Non-Variceal Upper GI Hemorrhage: Doorway to Diagnosis

Non-Variceal Upper GI Hemorrhage: Doorway to Diagnosis

Non-Variceal Upper GI Hemorrhage: Doorway to Diagnosis Jake Matlock, MD, and Martin L. Freeman, MD Endoscopy plays a central role in diagnosis and the...

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Non-Variceal Upper GI Hemorrhage: Doorway to Diagnosis Jake Matlock, MD, and Martin L. Freeman, MD Endoscopy plays a central role in diagnosis and therapy of upper gastrointestinal bleeding. Safe and effective endoscopy depends on appropriate pre-procedure assessment and management. The initial evaluation of patients with severe upper gastrointestinal hemmorrhage depends upon effective communication between the Gastroenterologist and Intensivist. Rapid assessment of the patient, including focused history, vitals, and physical exam should be followed by initiation of resuscitation with well defined endpoints. Medical therapy aimed at correction of coagulopathy, elevation of gastric pH, and lowering portal pressure is appropriate during resuscitation and stabilization. Plans for airway management, patient monitoring, and management of complications must be in place prior to endoscopy, and all personnel involved in endoscopy in active gastrointestinal bleeding should be familiar with both the equipment and techniques which may be required to localize and control bleeding lesions. Tech Gastrointest Endosc 7:112-117 © 2005 Elsevier Inc. All rights reserved. KEYWORDS gastrointestinal hemorrhage, endoscopy, resuscitation

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ndoscopy can be used to identify the exact cause and site of acute upper gastrointestinal bleeding in over 95% of cases. Findings at urgent endoscopy can contribute to precise prediction of rebleeding, guide triage of patients, and in most cases lead to definitive endoscopic therapy or direct surgical management. Emergency endoscopy in the acute GI bleeder can be technically difficult, risky to the patient, and require close coordination with intensive care physicians and nurses. Appropriate assessment and preparation of the patient before endoscopic intervention is essential to minimize the risk of subsequent complications.

Initial Approach to the Patient with Upper GI Hemorrhage Before proceeding to endoscopy, it is important that the patient is thoroughly evaluated, resuscitated, and triaged to the appropriate unit of the hospital. For patients admitted through the emergency department with signs of severe hemorrhage, such as frank hematemesis, hypotension, or endorgan dysfunction, intensive care unit admission for medical stabilization is appropriate. The development of new onset Division of Gastroenterology, University of Minnesota/Hennepin County Medical Center, Minneapolis, MN. Address reprint requests to Martin L. Freeman, MD, Professor of Medicine, University of Minnesota, Division of Gastroenterology Hennepin County Medical Center, 701 Park Avenue, Minneapolis, MN 55415. E-mail: [email protected]

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1096-2883/05/$-see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.tgie.2005.04.006

upper gastrointestinal bleeding in those already in the hospital will likewise often require transfer to the intensive care unit for ongoing management. It must be emphasized that clinical factors such as age greater than 65 years, medical comorbidities, shock, initial hemoglobin level, transfusion requirement, and blood on rectal examination or in nasogastric aspirate are at least as important in determining rebleeding risk and outcome as are endoscopic findings.1,2 Thus, it is reasonable to admit to the ICU all severe acute GI bleeders and those with lesser degrees of bleeding if they are elderly or have significant medical comorbidities. The major causes of mortality, including bleeding, underlying comorbid disease, and postoperative complications, can be best managed in the intensive care setting. Because of their poor tolerance of further bleeding, it is particularly advisable to admit the elderly or compromised patient who has had even a minor bleed to an ICU.

