Peptic ulcer bleeding patients with Rockall scores 6 are at risk of long-term ulcer rebleeding: A 3.5-year prospective longitudinal study

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1 bs_bs_banner doi: /jgh GASTROENTEROLOGY Peptic ulcer bleeding patients with Rockall scores 6 are at risk of long-term ulcer rebleeding: A 3.5-year prospective longitudinal study Er-Hsiang Yang,*,,1 Hsiu-Chi Cheng,*,,1 Chung-Tai Wu,*, Wei-Ying Chen,*, Meng-Ying Lin*, and Bor-Shyang Sheu*,, *Institute of Clinical Medicine, Department of Internal Medicine, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, and Department of Internal Medicine, Tainan Hospital, Ministry of Health and Welfare, Executive Yuan, Tainan, Taiwan Key words gastrointestinal bleeding, peptic ulcer disease, rebleeding. Accepted for publication 9 May Correspondence Professor Bor-Shyang Sheu, Department of Internal Medicine, National Cheng Kung University Hospital, 138 Sheng Li Road, Tainan, or 125 Chuang-Shan Road, Tainan Hospital, Ministry of Health and Welfare, Tainan, Taiwan. sheubs@mail.ncku.edu.tw Guarantor of the article: Professor Bor-Shyang Sheu Author contributions: Dr Yang E. H. and Cheng H. C. designed and performed the research study and wrote the manuscript. Dr Wu C. T., Dr Chen W. Y., and Dr Lin M. Y. collected and analyzed the data. Professor Sheu B. S. revised the manuscript critically and gave approval of the submitted and final versions. All authors approved the final version of the article, including the authorship list. Declaration of conflict of interest: The authors declare no financial relationship with any company involved in this study. There is no conflict of interest involved in this submission. 1 These authors contributed to this work equally. Abstract Background and Aim: Patients with high Rockall scores have increased risk of rebleeding and mortality within 30 days after peptic ulcer bleeding, but long-term outcomes deserve follow-up after cessation of proton pump inhibitors. The paper aimed to validate whether patients with high Rockall scores have more recurrent ulcer bleeding in a 3.5-year longitudinal cohort. Methods: Between August 2011 and July 2014, 368 patients with peptic ulcer bleeding were prospectively enrolled after endoscopic hemostasis to receive proton pump inhibitors for at least 8 to 16 weeks. These subjects were categorized into either a Rockall scores 6 group (n = 257) or a Rockall scores <6 group (n = 111) and followed up until July of 2015 to assess recurrent ulcer bleeding. Results: The proportion of patients with rebleeding during the 3.5-year follow-up was higher in patients with Rockall scores 6 than in those with scores <6 (10.51 vs per 100 person-year, P = 0.004, log rank test). Among patients with Rockall scores 6, activated partial thromboplastin time prolonged 1.5-fold (P = 0.045), American Society of Anesthesiologists physical status class III (P = 0.02), and gastric ulcer (P = 0.04) were three additional independent factors found to increase rebleeding risk. The cumulative rebleeding rate was higher in patients with Rockall scores 6 with more than or equal to any two additional factors than in those with fewer than two additional factors (15.69 vs per 100 person-year, P = 0.012, log rank test). Conclusions: Patients with Rockall scores 6 are at risk of long-term recurrent peptic ulcer bleeding. The risk can be independently increased by the presence of activated partial thromboplastin time prolonged 1.5-fold, American Society of Anesthesiologists class III, and gastric ulcer in patients with Rockall scores 6. Introduction Peptic ulcer bleeding is a common and lethal disease worldwide. 1 International guidelines advocate for the use of validated prognostic scales to risk-stratify patients with upper gastrointestinal bleeding. 2,3 Several scoring systems have been proposed to predict outcomes, including the Rockall score. 4 Previous studies have demonstrated that the Rockall score can predict the risk of rebleeding and mortality within 30 days following peptic ulcer bleeding. 5,6 Proton pump inhibitors (PPIs) heal peptic ulcers well and decrease the risk of rebleeding. 7 Especially in the case of those with high Rockall scores within the acute bleeding stage, 5,8,9 aggressive dosage or longer PPI duration has been shown to decrease the risk of rebleeding for the first month after bleeding. 10,11 Therefore, the use of PPIs is the current standard of treatment for peptic ulcer bleeding; more importantly, adequate dosage and duration must be indicated for patients with high Rockall scores. 156 Journal of Gastroenterology and Hepatology 33 (2018)

