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1 A prospective, randomized trial of large- versus small-, volume endoscopic injection of epinephrine for peptic ulcer bleeding Hwaideng Lin, MD, FACG,Yu-Hsi Hsieh, MD, Guan-Ying Tseng, MD, Chin-Lin Perng, MD, Full-Young Chang, MD, Shou-Dong Lee, MD, FACG Taiwan, Republic of China Background: Endoscopic injection of epinephrine in the treatment of bleeding peptic ulcer is considered highly effective, safe, inexpensive, and easy to use. However, bieeding recurs in 6% to 36% of patients.the aim of this study was to determine the optimal dose of epinephrine for endoscopic injection in the treatment of patients with bleeding peptic ulcer. Methods: One hundred fifty-six patients with active bleeding or nonbleeding visible vessels were randomized to receive small- (5-10 ml) or large-volume (13-20 ml) Injections of a 1 :10,000 solutlon of epinephrine. Results: The mean volume of epinephrine injected was 16.5 ml (95% CI [15.7, 17.3 ml]) in the large-v6lume group and 8.0 ml (95% CI [7.5,8.4 ml]) in the small-volume group. Initial hemostasis was achieved in all patients studied. The number of episodes of recurrent bleeding was smaller in the large-volume group (12/78,15.4%) compared with the small-volume group (24/78,30.8%, p = 0.037).The volume of blood transfused after entry into the study, duration of hospital stay, numbers of patients requiring urgent surgery, and mortality rates were not statistically different between the 2 groups. Conclusions: Injection of a large volume (>I3 ml) of epinephrine. can reduce the rate of recurrent - bleeding In with high-risk peptic ulcer and is superior to injection of lesser volumes of epinephrine when used to achieve sustained hemostasis. (Gastrointest Endosc 2002;55:615-9.) Although peptic ulcer bleeding ceases sponta- Injection therapy is also effective, safe, relatively neously in 70% to 80% of patients, it can be cata- inexpensive, and easy to use.2 Impressive rates of strophic in the remainder.1 The mortality rate asso- hemostasis have been obtained by using solutions of ciated with such bleeding has been reduced to 2% to various agents such as epinephrine, absolute alco- 6% through the endoscopic use of various methods of hol, hypertonic saline solution, 50% glucose/water, therapy.2 Endoscopic hemostatic techniques are thrombin, and fibrin sealants.3-13 Of these, epinephthus a major advance in the treatment of these rine is the most commonly used agent for endoscopic patients. By reducing both morbidity and mortality, injection. There is a wide range in the volume (2-25 endoscopic therapy has become the treatment of ml) of epinephrine injected in various studies to first choice for ulcer hemorrhage.2 Of the various achieve hemostasis.3-12 The reported rates of initial possible techniques, the efficacy and safety of heat hemostasis obtained with epinephrine injection probe coagulation and multipolar probe electrocoag- range from 80% to 100%.3-12 However, bleeding ulation are well established.1 Hemostatic rates of recurs in 6% to 36% of patients.3-12 The reason for 80% to 95% can be achieved with these modalities. this wide variation in rates of recurrent bleeding is However, bleeding recurs in 10% to 30% of patients.1 unknown. Additionally, the optimal volume of epi- Received May 14, For revision July 12, Accepted nephrine needed to obtain hemostasis has not been September 21,2001. established. Current affiliations: Division of Gastroenterology, Department of The mechanisms that underlie hemostasis in Medicine, VGH-TAIPEI, and the School of Medicine, National response to endoscopic injection of epinephrine are Yang-Ming University, Taipei, Buddhish Tzu Chi Dalin General Hospital, Chia-Yi, and Ton-Yen Geneml Hospital, Hsin-Chu, vasoconstriction, vessel compression, and latel let lbiwaa ROC. aggregation.14~15 Among these, the immediate Presented at Digestive Diseases Week, May 20-23, 2001, in mechanical compression of the bleeding vessel is Atlanta, Georgia (Gastrointest Endosc 2001;53:AB206). thought to be the most important for the initial con- Reprint requests: Hwai-Jeng Lin, MD, Division of trol if bleeding.16,17 Therefore, initial endoscopic Gastroenterology Department of Medicine, VGH-TAIPEI, Shih- Pai Rd, Sec 2, lbipei, Taiwan, 11217, R.O.C. injection of a larger volume of epinephrine is theo- Copyright by the American Society for Gastrointestinal retically better than injection of a smaller volume in Endoscopy /2002/$ patients at high risk for ulcer hemorrhage. The aim doi:lo. 1067/mge of this study was to compare the rates of recurrent VOLUME 55, NO. 6,2002 GASTROINTESTINfi ENDOSCOPY 615