ICU Evaluation of Severe Upper GI Bleeding The initial approach to the upper GI bleeder in the ICU requires coordination between the intensivist and gastroenterologist to assure rapid assessment of the severity of the hemorrhage, followed by resuscitation, brief history and physical examination, and planning for anticipated intervention. Vital signs should be taken, including blood pressure and pulse, with evaluation for postural changes. Severe GI bleed-

Non-variceal upper GI hemorrhage ing is usually defined as the association of bleeding with shock or refractory orthostatic hypotension, ongoing hematemesis, a fall in hematocrit of 6% to 8% or of hemoglobin of 2 to 3 g/dL from baseline, or a transfusion requirement exceeding two units of packed red blood cells within 12 hours. Severe and/or persistent bleeding occurs in approximately 20% to 25% of patients with upper gastrointestinal bleeding.2 This subgroup accounts for the majority of complications, urgent surgery, and mortality, which are most often due to underlying comorbid disease, further bleeding, or surgical complications. Assessment of the amount or volume of blood loss must take into account the clinical presentation, hemodynamic status, and level of hemoglobin or hematocrit. At the time of presentation, hemodynamic status and ongoing hematemesis are the best indicators of severity of bleeding, as more than 24 hours is required for equilibration of hemoglobin after acute blood loss. The medical history should focus on presenting symptoms, prior episodes of gastrointestinal bleeding, recent medications, and cardiopulmonary comorbidities, as these factors may provide clues to the etiology of the bleeding and allow for assessment of risk in the peri-procedural period. A brief physical examination must include examination of the neck veins for jugular venous pressure, chest for signs of congestive heart failure, and abdomen for presence or absence of bowel sounds and tenderness. In patients with significant abdominal pain or tenderness, an abdominal series (which includes flat-plate and upright x-ray of the abdomen and upright of the chest) should be obtained to rule out viscus perforation. Blood should be sent for type and crossmatch, hemoglobin, hematocrit, prothrombin time, platelet count, electrolytes, urea nitrogen, creatinine, and liver chemistries. An electrocardiogram is indicated for the elderly, for patients with cardiac disease, and for anyone who presents with shock or chest pain. The rapid assessment of patients with severe upper GI bleeding may provide clues to the etiology of their blood loss. Peptic ulcers are the most common cause of upper GI bleeding, and abdominal tenderness supports this diagnosis with guarding or rigidity suggesting the possibility of concomitant perforation. However, the presence of liver disease in the medical history, with attendant physical examination findings of scleral icterus, jaundice, splenomegaly, spider angioectasiae, palmar erythema, or ascites may suggest esophagogastric varices as the etiology for GI bleeding. A history of retching before bleeding is common, though not universal in Mallory–Weiss tears. The presence of a large vertical midline scar should never go unexplained, as a history of aortic aneurysm repair or aortoiliac bypass graphs mandates exclusion of an aorto-enteric fistula.

Resuscitation Resuscitation should begin concurrently with patient assessment. Intravenous access must be obtained immediately and, in patients with unstable vital signs, intravenous fluid should begin at once. Large-bore peripheral intravenous lines, 14 to 18 gauge, provide minimal resistance to flow, allowing for rapid infusion of fluids and expansion of plasma volume. Although one intravenous line may suffice for patients with relatively small volume bleeds, a minimum of two intrave-

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Figure 1 Two methods for airway protection during endoscopy for severe upper gastrointestinal bleeding: esophageal overtube (left) and endotracheal intubation (right). (Color version of figure is available online.)

nous lines should be started in patients with signs of severe bleeding so that adequate volume can be administered. If the patient has severe or protracted hypotension, central venous access is often required to assure maintenance of vascular access, to allow for monitoring of central venous pressure with administration of large fluid volumes, and to allow administration of vasoactive medications. Endpoints of resuscitation include: (1) normalization of blood pressure, (2) restoration of hemoglobin concentration to desirable level (should be maintained ⬎10 g/dL in older patients and those with significant cardiopulmonary comorbidity, but can be allowed to fall lower in younger, healthier patients), (3) initiation of correction of any coagulopathy or thrombocytopenia, and (4) correction of end-organ dysfunction. Expeditious resuscitation and preparation for endoscopy is critical, as early endoscopy (within 24 hours of hospital admission) allows triage of stable patients with low-risk endoscopic findings to floor or outpatient management,3 as well as improved outcomes for those with high-risk endoscopic findings.2 Endoscopy should be undertaken without delay once resuscitation is complete, particularly in those who are elderly or have medical comorbidities, as these patients may severely deteriorate if they are allowed to rebleed after initial stabilization. Although endoscopy may be occasionally useful before achieving effective hemodynamic resuscitation (eg, for hemostasis in severe bleeders unable to be fully resuscitated despite vigorous measures, for identification and direction of surgical or radiological management in torrential bleeding or unusual lesions such as suspected aorto-enteric fistula or hemobilia), as many endpoints of resuscitation as possible should be met before endoscopic intervention to minimize peri-procedural risk.