2 E-H Yang et al. Long-term rebleeding in Rockall scores 6 Nearly one-third of patients with peptic ulcer bleeding have rebleeding episodes within 1 2 years, and the number of episodes continues to increase in nearly half of these patients over the subsequent 10 years. 12 Concerning such a high cumulative rebleeding rate in long-term follow-up, it is of clinical importance to identify patients at risk of rebleeding and thus to start secondary prevention with PPIs. The risk scoring systems currently available can only be used to predict short-term outcomes. There is still a lack of evidence to validate the role of these scoring systems in predicting long-term outcomes, especially after PPI cessation. This study is thus of high originality to validate whether a high Rockall score can serve as a long-term predictor of rebleeding after cessation of PPI treatment. This study was a prospective large-scale design to demonstrate in a 3.5-year longitudinal cohort study of patients with Rockall scores 6 that these patients have an increased risk of recurrent bleeding. Our findings will be helpful to identify patients at risk of rebleeding in cases of peptic ulcer bleeding that thus have the potential to need secondary prevention with long-term PPIs. Methods Patients and study design. This 3.5-year, single-center, prospective cohort study conducted at a tertiary health-care center in Tainan, Taiwan. The study design was approved by the research and ethics committee of the hospital (trial registration identifier: NCT , ClincalTrials.gov), and all participants provided written informed consent prior to enrollment. A schematic flow chart of the study protocol is shown in Figure 1. From August 2011 to July 2014, patients who were 20 or more years old; presented with melena, hematochezia, or hematemesis; underwent esophagogastroduodenoscopy because of bleeding peptic ulcers with major stigmata of recent hemorrhage; and had received follow-up until July of 2015 were recruited. The major stigmata of recent hemorrhage were classified as Forrest class Ia, Ib, IIa, and IIb. 13 Patients were treated with endoscopic hemostasis, intravenous high-dose esomeprazole (Nexium; AstraZeneca AB, Södertälje, Sweden) or pantoprazole (Pantoloc; Takeda, Singen, Germany) therapy (80-mg loading and 8 mg/h) for 3 days, and then oral esomeprazole or pantoprazole for 8 to 16 weeks to achieve ulcer healing. Helicobacter pylori (H. pylori) infection was defined with positive results of a rapid urease test (Campylobacter-like organism test; Kimberly-Clark, Draper, UT, USA) before PPI use, a 13 C-urea breath test 2 weeks after cessation of PPIs, or histology. 14 Patients with H. pylori infection received a 7-day course of triple therapy, including 500-mg clarithromycin, 1-g amoxicillin, and 40-mg esomeprazole or pantoprazole twice daily. 15 The successful H. pylori eradication was defined by a negative result of histology or a 13 C-urea breath test performed 4 weeks after cessation of antibiotics. 14 Patients were excluded if they had cancer bleeding or ulcer bleeding due to the presence of a Dieulafoy s lesion or mechanical factors (i.e. gastrostomy tube induced pressure necrosis of the gastric mucosa); died within 8 weeks after initial peptic bleeding episode; had hypersensitivity to esomeprazole, pantoprazole, or any component of the formulation; or had previously participated in the study. In Taiwan, the National Health Insurance program provides a 16-week course of PPIs to treat peptic ulcer disease. Thus, if patients took a PPI for more than 16 weeks after the initial Figure 1 The schematic flow chart of the study design. Consecutive patients with endoscopically confirmed peptic ulcer bleeding were screened. PPI, proton pump inhibitor. Journal of Gastroenterology and Hepatology 33 (2018)

3 Long-term rebleeding in Rockall scores 6 E-H Yang et al. ulcer, they were excluded from the study. The Rockall score, which combines age, presence of shock, comorbidity, and endoscopic features, can predict the risk of rebleeding and mortality within 30 days following peptic ulcer bleeding. 4 The AIMS65 score is made up of albumin, international normalized ratio, mental status, systolic blood pressure, and age; it can predict mortality and length of hospital stay during index hospitalization. 16 The Rockall score and AIMS65 score were calculated for all included patients in order to stratify them into risk groups. Outcome measures for recurrent bleeding. Patients were followed up until July of 2015 to monitor the primary endpoint, recurrent ulcer bleeding that occurred after the first 8 weeks of initial peptic ulcer bleeding. Recurrent ulcer bleeding was defined as a new episode of melena or hematemesis with hemodynamic instability, including systolic blood pressure <90 mmhg, heart rate >120 beats per minute, a drop in hemoglobin level of more than 2 g/dl, or documented to be experiencing peptic ulcer bleeding using esophagogastroduodenoscopy. The follow-up status of patients was determined by regular gastroenterology and other clinic visits, chart record reviews, and/or telephone interviews. 