40–60% and 18–20% of post-operative cases, respectively. Vitamin B12 deficiency was seen greater in RYGB than SG (42.1% vs. 5%, P=0.003), which has been observed more commonly in malabsorptive (i.e., RYGB) rather than restrictive procedures (i.e., SG) (10,28-31). Similarly, our study found higher rates of anemia in PBSPs. In regards to post-bariatric surgery GERD, Gu et al. demonstrated a nearly five-fold increase in de novo GERD and worsening of GERD, greater in SG patients than RYGB patients (32). Additionally, RYGB improved obesity-related GERD more significantly than SG (40.4% in LSG and 74.2% in LRYGB) (32,33). GERD does put patients at an elevated risk for developing erosive esophagitis and thus can predispose patients to anemia. The two-fold increase in the female population observed in our study and the increased GERD rate in our PBSP population are related to the increased anemia rates observed (34). Due to the nature of our study, the different types of nutrient deficiencies related to anemia were not analyzed.

We also found that patients admitted for NVUGIB with a history of bariatric surgery had significantly lower odds of all-cause mortality (OR =0.48; P<0.001), AKI (OR =0.71; P<0.001), AMI (OR =0.62; P<0.01), shock (OR =0.88; P<0.05), and a composite of these four (OR =0.77; P<0.001) (Table 2). AKI is common in NVUGIB, resulting in a longer LOS and higher odds of mortality (35) (Table 2). However, our study found a reduction in the incidence of AKI among patients with a history of bariatric surgery. Several factors can explain this. Post-bariatric patients experience drastic weight loss, which helps improve metabolic health. Reducing body weight decreases kidney strain, improving renal function (21). This, combined with improved blood pressure control, is beneficial. Obesity is the most common risk factor for HTN, which can lead to chronic kidney damage and an increased incidence of AKI (36,37). In addition, patients with bariatric surgery also have a lower incidence of cardiovascular events, such as AMI and CHF (38). AKI is often linked to cardiovascular events; therefore, the reduced risk of AMI and CHF also lowers the risk of AKI (39). Treatment for AMI can sometimes lead to UGIB as patients are started on antiplatelet/coagulant therapy and/or percutaneous coronary intervention (39,40). However, data suggests that there is a decreased risk of AMI in patients with a history of bariatric surgery, particularly in an acute setting (40). Similar rates of all-cause mortality were observed in this study, which compared teaching hospitals to non-teaching hospitals (41,42).

The LOS was slightly lower for PBSPs, 4 days as compared to five for NBSPs. This could be because NBSPs tend to have more comorbidities, making managing these patients more challenging. According to a report from 2008, NVUGIB patients with comorbidities or complications tend to have a longer LOS (43). In addition, a 2023 analysis of hospital outcomes for NVUGIB indicates that the rate of self-pay is 5.7%, which is similar for both PBSPs and NBSPs (44). However, this study observed a lower proportion of Medicare/Medicaid utilization in PBSPs, which could be related to younger patient groups having private/employer insurance compared to the average senior age of the NBSP group.

Adam et al. suggest that patients with liver cirrhosis who undergo bariatric surgery have higher mortality rates compared to bariatric patients without cirrhosis (45). Another recent article suggests that patients with decompensated cirrhosis and NVUGIB have higher admission rates, mortality rates, and healthcare utilization than patients with controlled cirrhosis and those without cirrhosis (46,47). NVUGIB occurs in approximately 30–40% of cirrhotic patients (48). Interestingly, our study found lower rates of liver cirrhosis in patients who underwent bariatric surgery. This may be due to the selective bias in surgical candidacy. Patients with severe comorbidities, such as advanced liver disease, are not typically considered suitable candidates for bariatric surgery. In addition, there is a reduction in hepatic fat content, preventing the progression of non-alcoholic fatty liver disease, which can progress into cirrhosis (27,49). A follow-up cohort study at Mayo Clinic did not show hepatic decompensation, cardiovascular events, or mortality in bariatric patients with cirrhosis over more than 4 years (50). It remains unclear whether there’s a reduction in cirrhosis cases among PBSPs due to surgical candidacy, cirrhosis management, or other factors. A systematic review by Nojkov and Cappell showed that PUD is the most common cause of NVUGIB in cirrhotic patients, with a higher rebleeding rate (51). However, in this study, PUD was only found in 1.81% of PBSPs and 1.57% of NBSPs (P>0.05).