Airway Protection Airway protection should be considered before endoscopy in patients who have ongoing hematemesis, are uncooperative

114 or mentally obtunded, are hemodynamically unstable despite vigorous resuscitation, and in those in whom immediate surgery is anticipated. Aspiration pneumonia may occur in up to 20% of patients with an unprotected airway.4 Airway protection traditionally consists of endotracheal intubation, but an alternative approach suitable for some patients during endoscopy is use of a short (25 cm), flexible esophageal overtube (Fig. 1). Endotracheal intubation allows deep sedation and/or paralysis of the patient and prolonged airway protection for up to a week or more. Early prospective data suggested that endotracheal intubation may prevent the development of new infiltrates on chest radiograph following endoscopy in patients with severe upper gastrointestinal bleeding.4 However, intubation has the potential disadvantage that the patient will be on a ventilator for at least 24 to 48 hours and risk ventilator-acquired pneumonia. Furthermore, emergency endotracheal intubation in the patient with active upper GI bleeding can be challenging and has an attendant risk of acute aspiration of blood. More recent retrospective data involving larger numbers of patients failed to demonstrate a significant difference in the rates of aspiration pneumonia or cardiopulmonary events in patients with and without prophylactic endotracheal intubation.5 However, these same data do suggest a trend toward decreased occurrence of massive, fatal aspiration events at the time of endoscopy. Esophageal overtubes are useful substitutes for endotracheal intubation in cooperative patients, with adequate blood pressure to allow deeper than moderate sedation, and in whom airway protection is required only for the duration of the endoscopy. We usually place an overtube early in the endoscopy if blood is seen to reflux up the esophagus during initial inspection. Although practices vary, we do not allow patients to reflux blood out the esophagus and into the pharynx during therapeutic or prolonged endoscopy, preferring to interrupt the procedure and establish airway protection as quickly as possible, by either available method.

The Role of Nasogastric Aspiration Upper GI hemorrhage may present with hematemesis (either fresh or “coffee ground” blood), melena (black tarry stools), hematochezia (red or maroon blood either alone or mixed with stool), syncope (with or without overt bleeding), or any combination of these. Often, the clinical presentation does not clearly point to an upper tract source, particularly in patients presenting with hematochezia, melena, or syncope. Although a negative nasogastric aspirate does not rule out an upper tract source, the returns from nasogastric aspiration can help to risk stratify patients. Canadian registry data (RUGBE) indicate that a bloody nasogastric aspirate predicts high-risk lesions (active bleeding or visible vessel) at the time of endoscopy with high specificity (75.8%), and that a clear nasogastric aspirate, while unable to rule out an upper tract source, predicts the presence of a low risk endoscopic lesion with high specificity (93.5%).6 However, a clear nasogastric aspirate should never be taken as a substitute for upper endoscopy. Although it is reasonable to undertake colonoscopy without upper endoscopy in hemodynamically stable pa-

J. Matlock and M.L. Freeman Table 1 Checklist before Emergency Endoscopy for Acute Upper Gastrointestinal Bleeding 1. Adequate intravenous access and volume resuscitation 2. Two or more assistants present 3. Airway protection -oral suction ready -consider esophageal overtube or endotracheal intubation 4. Monitoring -pulse oximetry -automated blood pressure -electrocardiogram 5. Endoscopic accessories and therapeutic devices ready and tested 6. Surgical consultation considered

tients with ongoing hematochezia and a nasogastric aspirate showing clear bile, upper endoscopy is indicated before colonoscopy in all patients with severe upper GI bleeding, regardless of stool character. Upper endoscopy is quick, easy, and can be performed without the delay required for a bowel prep; it is highly accurate in diagnosing or excluding upper tract sources of bleeding; and up to 10% of patients presenting with severe hematochezia alone have upper GI sources. Although gastric lavage has been advocated for clearance of the upper tract of obscuring blood, few data exist to support its routine use, and we feel that the additional risk of aspiration with large volume lavage of the stomach is unwarranted unless initial endoscopic examination is inadequate because of large volumes of blood or fluid. When necessary, a large-bore (36 Fr. or larger) Edlich tube (orogastric tube) inserted through an esophageal overtube provides an adequate lumen for clearance of most clots while providing some protection against pulmonary aspiration.