17 Telephone interviews were conducted by study physicians with patients or with patients spouses or first-degree relatives if the patients were dead or unavailable. Patients were assessed for symptoms of recurrent ulcer bleeding, given a medication review, and asked to provide a history of hospitalization and esophagogastroduodenoscopy. Death, hospitalization, or a peptic ulcer bleeding event was recorded by reviewing all the chart records, including clinic, hospital, and emergency room visits, as well as endoscopic findings. Statistical analysis. The estimated long-term rebleeding rates in the low-risk group and in the high-risk group were estimated to be 2.5% and 13%, respectively, and the ratio of the two groups was proposed to be 0.5 (0.33/0.67) based on the results of previous studies. 11,18 With a two-sided α value of 0.05 and a power of 90% (β = 0.10), the total number of patients required was at least 312. Assuming a dropout rate of 15%, 368 patients were needed. The patient characteristics were compared and tested using either a Pearson s χ 2 -test or a Fisher s exact test as appropriate. Continuous variables were categorized to avoid multiplicative errors. A multiple Cox regression analysis with forward selection at P < 0.1 was applied to assess independent risk factors related to recurrent bleeding, and multicollinearity checks were also applied. Low variance inflation factor values were documented among the covariates, and no potential multicollinearity problems were found. There were no hazard ratios that violated the assumption of proportional hazards using ASSESS statement and ph option of SAS PROC PHREG. The log rank test was used to compare Kaplan Meier curves among the study groups. Because patients with Rockall scores 6 had increased risk of mortality, death was a competing risk for recurrence bleeding. A competing-risk regression using the Fine and Gray method was used to calculate cause-specific hazards. Standard software (SPSS v17.0 and SAS v9.4) was used for statistical analyses. All tests were two-tailed, and P values less than 0.05 indicated significant differences. Results Demographic features and patient follow-up. A total of 474 patients with peptic ulcer bleeding were consecutively assessed for eligibility for this study (Fig. 1). One hundred and six patients were excluded: 19 did not meet the inclusion criteria, six declined to participate, 13 had bleeding from gastric cancer and metastatic or other cancers, 24 had protocol violation, 15 had bleeding from esophageal ulcer or Mallory Weiss tears, and 29 died within 8 weeks. The remaining 368 patients were placed in either a Rockall scores 6 group (n = 257) or a Rockall scores <6 group (n = 111) according to their Rockall scores assessed at the first peptic ulcer bleeding episode. The median follow-up was 20.7 months (ranging from 1 to 46.5 months). There were significant differences in the proportion of patient characteristics between the two groups, including factors that were either directly or indirectly associated with the Rockall score. The factors directly relevant to the Rockall score were age 65 years, shock on arrival, comorbidities with cirrhosis, end-stage renal disease with maintenance dialysis, malignant diseases, lung diseases, heart diseases, active disease with nosocomial bleeding, gastric ulcer, and Forrest Ia or Ib lesions. Some factors related to the Rockall score indirectly included bleeding severity with hemoglobin levels <7 g/dl and blood urea nitrogen levels 8.92 μmol/l; comorbidity as prolonged prothrombin time 4 s, serum albumin <35 g/l, serum total bilirubin 51.3 μmol/l, and estimated glomerular filtration rate <30 ml/min; American Society of Anesthesiologists (ASA) physical status classification III; and initial anti-platelet agent use. Other factors were ulcer size 2 cm, H. pylori infection, non-h. pylori, and non-non-steroidal antiinflammatory drug (NSAID) treatment (P < 0.05; Table 1). A total of 334 patients received H. pylori infection survey, and 154 patients were infected. Among them, 71 in the Rockall scores 6 group received H. pylori eradication, but one failed, and 65 in the Rockall scores <6 group received H. pylori eradication and none failed. The proportion of NSAID use at the time of peptic ulcer bleeding was not different between patients with Rockall scores 6 and <6 (43.2% vs. 36.0%, P = 0.2; Table 