2 H-J Lin, Y-H Hsieh, G-Y Tseng, et al. Peptic ulcer bleeding: large- us. small-volume endoscopic injection of epinephrine ' bleeding after injection of 2 different volumes of epinephrine in patients with ulcer bleeding. In addition, transfusion requirements, need for surgery, mortality, and lengths of hospital stay were compared between large- and small-volume injection groups of patients. PATIENTS AND METHODS Patients hospitalized with hematemesis or melena underwent endoscopy within 24 hours of admission. Those between the ages of 18 and 80 years were eligible for inclusion in the study if they had an ulcer with spurting hemorrhage, an oozing visible vessel, or a non-bleeding visible vessel. For inclusion, patients with a nonbleeding visible vessel had to have one of the following signs of recent bleeding: "coffee ground" material or blood in the stomach andlor duodenum; shock; or an initial hemoglobin level of less than 10 gldl (normal: gldl). By history, no patient had chronic blood loss before study entry. Exclusion criteria were inability or unwillingness to give written informed consent, bleeding tendency (platelet count <50,000/mm3, prothrombin time <30% taking anticoagulant medication), bleeding gastric malignancy, pregnancy, or more than one bleeding source. Possible complications of endoscopic treatment were discussed with the patients and their relatives, and written informed consent was obtained before entry into the trial. The protocol was approved by the Clinical Research Committee of our hospital. This study was a prospective, single-blind, randomized comparative trial. Patients were randomized by using numbered envelopes to 1 of 2 treatment groups according to a randomization table: small-volume epinephrine group or large-volume epinephrine group. The randomization methodology balanced the number of patients in each group and was prepared by a statistician who was not directly involved in the study. Patients were cared for by the investigators and other physicians not involved in the study. A single, experienced gastroenterologist performed all hemostatic treatments. A commercially available endoscope (GIF-XQ240, Olympus Optical Co., Ltd., Tokyo, Japan) and a 4 rnrn, 23 G injector needle (NM-8L, Olympus) were used. In the small-volume injection group, 5 to 10 ml of a 1:10,000 solution of epinephrine were injected around the bleeding site (1 mllinjection at 2 to 3 mm from the point of bleeding). In the large-volume epinephrine group, 13 to 20 ml of a 1:10,000 solution of epinephrine were injected around the bleeding site. During injection, electrocardiographic monitoring was used to detect arrhythmias. Initial hemostasis was defined as cessation of hemorrhage for 5 minutes after endoscopic treatment. The injection treatment was considered to have failed if hemostasis was not obti?iined after injection of 10 ml of the epinephrine solution in the small-injection group and after injection of 20 ml in the large-volume group. These patients underwent alternative endoscopic treatments or surgery. Recurrent bleeding was suspected if fresh blood was found in the stomach 6 hours after entry into the study; if vital signs were unstable; or if there was continued melena or bloody stools, or hematemesis. When there was a suspicion of recurrent bleeding, the patient underwent emergency endoscopy. If there was active bleeding or a fresh blood clot was found at the ulcer base, recurrence of bleeding was regarded as ~~~firmed. For ethical reasons, treatment regimens were discussed with patients in whom initial hemostasis was not. achieved or who had evidence of recurrent bleeding. The therapeutic options included a second injection of epi- nephrine, heat probe thermocoagulation, and surgery. One biopsy from the gastric antrum and one from the gastric body were obtained after cessation of bleeding, and the presence or absence of Helicobacter pylori infection