While this data shows statistical differences in various morbidity and mortality factors, the patient may not be a good candidate or opt out of bariatric surgery, as the procedure does hold its risks. There are specific relative contraindications for bariatric surgery, such as severe heart failure, unstable coronary artery disease, end-stage lung disease, active cancer diagnosis/treatment, cirrhosis, uncontrolled drug or alcohol dependency, severely impaired intellectual, Crohn’s disease, ventral hernias, severe adhesions, large livers, high BMI with central obesity, physiological intolerance of pneumoperitoneum (50). Thus, it may be possible that the decrease in observed comorbidities may be due to selection bias, as the PBSP may have had less severe comorbid conditions preoperative than the NBSP. It may be worthwhile to evaluate further the risks of pursuing bariatric surgery and its potential protective effects on its relative contraindications.

This study did not compare different outcomes based on gender or ethnicity, cancer or autoimmune history, the various types of NVUGIB, primary vs. recurrent bleeding, recent drug use, the different types of bariatric surgery, post-operative time related to the time of admission, or BMI. Also, this study has limitations that need to be addressed. The nature of this dataset is unable to trace patient encounters or admission diagnoses longitudinally or decipher the frequency of admissions or number of admissions of the same patient. Hence, problems can be over-calculated due to readmissions of the same patient. Also, propensity scoring was unable to be performed with this data. With NIS data, treatment medications, and lab values are not available. Specific causes of morbidity, mortality, or NVUGIB cannot be deciphered in this dataset. NIS can only differentiate the main reason for admission, in this case, we decided based on obesity and NVUGIB using ICD-9 and ICD-10 codes. The use of ICD-9 and ICD-10 has variability as variability exists in documentation. NIS uses ICD codes, which depend on healthcare workers’ style of billing and coding, creating unknown confounders. Finally, the NIS does not detail important clinical predictors, such as the severity of NVUGIB, duration of comorbidities, and baseline function. Surgical details are unknown, so bariatric surgery complications, timing before the NVUGIB event, and frequency or revisions are unknown. The NIS does not have information on specific management, which includes treatment medications and lab values, is unavailable. Since this is a retrospective cohort study, it has an inherent low external validity. Also, there is a lack of controlled randomized studies to suggest that bariatric surgery is a protective measure for the comorbidities observed in this study.

Conclusions

Patients admitted for NVUGIB with a history of bariatric surgery are at a lower risk of mortality, AMI, shock, and AKI compared to those without a history of bariatric surgery. This suggests that these patients may experience milder bleeding episodes. These findings are essential because patients at increased risk of NVUGIB may benefit from early intervention with weight loss. This raises the question of whether patients at risk of NVUGIB should undergo bariatric surgery to decrease their overall risk of morbidity and mortality but further research must be conducted to substantiate this finding.

Acknowledgments

This project was a poster presentation at Digestive Disease Week, held from May 18^th to the 21^st, 2024, in Washington, DC, USA.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-100/rc

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-100/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-100/coif). The 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 (as revised in 2013).

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/.