1). Patients with Rockall scores 6 had higher rebleeding risk during 3.5-year follow-up. During the 3.5-year follow-up, 45 patients in the Rockall scores 6 group (43.2% (95% confidence interval [CI], %)) and eight patients in the Rockall scores <6 group (13.5% [95% CI, %]) had recurrent bleeding. The overall rebleeding rate was 33.2% (95% CI, %). The proportionate cumulative probability of rebleeding was higher in patients with Rockall scores 6 than in those with Rockall scores <6 (10.51 vs 3.63 per 100 person-year, P = 0.004, log rank test; Fig. 2). The Fine and Gray competing-risk regression for death, which was a competing risk occurring instead of the rebleeding event, showed that Rockall scores 6 were still a significant rebleeding factor (cause-specific hazard 2.67, 95% CI, , P = 0.01). After initial peptic ulcer bleeding, there were 100 and 7 patients keeping receiving long-term anti-platelet agents and 15 and Journal of Gastroenterology and Hepatology 33 (2018)

4 E-H Yang et al. Long-term rebleeding in Rockall scores 6 Table 1 The difference in the baseline characteristics between the Rockall scores 6 and <6 groups Parameters mean ± SD; n (%) Rockall scores 6 (n = 257) Rockall scores <6 (n = 111) P value Female 81 (31.5) 27 (24.3) 0.16 Age 65 years 173 (67.3) 32 (28.8) <0.001 Shock on arrival 62 (23.7) 9 (8.1) <0.001 Ulcer characteristics Gastric ulcer 148 (57.6) 42 (37.8) Ulcer 2 cm 55 (21.4) 13 (11.7) 0.03 Forrest Ia or Ib type 70 (27.2) 49 (44.1) Cirrhosis 31 (12.1) 0 <0.001 End-stage renal disease 29 (11.3) 0 <0.001 Malignant diseases 37 (14.4) 3 (2.7) Lung diseases 48 (18.7) 1 (0.9) <0.001 Heart diseases 75 (29.2) 3 (2.7) <0.001 Nosocomial bleeding 53 (20.6) 1 (0.9) <0.001 ASA physical status 174 (67.7) 6 (5.4) <0.001 class III H. pylori infection 86/227 (37.8) 68/107 (63.6) <0.001 NSAID use 111 (43.2) 40 (36.0) 0.20 Non-H. pylori and non- 76 (29.6) 19 (17.1) 0.01 NSAID Initial anti-platelet agent 115 (44.7) 14 (12.6) <0.001 use Hemoglobin levels <7g/ 62 (24.1) 7 (6.3) <0.001 dl Platelet count < / 14 (5.4) 3 (2.7) 0.25 L PT prolong 4 s 31 (12.1) 2 (1.8) aptt prolong 1.5-fold 7 (2.7) Serum albumin <35 g/l 143 (55.6) 34 (30.6) <0.001 Serum total bilirubin 10 (3.9) μmol/l BUN levels 8.92 μmol/l 216 (84.0) 77 (70.0) egfr <30 ml/min 65 (25.3) 0 <0.001 Pearson s chi-squared test and the Fisher s exact test with two-tailed analysis were used as appropriate. Systolic blood pressure <100 mmhg on arrival. The number of patients who received H. pylori infection survey was 334. Activated partial thromboplastin time: normal range s. BUN: normal range μmol/l. Hemoglobin: normal range g/dl. Platelet: normal range /L. Prothrombin time: normal range s. Serum albumin: normal range g/l. Serum total bilirubin: normal range μmol/l. aptt, activated partial thromboplastin time; ASA, American Society of Anesthesiology; BUN, blood urea nitrogen; egfr, estimated glomerular filtration rate; H. pylori, Helicobacter pylori; NSAID: non-steroidal antiinflammatory drug; PT, prothrombin time. patients discontinuing anti-platelet agents, which were given for primary prevention, in the Rockall scores 6 group and the Rockall scores <6 group, respectively. Excluding the patients with long-term anti-platelet agent use, the cumulative probability of rebleeding was still higher in the Rockall scores 6 group than in the Rockall scores <6 group (11.90 vs 3.34 per 100 personyear, P = 0.001, log rank test). There were 53 patients with unknown H. pylori status or without successful H. pylori eradication. Excluding these patients, the cumulative rebleeding risk was still increased in the Rockall scores 6 group than in the Rockall scores <6 group (9.12 vs 3.81 per 100 person-year, P = 0.02, log rank test). Additional independent factors for Rockall scores 6 correlated to rebleeding risk. In the Rockall scores 6 group, 45 patients had rebleeding during the 3.5-year followup. Among them, only 10 cases could be attributed to definite or possible NSAID reuse (n = 6), persistent H. pylori infection due to lost follow-up (n = 3), or both (n = 1). The remaining 35 cases were attributed to unknown etiologies; therefore, a Cox proportional hazard model was further conducted to analyze whether there were additional risk factors for Rockall scores 6 associated with long-term recurrent bleeding. Because there remained 30 patients with unknown H. pylori status, the worst-case and best-case scenario assumed that all and none of them had H. pylori infection, respectively. Accordingly, the rebleeding rates were higher in patients with persistent H. pylori infection than in those without in the worst-case scenario (23.9% vs 16.1%, hazard ratio 2.22 [ ], P = 0.02) but not in the best-case scenario (25.0% vs 17.0%, hazard ratio 1.75 [ ], P = 0.29; Table 2). Furthermore, the multiple Cox regression with forward selection confirmed that activated partial thromboplastin time (aptt) prolonged 1.5-fold, ASA physical status class III, presence of malignant disease, and gastric ulcer were four independent factors (Table 2). Persistent H. pylori infection in the worst-case scenario was not an independent factor. Because the presence of malignant disease is one of the parameters included in the Rockall score, there were three additional independent risk factors used to determine the cumulative rebleeding among the patients for Rockall scores 6. Based on these three additional factors, the patients in the Rockall scores 6 group were divided into two risk subgroups: one with only one or no additional factor subgroup and the more than or equal to any two additional factors subgroup. The proportion of patients with cumulative rebleeding was significantly higher in the more than or equal to any two additional factors subgroup than in the only one or no additional factor subgroup (15.69 vs 7.63 per 100 person-year, P = 0.012, log rank test; Fig. 3). Causes of rebleeding during the 3.5-year follow-up in patients with Rockall scores <6. In the Rockall scores <6 group, eight patients had rebleeding during the 3.5-year follow-up; the possible causes of which were attributed to NSAID reuse (n = 4), H. pylori infection due to false negative results at the initial bleeding episode (n = 2), subtotal gastrectomy-related marginal ulcer recurrence (n = 1), and uncertain cause (n = 1). AIMS65 score cannot predict long-term rebleeding in patients with peptic ulcer bleeding. We further categorized the enrolled patients into an AIMS65 scores 2 group (n = 101) and an AIMS65 scores <2 group (n = 267). During the 3.5-year follow-up, 15 patients in the AIMS65 scores 2 group and 38 patients in the AIMS65 scores <2 group had rebleeding; therefore, there was no significant difference in the cumulative proportion of rebleeding between the AIMS65 scores 2 group Journal of Gastroenterology and Hepatology 33 (2018)

5 Long-term rebleeding in Rockall scores 6 E-H Yang et al. Figure 2 The Kaplan Meier curves demonstrated that the cumulative probability of recurrent bleeding-free during the 3.5-year followup was lower in patients with Rockall scores 6 ( ) than in those with Rockall scores <6 ( ) (P = 0.004, log rank test). Rockall scores < 6; Rockall scores 6; Censored. and the AIMS65 scores <2 group (9.08 per 100 person-year vs 7.86 per 100 person-year, P = 0.601, log rank test; Fig. 4). Discussion This prospective cohort study disclosed that patients with Rockall scores 6 had an increased risk of long-term recurrent peptic ulcer bleeding. The study further illustrated that H. pylori infection and NSAID reuse were two major causes of recurrent peptic ulcer bleeding in patients with Rockall scores <6, but not in those with Rockall scores 6. Nevertheless, aptt prolonged 1.5-fold, ASA physical status class III, and gastric ulcer were three additional factors for patients with Rockall scores 6 to have increased risk of recurrent peptic ulcer bleeding. Helicobacter pylori infection and NSAID use are the major causes not only of peptic ulcer bleeding but also of rebleeding. 19,20 This study reinforced this finding and showed that false-negative tests for H. pylori and NSAID reuse remained the major causes of rebleeding in the Rockall scores <6 group, that is, six in eight patients. However, only 10 in 45 patients in the Rockall scores 6 group had rebleeding, which could be attributed to these two factors. Additionally, persistent H. pylori infection was not an independent factor correlated to rebleeding (Table 2). Moreover, with the declining prevalence of H. pylori infection, the proportion of patients with idiopathic bleeding ulcers has been increasing in the past decade. 21 Importantly, patients with idiopathic bleeding ulcers have increased risk of recurrent ulcer bleeding over the subsequent 1 to 7 years. 22 Therefore, issues explaining the underlying mechanism for the development of idiopathic bleeding ulcers and factors to stratify patients at risk of long-term rebleeding are emerging. 