Medication Administration Prior to Endoscopy The focus of medical management of severe upper GI bleeding in the preendoscopy period should certainly be restoration of volume status and stabilization of hemodynamics. While vascular access and administration of fluids and blood products are the most important aspects of this management, a few medications have an adjunctive role in preparation of patients for endoscopy. The most obvious and widely used of these medications are the proton pump inhibitors (PPI), which through elevation of intragastric pH may help to stabilize clot in the upper tract and decrease the risk of rebleeding.2 In patients with severe upper gastrointestinal bleeding, the presence of blood and clots in the upper tract may interfere with absorption of orally administered medications, mandating the use of an intravenous PPI. Infusion of octreotide controls bleeding in up to 90% of portal hypertensive or variceal bleeds, and has been shown to be equivalent to emergency sclerotherapy, allowing time for more effective resuscitation and creating a more controlled environment for endoscopic intervention.7 Bolus administration of erythromycin before endoscopy has been advocated for clearance of blood from the stomach

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Figure 2 Therapeutic upper endoscope with two working channels and an accessory irrigation channel. Reprinted with permission. Adapted from Freeman.12

before upper endoscopy in patients with severe GI bleeding. Erythromycin induces rapid gastric emptying through its action on the motilin receptor. When infused (250 mg) 20 to 30 minutes before endoscopy, erythromycin decreases the duration of endoscopy, increases the quality of examination, and decreases the need for repeat endoscopy.8,9

Patient Preparation, Sedation, and Monitoring In addition to providing the ideal setting for resuscitation, the intensive care unit is the appropriate setting for urgent endoscopy in patients with severe acute upper GI bleeding. Deterioration can be sudden, and close patient monitoring and support are essential. Endoscopy should not be undertaken until the adequate preparations have been performed (see Table 1). At least two support personnel should be available to assist, so that the endoscopist can concentrate on the technical performance of the procedure. One assistant at the head of the bed is primarily responsible for patient care and monitoring, while the other assistant sets up and handles accessory devices. As aspiration is the most common complication of endoscopy in severe upper GI bleeding, close attention should be paid to airway protection. As discussed above, endotracheal intubation should be considered in all patients, particularly those with altered mental status or massive bleeding. At the very least, diagnostic endoscopy in the GI bleeder should never be undertaken until oral suction is set up, turned on, and the assistant at the head of the bed has the suction catheter placed near the patient’s mouth, ready to aspirate any secretions or regurgitated blood. Monitoring equipment, including the electrocardiograph monitor, automatic blood pressure monitor, and pulse oximetry should be functioning and visible to both the endoscopist and the assistant responsible for patient care and monitoring. The apparently resuscitated and stable patient can quickly be converted to hemodynamic or cardiorespiratory instability through the vasodepressor and respiratory-depressant effects of both benzodiazepines and narcotics. Both classes of drugs may exacerbate hypotension in volume-depleted pa-

115 tients and increase the risk of aspiration through alterations in mental status, decreased gag reflex, and respiratory depression. If motility control is necessary, particularly to examine the duodenum, glucagon can be administered IV in increments of 0.2 to 0.4 mg. In much the same way that resuscitation should be a collaborative effort between the gastroenterologist and the intensivist, the therapy of culprit lesions in the upper GI tract should involve at least cursory collaboration between the gastroenterologist and the surgeon. Surgical backup should be readily available, and in the severely bleeding patient, it is useful to have the surgeon present to observe the endoscopic findings and facilitate urgent surgery, particularly when attempting endoscopic hemostasis in deep, posterior duodenal bulbar ulcers or other high-risk lesions.