References

1. Antunes C, Tian C, Copelin II EL. Upper Gastrointestinal Bleeding. In: StatPearls. Treasure Island: StatPearls Publishing; 2024.
2. Bardou M, Benhaberou-Brun D, Le Ray I, et al. Diagnosis and management of nonvariceal upper gastrointestinal bleeding. Nat Rev Gastroenterol Hepatol 2012;9:97-104. [Crossref] [PubMed]
3. Alali AA, Barkun AN. An update on the management of non-variceal upper gastrointestinal bleeding. Gastroenterol Rep (Oxf) 2023;11:goad011. [Crossref] [PubMed]
4. Abougergi MS, Peluso H, Mrad C, et al. The Impact of Obesity on Mortality and Other Outcomes in Patients With Nonvariceal Upper Gastrointestinal Hemorrhage in the United States. J Clin Gastroenterol 2019;53:114-9. [Crossref] [PubMed]
5. Camilleri M, Malhi H, Acosta A. Gastrointestinal Complications of Obesity. Gastroenterology 2017;152:1656-70. [Crossref] [PubMed]
6. Wolfe BM, Kvach E, Eckel RH. Treatment of Obesity: Weight Loss and Bariatric Surgery. Circ Res 2016;118:1844-55. [Crossref] [PubMed]
7. Elder KA, Wolfe BM. Bariatric surgery: a review of procedures and outcomes. Gastroenterology 2007;132:2253-71. [Crossref] [PubMed]
8. Arterburn DE, Telem DA, Kushner RF, et al. Benefits and Risks of Bariatric Surgery in Adults: A Review. JAMA 2020;324:879-87. [Crossref] [PubMed]
9. HCUP Databases. Healthcare Cost and Utilization Project (HCUP). Rockville: Agency for Healthcare Research and Quality; 2021. Available online: https://hcup-us.ahrq.gov/nisoverview.jsp
10. Davies DJ, Baxter JM, Baxter JN. Nutritional deficiencies after bariatric surgery. Obes Surg 2007;17:1150-8. [Crossref] [PubMed]
11. Lanas A, Dumonceau JM, Hunt RH, et al. Non-variceal upper gastrointestinal bleeding. Nat Rev Dis Primers 2018;4:18020. [Crossref] [PubMed]
12. El-Serag H. The association between obesity and GERD: a review of the epidemiological evidence. Dig Dis Sci 2008;53:2307-12. [Crossref] [PubMed]
13. Weissman S, Aziz M, Bangolo AI, et al. Relationships of hospitalization outcomes and timing to endoscopy in non-variceal upper gastrointestinal bleeding: A nationwide analysis. World J Gastrointest Endosc 2023;15:285-96. [Crossref] [PubMed]
14. Batsis JA, Romero-Corral A, Collazo-Clavell ML, et al. Effect of weight loss on predicted cardiovascular risk: change in cardiac risk after bariatric surgery. Obesity (Silver Spring) 2007;15:772-84. [Crossref] [PubMed]
15. Chiang BN, Perlman LV, Epstein FH. Overweight and hypertension: a review. Circulation 1969;39:403-21. [Crossref] [PubMed]
16. Navaneethan SD, Yehnert H. Bariatric surgery and progression of chronic kidney disease. Surg Obes Relat Dis 2009;5:662-5. [Crossref] [PubMed]
17. Chagnac A, Weinstein T, Herman M, et al. The effects of weight loss on renal function in patients with severe obesity. J Am Soc Nephrol 2003;14:1480-6. [Crossref] [PubMed]
18. Sjöström L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004;351:2683-93. [Crossref] [PubMed]
19. Sood P, Kumar G, Nanchal R, et al. Chronic kidney disease and end-stage renal disease predict higher risk of mortality in patients with primary upper gastrointestinal bleeding. Am J Nephrol 2012;35:216-24. [Crossref] [PubMed]
20. Montereggi A, Leone A, Castelli G, et al. Prevalence and subtypes of systemic hypertension in an unselected patient population with severe obesity undergoing bariatric surgery. G Ital Cardiol (Rome) 2012;13:291-6. [PubMed]
21. Bjornstad P, Nehus E, van Raalte D. Bariatric surgery and kidney disease outcomes in severely obese youth. Semin Pediatr Surg 2020;29:150883. [Crossref] [PubMed]
22. Bays HE. Why does type 2 diabetes mellitus impair weight reduction in patients with obesity? A review. Obes Pillars 2023;7:100076. [Crossref] [PubMed]
23. Kindel TL, Strande JL. Bariatric surgery as a treatment for heart failure: review of the literature and potential mechanisms. Surg Obes Relat Dis 2018;14:117-22. [Crossref] [PubMed]
24. Kwok CS, Pradhan A, Khan MA, et al. Bariatric surgery and its impact on cardiovascular disease and mortality: a systematic review and meta-analysis. Int J Cardiol 2014;173:20-8. [Crossref] [PubMed]
25. Berger S, Meyre P, Blum S, et al. Bariatric surgery among patients with heart failure: a systematic review and meta-analysis. Open Heart 2018;5:e000910. [Crossref] [PubMed]
26. Lanas Á, Carrera-Lasfuentes P, Arguedas Y, et al. Risk of upper and lower gastrointestinal bleeding in patients taking nonsteroidal anti-inflammatory drugs, antiplatelet agents, or anticoagulants. Clin Gastroenterol Hepatol 2015;13:906-12.e2. [Crossref] [PubMed]