21 Accordingly, a validated prognostic score to risk-stratify patients in a long-term follow-up is required. Our study disclosed that patients with Rockall scores 6 had higher rebleeding rates than those with Rockall scores <6 (10.51 per 100 person-year vs 3.63 per 100 person-year, log rank test, P=0.004). The Rockall scoring system was still shown to be a significant indicator of long-term rebleeding after adjustment for death, a competing risk for rebleeding (cause-specific hazard 2.67, 95% CI, , P = 0.01). Previous studies have used other risk scoring systems, for example, the AIMS65 score, 16 to classify patients. Our study showed that patients with AIMS65 scores either 2 or <2 had similar rebleeding risk (9.08 per 100 person-year vs 7.86 per 100 person-year, log rank test, P = 0.601; Fig. 4). Nevertheless, our study was not designed to test this hypothesis; thus, it might lack the appropriate power to do so. More research is needed to validate the score. This is the first study to validate that the Rockall scoring system can predict long-term risk of recurrent peptic ulcer bleeding. The reasons for this are proposed as follows: The Rockall scoring system is composed of both clinical and endoscopic findings. 4,23 Because our study aimed to recognize high-risk group for rebleeding, all enrolled patients had peptic ulcer with high-risk stigmata at endoscopy, 13 that is, a score of 3 for the endoscopic variables. Moreover, peptic ulcer healing could be anticipated after an 8-week PPI treatment; thus, index endoscopic features should not drive long-term rebleeding rate. Therefore, patients with Rockall scores 6 had a score of 3 at least for the clinical variables, including senility, comorbidity, and shock on arrival. These findings reinforced arguments that the presence of senility and comorbidities is correlated to an increased risk of long-term recurrent peptic ulcer disease and bleeding There are many possible mechanisms of rebleeding in comorbid patients, including 160 Journal of Gastroenterology and Hepatology 33 (2018)

6 E-H Yang et al. Long-term rebleeding in Rockall scores 6 Table 2 The Cox proportional hazard model to analyze factors associated with the cumulative probability of recurrent bleeding during 3.5-year followup in patients with Rockall scores 6 Factors, n (%) Risks of recurrent bleeding Univariable analysis Multivariable analysis With the factor Without the factor Hazard ratio (95% CI) P value Hazard ratio (95% CI) P value Female versus male 17/81 (21.0) versus 28/176 (15.9) 1.50 ( ) 0.19 Age 65 years versus <65 years 35/173 (20.2) versus 10/84 (11.9) 1.78 ( ) 0.11 Shock on arrival versus none 9/61 (14.8) versus 36/196 (18.4) 0.76 ( ) 0.46 Cirrhosis versus none 7/31 (22.6) versus 38/226 (16.8) 1.42 ( ) 0.40 End-stage renal disease 6/29 (20.7) versus 38/228 (17.1) 1.55 ( ) 0.32 Malignant diseases 10/37 (27.0) 35/220 (15.9) 2.57 ( ) ( ) 0.01 Lung diseases 7/48 (14.6) 38/209 (18.2) 0.99 ( ) 0.94 Nosocomial bleeding 8/53 (15.1) 37/204 (18.1) 0.91 ( ) 0.81 ASA physical status class III 37/174 (21.3) 8/83 (9.6) 2.71 ( ) ( ) 0.02 Persistent H. pylori infection Worst-case scenario 11/46(23.9) 34/211 (16.1) 2.22 ( ) 0.02 Best-case scenario 4/16 (25.0) 41/241 (17.0) 1.75 ( ) 0.29 Long-term anti-platelet agent use 15/100 (15.0) 30/157 (19.1) 0.73 ( ) 0.31 Ulcer characteristics Gastric ulcer 31/148 (20.9) 14/109 (12.8) 1.84 ( ) ( ) 0.04 Ulcer 2 cm 11/55 (20.0) 34/202 (16.8) 1.19 ( ) 0.62 Forrest Ia or Ib type 15/70 (21.4) 30/187 (16.0) 1.22 ( ) 0.53 Hemoglobin levels <7 g/dl 10/62 (16.1) 35/195 (17.9) 0.93 ( ) 0.85 Platelet count < /L 3/14 (21.4) 42/243 (17.3) 1.40 ( ) 0.58 PT prolong 4 s 5/31 (16.1) 40/226 (17.7) 1.19 ( ) 0.71 aptt prolong 1.5-fold 2/7 (28.6) 43/250 (17.2) 4.21 ( ) ( ) Serum albumin <35 g/l 30/143 (21.0) 15/114 (13.2) 1.65 ( ) 0.12 Cox proportional hazard model. Systolic blood pressure <100 mmhg on arrival. There remained 30 patients with unknown H. pylori status; thus, the worse-case and best-case scenario assumed that all and none of them had H. pylori infection, respectively. There were 15 patients who discontinued anti-platelet agents after initial peptic ulcer bleeding because anti-platelet agents were given for primary prevention. Activated partial thromboplastin time: normal range s. Hemoglobin: normal range g/dl. Platelet: normal range /L. Prothrombin time: normal range s. Serum albumin: normal range g/l. aptt, activated partial thromboplastin time; ASA, American Society of Anesthesiology; CI, confidence interval; H. pylori, Helicobacter pylori; PT, prothrombin time. Figure 3 The cumulative recurrent bleeding risks during the 3.5-year follow-up stratified according to the Rockall score 6, with more than or equal to any two additional factors ( ) and with only one or no factors ( ). Rockall scores 6 with only one or no additional factor; Rockall scores 6 with any two additional factors; Censored. Journal of Gastroenterology and Hepatology 33 (2018)