was determined by means of a rapid urease test. Vital signs were monitored hourly for the first 12 hours, every 2 hours for the second 12 hours, every 4 hours for the following 24 hours until they became stable, and then 4 times daily. A nasogastric tube was inserted and maintained for 24 hours after treatment. Hemoglobin level and hematocrit were determined at least once daily, and blood transhsions were given to maintain the hemoglobin concentration at greater than 10 g/l. Omeprazole (40 mg) was given intravenously every 6 hours for 3 days, then orally (20 mglday) for 2 months. If the rapid urease test was positive, treatment for 1 week with triple drug therapy (omeprazole + clarithromycin + amoxycillin) was initiated within 24 hours of enrollment. Endoscopy was performed 72 hours after cessation of bleeding by the same endoscopist who performed the initial treatment. If there was no evidence of hemorrhage and no clot in the ulcer base, the patient was discharged and followed up with an endoscopy 2 to 3 months later. Shock was defined as systolic pressure less than 100 mm Hg and pulse rate greater than 100 beatslmin accompanied by cold skin, sweating, pallor, and oliguria. Ultimate hemostasis was defined as the lack of recurrent bleeding for 14 days after treatment. The outcomes assessed were initial recurrence of bleeding, blood transfusion requirement, surgery, length of hospital stay, and mortality. Outcomes were assessed within 14 days after enrollment in the study. Statistical analysis The sample size was calculated based on previous experience with injection of a small volume of epinephrine, which had a rate of recurrent bleeding of 36%.378 If the rate of recurrent bleeding with injection of the larger volume of epinephrine was taken as 14.5%, a sample size of 76 was required for each group to achieve a statistical power of 90% at 10% type I error. The Mann-Whitney rank sum test was used for the analysis of nonparametric quantitative data (age, volume of blood transfusion, volume of epinephrine injection, ulcer size, hemoglobin, and length of hospital stay). Unless otherwise indicated, values are expressed as mean (SD). The chi-square test, with or without Yates correction, and the Fisher exact test were used when appropriate to compare the location of bleeding, endoscopic findings, gastric contents, number of patients with H pylori infection, shock, comorbid illness, hemostasis, emergency 616 GASTROINTESTINAL ENDOSCOPY VOLUME 55, NO. 6,2002

3 Peptic ulcer bleeding: large- vs. small-volume endoscopic injection of epinephrine H- J Lin, Y-H Hsieh, G-Y Tseng, et al. Table 1. Clinical variables of patients at study entry Age (mean, y) Gender (ME') Locations of bleeding ulcers Stomach Duodenum Stoma Endoscopic findings Spurting Oozing visible vessel Nonbleeding visible vessel Gastric contents Blood Coffee grounds Clear Positive H pylori Shock Medical illness Small-volume Large-volume epinephrine epinephrine n = 78 n = 78 Table 2. Results of endoscopic therapy Small-volume Large-volume epinephrine epinephrine n = 78 n = 78 Volume injected 8.0( ) 16.5 [15.7, 17.31* Volume blood transfused 885 ml 734 ml after entry [558, [472, 995]* Initial hemostasis 78 (100%) 78 (100%) Recurrent bleeding 24 (30.8%) 12 (15.4%)t Spurting$ 6 (7.7%) 3 (3.8%) Oozing visible vessel* 7 (9%) 4 (5.1%) Nonbleeding visible vessel* 11 (14.1%) 5 (6.4%) Emergency surgery 2 (2.6%) 2 (2.6%) Stay in hospital (d) Deaths from bleeding 0 (0%) 0 (0%) *Mean (95% CI). tp = $Stigmata at entry into the trial. 30.8%; p = 0.037). The mean interval from initial Mean hemoglobin (g/l) hemostasis to an episode of recurrent bleeding was Mean ulcer size (cm) days (3.7) in the small-volume group and 3 days p > 0.05 for all variables between the two groups. (3.7) in the large-volume group (p = 0.68). Of the 24 patients in the small-volume injection operation, and mortality between the 2 groups. A p value group who had recurrent bleeding, 8 were treated a of ~0.05 was considered significant. second time by injection of epinephrine (ultimate RESULTS hemostasis achieved in 6 whereas 2 required heat probe coagulation); 12 underwent heat probe coagu- A total of 944 patients whose main symptoms lation (ultimate hemostasis achieved in 12); 2 were were hematemesis, melena, or