27. Bilal M, Samuel R, Khalil MK, et al. Nonvariceal upper GI hemorrhage after percutaneous coronary intervention for acute myocardial infarction: a national analysis over 11 months. Gastrointest Endosc 2020;92:65-74.e2. [Crossref] [PubMed]
28. De Backer D, Creteur J, Dubois MJ, et al. Microvascular alterations in patients with acute severe heart failure and cardiogenic shock. Am Heart J 2004;147:91-9. [Crossref] [PubMed]
29. Knight T, D'Sylva L, Moore B, et al. Burden of Iron Deficiency Anemia in a Bariatric Surgery Population in the United States. J Manag Care Spec Pharm 2015;21:946-54. [Crossref] [PubMed]
30. Lupoli R, Lembo E, Saldalamacchia G, et al. Bariatric surgery and long-term nutritional issues. World J Diabetes 2017;8:464-74. [Crossref] [PubMed]
31. Alexandrou A, Armeni E, Kouskouni E, et al. Cross-sectional long-term micronutrient deficiencies after sleeve gastrectomy versus Roux-en-Y gastric bypass: a pilot study. Surg Obes Relat Dis 2014;10:262-8. [Crossref] [PubMed]
32. Gu L, Chen B, Du N, et al. Relationship Between Bariatric Surgery and Gastroesophageal Reflux Disease: a Systematic Review and Meta-analysis. Obes Surg 2019;29:4105-13. [Crossref] [PubMed]
33. American Society of Hematology. Iron-deficiency anemia. Available online: https://www.hematology.org/education/patients/anemia/iron-deficiency
34. Chang P, Friedenberg F. Obesity and GERD. Gastroenterol Clin North Am 2014;43:161-73. [Crossref] [PubMed]
35. Kabaria S, Tawadros A, Rotundo L, et al. Impact of acute kidney injury in hospitalizations with non-variceal upper gastrointestinal bleeding. J Gastroenterol Res 2021;5:170-80.
36. Shariq OA, McKenzie TJ. Obesity-related hypertension: a review of pathophysiology, management, and the role of metabolic surgery. Gland Surg 2020;9:80-93. [Crossref] [PubMed]
37. Hall ME, do Carmo JM, da Silva AA, et al. Obesity, hypertension, and chronic kidney disease. Int J Nephrol Renovasc Dis 2014;7:75-88. [Crossref] [PubMed]
38. Mosko JD, Nguyen GC. Increased perioperative mortality following bariatric surgery among patients with cirrhosis. Clin Gastroenterol Hepatol 2011;9:897-901. [Crossref] [PubMed]
39. Niu C, Zhang J, Ukrani H, et al. Reduction of cardiovascular complications during delivery hospitalization in patients undergoing bariatric procedures. Int J Obes (Lond) 2024;48:1133-9. [Crossref] [PubMed]
40. Campos GM, Khoraki J, Browning MG, et al. Changes in Utilization of Bariatric Surgery in the United States From 1993 to 2016. Ann Surg 2020;271:201-9. [Crossref] [PubMed]
41. Odutayo A, Wong CX, Farkouh M, et al. AKI and Long-Term Risk for Cardiovascular Events and Mortality. J Am Soc Nephrol 2017;28:377-87. [Crossref] [PubMed]
42. SAGES guideline for clinical application of laparoscopic bariatric surgery. Surg Obes Relat Dis 2009;5:387-405. [Crossref] [PubMed]
43. Yoo AY, Joo MK, Park JJ, et al. Recurrent Non-Variceal Upper Gastrointestinal Bleeding among Patients Receiving Dual Antiplatelet Therapy. Diagnostics (Basel) 2023;13:3444. [Crossref] [PubMed]
44. Kruger AJ, Abougergi MS, Jalil S, et al. Outcomes of Nonvariceal Upper Gastrointestinal Bleeding in Patients With Cirrhosis: A National Analysis. J Clin Gastroenterol 2023;57:848-53. [Crossref] [PubMed]
45. Adam V, Barkun AN. Estimates of costs of hospital stay for variceal and nonvariceal upper gastrointestinal bleeding in the United States. Value Health 2008;11:1-3. [Crossref] [PubMed]
46. Asotibe JC, Shaka H, Akuna E, et al. Outcomes of Non-Variceal Upper Gastrointestinal Bleed Stratified by Hospital Teaching Status: Insights From the National Inpatient Sample. Gastroenterology Res 2021;14:268-74. [Crossref] [PubMed]
47. Kolotkin RL, Crosby RD, Gress RE, et al. Health and health-related quality of life: differences between men and women who seek gastric bypass surgery. Surg Obes Relat Dis 2008;4:651-8; discussion 658-9. [Crossref] [PubMed]
48. Izzy M, Angirekula M, Abu Dayyeh BK, et al. Bariatric surgery proves long-term benefit in patients with cirrhosis. Gastroenterol Rep (Oxf) 2021;9:252-6. [Crossref] [PubMed]
49. Głuszyńska P, Lemancewicz D, Dzięcioł JB, et al. Non-Alcoholic Fatty Liver Disease (NAFLD) and Bariatric/Metabolic Surgery as Its Treatment Option: A Review. J Clin Med 2021;10:5721. [Crossref] [PubMed]
50. Farooq U, Tarar ZI, Franco D, et al. Comparison of outcomes between variceal and non-variceal gastrointestinal bleeding in patients with cirrhosis: Insights from a Nationwide Inpatient Sample. Ann Gastroenterol 2022;35:618-26. [Crossref] [PubMed]
51. Nojkov B, Cappell MS. Distinctive aspects of peptic ulcer disease, Dieulafoy's lesion, and Mallory-Weiss syndrome in patients with advanced alcoholic liver disease or cirrhosis. World J Gastroenterol 2016;22:446-66. [Crossref] [PubMed]