7 Long-term rebleeding in Rockall scores 6 E-H Yang et al. Figure 4 The cumulative recurrent bleeding risks during the 3.5-year follow-up between the AIMS65 scores 2 group ( ) and the AIMS65 scores <2 group ( ). AIMS65 scores < 2; AIMS65 scores 2; Censored. decreased mucosal perfusion, impaired hemostasis, malnutrition, and poor oxygenation. 30 Furthermore, this study demonstrated that aptt prolonged 1.5-fold, the ASA classification III, and gastric ulcer were three additional risk factors to predict rebleeding for Rockall scores 6 (Table 2). The aptt level is available to assess the intrinsic pathway of coagulation. 31 The ASA classification is based on the severity of comorbidity. 32 Moreover, the pathophysiology of gastric ulcer is impaired mucosal defense, which is correlated to ischemia, age, or underlying diseases. 33 Previous studies have also shown that patients with idiopathic ulcer have increased prevalence of comorbidities or high-grade ASA classification. 22,34 Accordingly, our study showed that patients with two or more additional factors had higher cumulative rebleeding risk than those with only one or no additional factors (15.69 vs 7.63 per 100 person-year, log rank test, P = 0.012; Fig. 3). Our data thus suggested that once patients obtain a Rockall score 6, the presence of these three additional factors puts them at increased risk of recurrent peptic ulcer bleeding. The study had some limitations. First, it may have recall bias because of our design, in which some patients rebleeding events were documented by telephone interviews. 17 Nevertheless, because recurrent peptic ulcer bleeding is a major event, most patients could remember clearly such episodes. Second, there were patients with unknown or without successful H. pylori eradication. Nevertheless, the cumulative rebleeding risk was still increased in patients with Rockall scores 6, even among those with definitely negative H. pylori status or successful eradication. Thus, the high risk of long-term recurrent bleeding was mainly attributed to high Rockall scores but not untreated H. pylori infection. Third, this study did not validate the findings in an external cohort. Efficient prevention of recurrent ulcer bleeding depends on how a subgroup at risk of recurrent ulcer bleeding is identified. This study was conducted under standardized treatment conditions. Moreover, use of full Rockall scores to serve as a risk predictor is easy and intuitive for clinical practice because full Rockall score is one of the most widely used scoring systems for a long time. 2,3 The implementation of long-term PPI management to reduce rebleeding for certain high-risk patients shall be promising. 35 In conclusion, patients with Rockall scores 6 exhibited higher long-term cumulative recurrent ulcer bleeding rates during a 3.5-year follow up than those with Rockall scores <6. For patients with Rockall scores 6, aptt prolonged 1.5-fold, high-grade ASA physical status class III, and gastric ulcer were three additional factors to indicate increased risk of long-term recurrent peptic ulcer bleeding. Acknowledgments We are grateful to Professor Sheng-Hsiang Lin for providing statistical consulting services from the Biostatistics Consulting Center, National Cheng Kung University Hospital. This study was funded in part by research grants from the Ministry of Science and Technology (National Science Council) of Taiwan (NSC B MY3); Ministry of Health and Welfare of Taiwan (MOHW106-TDU-B ); the National Cheng Kung University Hospital in Tainan, Taiwan (NCKUH , NCKUH , and NCKUEDA10207); and the E-DA Hospital in Kaohsiung, Taiwan (NCKUEDA10207). References 1 Katschinski B, Logan R, Davies J, Faulkner G, Pearson J, Langman M. Prognostic factors in upper gastrointestinal bleeding. Dig. Dis. Sci. 1994; 39: Sung JJ, Chan FK, Chen M et al. Asia-Pacific Working Group consensus on non-variceal upper gastrointestinal bleeding. Gut 2011; 60: Journal of Gastroenterology and Hepatology 33 (2018)

8 E-H Yang et al. Long-term rebleeding in Rockall scores 6 3 Gralnek IM, Dumonceau JM, Kuipers EJ et al. Diagnosis and management of nonvariceal upper gastrointestinal hemorrhage: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: a Rockall TA, Logan RF, Devlin HB, Northfield TC. Risk assessment after acute upper gastrointestinal haemorrhage. Gut 1996; 38: Sanders DS, Carter MJ, Goodchap RJ, Cross SS, Gleeson DC, Lobo AJ. Prospective validation of the Rockall risk scoring system for upper GI hemorrhage in subgroups of patients with varices and peptic ulcers. Am. J. Gastroenterol. 2002; 97: Church NI, Dallal HJ, Masson J et al. Validity of the Rockall scoring system after endoscopic therapy for bleeding peptic ulcer: a prospective cohort study. Gastrointest. Endosc. 2006; 63: Bardhan KD. Is there any acid peptic disease that is refractory to proton pump inhibitors? Aliment. Pharmacol. Ther. 1993; 7(Suppl. 