both, presented to the treated with supportive measures (ultimate hemoemergency department between September 1999 stasis achieved in both); and, 2 underwent surgery and June A total of 840 patients underwent and recovered uneventfully. endoscopy within 12 hours of arrival at the emer- Of the 12 patients in the large-volume injection gency department; 720 had peptic ulcers. Peptic group in whom bleeding recurred, 9 underwent heat ulcers with spurting hemorrhage, oozing visible ves- probe coagulation (ultimate hemostasis achieved in sel, or nonbleeding visible vessel were found in 168 9); 1 was treated with supportive measures alone patients. Twelve patients were excluded for the fol- (with ultimate hemostasis); and 2 had surgery and lowing reasons: no informed consent (n = 61, bleed- recovered uneventfully. ing diathesis (n = 2), gastric malignancy (n = 21, and There was no death from peptic ulcer bleeding in lack of cooperation (n = 2). There were 156 patients either group. However, 4 patients died of unrelated illenrolled in the study, 78 in each group. The 2 groups ness in the large-volume group (2 pneumonia, 1 terwere well matched for factors that could potentially minal lung cancer, 1 urinary tract infection with sepaffect outcome (Table 1). The numbers of patients sis) and 6 died in the small-volume epinephrine group with comorbid illness were similar between the (3 decompensated liver cirrhosis, 1 urinary tract infecgroups (including 6 with cirrhosis in the small-vol- tion with sepsis, 1 uremia, 1 biliary tract infection ume group and 5 with cirrhosis in the large-volume with sepsis). The volume of blood transfused, duration group). ~i history, no patient had chronic blood loss of hospital stay, number of operations, and number of before entry into the study. deaths were not statistically different between the 2 Thg clinical outcomes for the patients studied are groups (Table 2). At 1 week after endoscopic treatshown in Table 2. The volume of epinephrine inject- ment, there were no complications in either group ed was higher in the large-volume group (mean 16.5 including perforation of a peptic ulcer, aspiration ml, range ml; vs. 8.0 ml, 95% CI [7.5,8.4 pneumonia, cardiac complications, and fever. ml]). ~nitial hemostasis was achieved in all patients in both groups. There were fewer episodes of recur- DISCUSSION rent bleeding in the large-volume group (12178, Patients with actively bleeding peptic ulcer or pep- 15.4%) than in the small-volume group (24178, tic ulcer with nonbleeding vessel were enrolled in this VOLUME 55, NO. 6,2002 GASTROINTESTINAL ENDOSCOPY 617

4 H-J Lin, Y-H Hsieh, G-Y Tseng, et al. Peptic ulcer bleeding: large- vs. small-volume endoscopic injection of epinephrine prospective study. Previous studies have confirmed that conservative management of patients with these stigmata is associated with a high risk of uncontrolled bleeding and recurrent bleeding.1 Consequently, it was unethical to include a control in the current study. Endoscopic findings were interpreted and endoscopic treatment performed by an experienced specialist endoscopist to minimize bias, although the determination of recurrent bleeding by endoscopic criteria was subjective. The mortality rate for peptic ulcer hemorrhage can be decreased with better hospital care including combined medical and surgical approaches and aggressive endoscopic treatment.192 Recurrence of bleeding in patients with peptic ulcer hemorrhage has been consistently described as the most important prognostic factor.18,lg If it can be prevented, the mortality rate can potentially be reduced. Although a high rate of initial hemostasis can be achieved with endoscopic injection of epinephrine, a wide range of rates of recurrent bleeding after therapy are reported.3-12 Thus far, there is no proven explanation for this phenomenon. Mechanical compression of the bleeding vessel is the most important factor in the initial control of bleeding However, the hemostatic effect may be prolonged by a combination of tamponade and vasoconstriction,20 and thus injection of a larger volume of epinephrine may be beneficial in preventing recurrent bleeding through these same mechanisms. In the present study, the rate of recurrent bleeding was significantly lower when a