1): discussion Lahiff C, Shields W, Cretu I et al. Upper gastrointestinal bleeding: predictors of risk in a mixed patient group including variceal and nonvariceal haemorrhage. Eur. J. Gastroenterol. Hepatol. 2012; 24: Sheu BS, Wu CY, Wu MS et al. Consensus on control of risky nonvariceal upper gastrointestinal bleeding in Taiwan with National Health Insurance. Biomed. Res. Int. 2014; 2014: Cheng HC, Chang WL, Yeh YC, Chen WY, Tsai YC, Sheu BS. Sevenday intravenous low-dose omeprazole infusion reduces peptic ulcer rebleeding for patients with comorbidities. Gastrointest. Endosc. 2009; 70: Cheng HC, Wu CT, Chang WL, Cheng WC, Chen WY, Sheu BS. Double oral esomeprazole after a 3-day intravenous esomeprazole infusion reduces recurrent peptic ulcer bleeding in high-risk patients: a randomised controlled study. Gut 2014; 63: Trawick EP, Yachimski PS. Management of non-variceal upper gastrointestinal tract hemorrhage: controversies and areas of uncertainty. World J. Gastroenterol. 2012; 18: Gralnek IM, Barkun AN, Bardou M. Management of acute bleeding from a peptic ulcer. N. Engl. J. Med. 2008; 359: Sheu BS, Wu MS, Chiu CT et al. Consensus on the clinical management, screening-to-treat, and surveillance of Helicobacter pylori infection to improve gastric cancer control on a nationwide scale. Helicobacter 2017; 22: e Liou JM, Lin JT, Chang CY et al. Levofloxacin-based and clarithromycin-based triple therapies as first-line and second-like treatments for Helicobacter pylori infection: a randomised comparative trial with crossover design. Gut 2010; 59: Saltzman JR, Tabak YP, Hyett BH, Sun X, Travis AC, Johannes RS. A simple risk score accurately predicts in hospital mortality, length of stay, and cost in acute upper GI bleeding. Gastrointest. Endosc. 2011; 74: Golden DB, Kagey-Sobotka A, Norman PS, Hamilton RG, Lichtenstein LM. Outcomes of allergy to insect stings in children, with and without venom immunotherapy. N. Engl. J. Med. 2004; 351: Hung LC, Ching JY, Sung JJ et al. Long-term outcome of Helicobacter pylori-negative idiopathic bleeding ulcers: a prospective cohort study. Gastroenterology 2005; 128: Malfertheiner P, Chan FK, McColl KE. Peptic ulcer disease. Lancet 2009; 374: Tang RS, Chan FK. Therapeutic management of recurrent peptic ulcer disease. Drugs 2012; 72: Chow DK, Sung JJ. Non-NSAID non-h. pylori ulcer disease. Best Pract. Res. Clin. 2009; 23: Wong GL, Wong VW, Chan Y et al. High incidence of mortality and recurrent bleeding in patients with Helicobacter pylori-negative idiopathic bleeding ulcers. Gastroenterology 2009; 137: Tham TC, James C, Kelly M. Predicting outcome of acute non-variceal upper gastrointestinal haemorrhage without endoscopy using the clinical Rockall Score. Postgrad. Med. J. 2006; 82: van Leerdam ME, Vreeburg EM, Rauws ED et al. Acute upper GI bleeding: did anything change? Time trend analysis of incidence and outcome of acute upper GI bleeding between 1993/1994 and Am. J. Gastroenterol. 2003; 98: Huang KW, Luo JC, Leu HB et al. Chronic obstructive pulmonary disease: an independent risk factor for peptic ulcer bleeding: a nationwide population-based study. Aliment. Pharmacol. Ther. 2012; 35: Luo JC, Leu BV, Hou MC et al. Cirrhotic patients at increased risk of peptic ulcer bleeding: a nationwide population-based cohort study. Aliment. Pharmacol. Ther. 2012; 36: Hsu YC, Lin JT, Chen TT, Wu MS, Wu CY. Long-term risk of recurrent peptic ulcer bleeding in patients with liver cirrhosis: a 10-year nationwide cohort study. Hepatology 2012; 56: Tseng GY, Lin HJ, Fang CT et al. Recurrence of peptic ulcer in uraemic and non-uraemic patients after Helicobacter pylori eradication: a 2-year study. Aliment. Pharmacol. Ther. 2007; 26: Wu CY, Wu MS, Kuo KN, Wang CB, Chen YJ, Lin JT. Long-term peptic ulcer rebleeding risk estimation in patients undergoing haemodialysis: a 10-year nationwide cohort study. Gut 2011; 60: Crooks CJ, West J, Card TR. Comorbidities affect risk of nonvariceal upper gastrointestinal bleeding. Gastroenterology 2013; 144: Kitchens CS. To bleed or not to bleed? Is that the question for the PTT? J. Thromb. Haemost. 2005; 3: Marmo R, Koch M, Cipolletta L et al. Predictive factors of mortality from nonvariceal upper gastrointestinal hemorrhage: a multicenter study. Am. J. Gastroenterol. 2008; 103: Soll AH. Pathogenesis of peptic ulcer and implications for therapy. N. Engl. J. Med. 1990; 322: Chan HL, Wu JC, Chan FK et al. Is non-helicobacter pylori, non- NSAID peptic ulcer a common cause of upper GI bleeding? A prospective study of 977 patients. Gastrointest. Endosc. 2001; 53: Laine L, Jensen DM. Management of patients with ulcer bleeding. Am. J. Gastroenterol. 2012; 107: Journal of Gastroenterology and Hepatology 33 (2018)

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