larger volume (>I3 ml) of epinephrine was injected (12178 patients, 15.4%; vs patients, 30.8%; p < 0.05). Because submucosally injected epinephrine does not damage tissue or have appreciable systemic effects, large volumes can be used with a low risk of complication.21 To date, only a single case of hypertension and ventricular tachycardia after epinephrine injection of a Mallory-Weiss tear has been reported.22 Sung et al.23 confirm that although the plasma level of epinephrine rises 4 to 5 times above basal level immediately after injection, cardiovascular complications are not commonly observed. It has been confirmed that endoscopic injection of epinephrine is safe.3-12 An intragastric ph of greater than 6 has been shown to lower the risk of recurrent bleeding in paqents with bleeding peptic ulcers.24 Therefore, a high dose infusion of omeprazole reduces the risk of recurrent bleeding after successful endoscopic therapy.25,26 In the current study, the same intravenous dose of omeprazole was used as in a prior study,26 but higher rates of recurrent bleeding were noted. Differences in the therapeutic modalities applied for bleeding may explain the differences in rates of 618 GASTROINTESTINAL ENDOSCOPY recurrent bleeding in these studies; heat probe coagulation or multipolar electrocoagulation were used in the previous studies In addition, thermocoagulation was successful in controlling recurrent bleeding when epinephrine injection failed to do so in patients in the current study. Combination therapy (injection with contact thermocoagulation, electrocoagulation, or laser photocoagulation) has been shown to be superior to injection therapy alone.8,11,27 However, it is often difficult to achieve hemostasis with contact devices or the application of laser emergency when visualization of the bleeding site is unsatisfactory (e.g., massive bleeding in a deformed duodenal bulb). In addition, these methods may not be available in rural hospitals. Therefore, epinephrine injection is frequently used as the first therapeutic modality for peptic ulcer bleeding. The aim of this study was to determine the volume of injected epinephrine that is optimal for arresting peptic ulcer bleeding. Consequently, use of a contact probe was not included. The distribution of comorbid illness (number and severity) was similar in the 2 treatment groups in the current study. Therefore, the differences in outcome after endoscopic therapy are unlikely to have been influenced by the presence of comorbid illness. Some factors (e.g., ulcer size, active bleeding, shock, ulcer location) can be linked to the failure of injection therapy These were also similar between the 2 groups in the present study. Length of hospital stay, numbers of patients who underwent surgery, and mortality were similar for the 2 groups. This may be due to the early detection of recurrent bleeding and the aggressive endoscopic therapy for such bleeding, thus minimizing the difference with respect to these outcomes between the 2 groups. In conclusion, injection of a large volume (>I3 ml) of a 1: 10,000 solution of epinephrine can reduce the rate of recurrent bleeding in patients with peptic ulcers at high risk of bleeding, and is superior to injection of lesser volumes when used to achieve sustained hemostasis. REFERENCES 1. Consensus Development Panel. Consensus statement on therapeutic endoscopy and bleeding ulcers. Gastrointest Endosc 1990;36:S Kubba AK, Palmer KR. Role of endoscopic injection therapy in the treatment of bleeding ulcer. Br J Surg 1996;83: Lin, HJ, Perng CL, Lee SD. Is sclerosant injection mandatory after an epinephrine injection for arrest of peptic ulcer hemorrhage? A prospective, randomized, comparative study Gut 1993;34: Lin HJ, Perng CL, Lee FY, Chan CY, Huang ZC, Lee SD, Lee CH. Endoscopic injection for arrest of peptic ulcer hemorrhage: final results of a prospective, randomized comparative trial. Gastrointest Endosc 1993;39:15-9. VOLUME 55, NO. 6,2002

5 Peptic ulcer bleeding: large- vs. small-volume endoscopic injection of epinephrine H- J Lin, Y-H Hsieh, G-Y Tseng, et al. 5. Choudari CP, Palmer KR. Endoscopic injection therapy for bleeding peptic ulcer; a comparison of epinephrine alone with epinephrine plus ethanolamine oleate. Gut 1994;35: Chung SCS, Leong HT, Chan ACW, Lau JYW, Yung MY, Leung JWC, et al. Epinephrine or epinephrine plus alcohol for injection of bleeding ulcers: a prospective randomised trial. Gastrointest Endosc 1996;43: Kubba AK, Murphy W, Palmer KR. Endoscopic injection for bleeding peptic ulcer: a comparison of epinephrine alone with epinephrine plus human thrombin. Gastroenterology 1996; 111: Lin HJ, Tseng GY, Perng CL, Lee FY, Chang FY, Lee SD. Comparison of epinephrine injection and bipolar electrocoagulation for the arrest of peptic ulcer bleeding. Gut 1999;44: Villanueva C, Balanz6 J, Torras X, Soriano G, Srinz S, Vilardell F. Value of second look endoscopy after injection therapy for bleeding peptic ulcer: a prospective and randomized trial. Gastrointest Endosc 1994;40: Carter R, Anderson JR. Randomized trial of epinephrine injection and laser photocoagulation in the control of haemorrhage from peptic ulcer. Br J Surg 1994;81: Chung SCS, Lau JYW, Sung JJY, Chan ACW, Lai CW, Ng EKW, et al. Randomised comparison between adrenalin injection alone and adrenaline injection plus heat probe treatment for actively bleeding ulcers. BMJ 1997;3 14: Lai KH, Peng SN, Guo WS, Lee FY, Chang FY, Malik U, et al. Endoscopic injection for the treatment of bleeding ulcers: local tamponade or drug effect. Endoscopy 1994:26: Rutgeerts P, Rauws E, Wara P, Swain P, Hoos A, Solleder E, et al. Randomised trial of single and repeated fibrin glue compared with injection of polidocanol in treatment of bleeding peptic ulcer Lancet 1997;350: Chung SCS, Leung FW, Leung JWC. Is vasoconstriction the mechanism of hemostasis in bleeding ulcers with adrenalin? A study using reflectance spectrophotometry [abstract]. Gastrointest Endosc 1988;34:A O'Brien JR. Some effects of adrenaline and anti-adrenaline compounds on platelets in vitro and in vivo. Nature 1963;200: Rutgeerts P, Geboes K, Vantrappen G. Tissue damage produced by hemostatic injections [abstract]. Gastrointest Endosc 1986;32: Randell GM, Jensen DM, Hirabayashi K, Machicado GA. Controlled study of different sclerosing agents for coagulation of canine gut arteries. Gastroenterology 1989;96: Allan R, Dykes P. A study of the factors influencing mortality rates from gastrointestinal haemorrhage QJM 1976;45: Turner IB, Jones M, Piper DW. Factors influencing mortality from bleeding peptic ulcers. Scand J Gastroenterol 1991;26: Pinkas H, McAllister E, Norman J, Robison B, Brady PG, Dawson PJ. Prolonged evaluation of epinephrine and normal saline solution injections in an acute ulcer model with a single bleeding artery. Gastrointest Endosc 1995;42: Rutgeerts P, Geboes K, Vantrappen G. Experimental studies of injection therapy for severe nonvariceal bleeding in dogs. Gastroenterology 1989;97: Stevens PD, Lebwohl 0. Hypertensive emergency and ventricular tachycardia after endoscopic epinephrine injection of a Mallory Weiss tear. Gastrointest Endosc 1994;40: Sung JY, Chung SCS, Low JM, Leung JWC, Li AKC, Cocks R, et al. Systemic absorption of epinephrine after endoscopic submucosal injection in patients with bleeding peptic ulcers. Gastrointest Endosc 1993;39: Green FW, Kaplan MM, Cutis LE, Levine PH. Effect of acid and pepsin on blood coagulation and platelet aggregation. Gastroenterology 1978;74: Lau JYW, Sung JJY, Lee KKC, Yung MY, Wong SKH, Wu JCY, et al. Effect of intravenous omeprazole on recurrent bleeding after endoscopic treatment of bleeding peptic ulcers. N Engl J Med 2000;343: Lin HJ, Lo WC, Lee FY, Perng CL, Tseng GY. A prospective randomized comparative trial showing that omeprazole prevents rebleeding in patients with bleeding peptic ulcer after successful endoscopic therapy. Arch Int Med 1998;158: Loizou LA, Brown SG. Endoscopic treatment for bleeding peptic ulcers: randomized comparison of adrenaline injection and adrenaline injection 1 Nd:YAG laser photocoagulation. Gut 1991;32: Brullet E, Calvet X, Campo R, Rue M, Catot L, Donoso L. Factors predicting failure of endoscopic injection therapy in bleeding duodenal ulcer. Gastrointest Endosc 1996;43: Brullet E, Campo R, Calvet X, Coroleu D, Rivero E, Sim-Deu J. Factors related to the failure of endoscopic injection therapy for bleeding gastric ulcer. Gut 1996;39: VOLUME 55, NO. 6,2002 GASTROINTESTINU ENDOSCOPY 619

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