Endoscopy in Upper GI Bleeding: Equipment and Accessories Because endoscopy in upper GI bleeding is aimed at delivering therapy, careful attention to choice of endoscopes and preparation of accessories is essential. The alternatives are a therapeutic endoscope with a large (3.7 mm) channel with or without a second channel, versus a diagnostic endoscope with a single small (2.8 mm) channel. We recommend a two-channel therapeutic endoscope for the majority of cases of upper GI bleeding and for cases of suspected active or severe nonvariceal bleeding (Fig. 2). A large channel is essential to pass 10 French hemostatic probes, which are not only more effective for hemostasis, but may greatly enhance the thoroughness of the diagnostic examination. Advantages of dual channels include the ability to suction greater quantities of blood; to simultaneously use two devices or a therapeutic device in one channel and suction through another. Presence of a therapeutic device in a single-channel endoscope precludes suction and may lead to over-insufflation and risk of aspiration. In addition, therapeutic endoscopes have an accessory irrigation channel that can provide high-intensity irrigation when connected with an irrigation pump. In circumstances such as suspected aorto-enteric fistula or upper GI angioectasiae, a pediatric colonoscope or pushenteroscope can be very useful to examine the distal duodenum and proximal jejunum. For suspected hemobilia, or for a suspected duodenal source without adequate visualization with an end-viewing scope, a side-viewing duodenoscope may be essential (Fig. 3). Actively bleeding lesions often can be clearly visualized for only seconds before disappearing beneath a rapidly enlarging pool of blood. To capitalize on any available opportunity, accessories should be ready, plugged-in, and tested before beginning the procedure. To assure that all necessary equipment is available and easy to locate, some centers use a mobile “bleeding cart” which contains all of the accessories necessary for diagnosis and therapy of GI bleeding. Equipment on such a cart should include esophageal overtubes, hemostatic probes and generator units with backup probes available, sclerotherapy needles, band-ligation devices, sclerosant solutions, cannulas, snares, baskets and other devices neces-

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Figure 3 Duodenoscopic view of delayed hemorrhage post biliary sphincterotomy. A side-viewing duodenoscope is essential for visualization and treatment of many causes of duodenal bleeding.

sary to break up or remove clots, and finally, a Water Pik or other high-pressure irrigation device.

Diagnostic Endoscopy in Upper GI Bleeding: Techniques Visualization of and access to the source of bleeding are the most critical aspects of endoscopic hemostatic therapy. Precise localization of the bleeding lesion may take up to an hour or more. A rapid scan of the entire upper tract followed by concentration on the areas of freshest blood or clot yields the greatest chance of finding a culprit lesion. Initially, the esophagus is evaluated for varices, ulcers, and tears. The approach to the stomach and duodenum is determined by the amount of blood present. If large amounts of gastric blood or clot are present, it is often valuable to skim over the pool, examine the exposed stomach, and proceed quickly to the duodenum. However, if the stomach is clean and free of blood, it should be examined carefully before proceeding to the duodenum. Looping of the endoscope along the greater curvature while traversing the pylorus can produce artifacts easily confused with upper GI angioectasiae. A retroflexed view will allow examination of the cardia and fundus for Mallory–Weiss tears, gastric varices, ulcers, or angioectasiae. After examination of the stomach, a careful examination of the duodenum is warranted. A snare can be used to break up fresh clots, which then can be either pulled or suctioned back into the stomach. When there is extensive clot adherent to the walls of the stomach and duodenum, a systematic and exhaustive search with careful irrigation or manipulation of each clot and fold may be necessary to identify the source of bleeding. Focused irrigation with 3% hydrogen peroxide may improve visualization by rendering overlying blood semitranslucent and more easily removed.10,11 Forceful target-irrigation can be accomplished with a therapeutic endoscope either by hooking up an irrigation pump to the accessory channel or by using a hemostatic probe such as a heater or bipolar probe. Under direct visual control, the catheter or probe can be very effective in washing away blood

J. Matlock and M.L. Freeman and most clots. Irrigation through probes or the third, accessory channel provides a high-velocity, narrow jet, and is more effective at dislodging clots than irrigation through a working channel, which tends to “dribble” a large volume of water without much force. The irrigation pump can be operated with a foot switch, freeing up both hands for other tasks. Heater or bipolar probes can also be used for manipulating clots and edematous folds. Stiff probes can be used to depress the proximal margin of an ulcer to allow full examination of the ulcer base for stigmata of recent hemorrhage. Rotating the endoscope so that the lesion is positioned in the quadrant where the probe emerges into view (usually between 3 and 6 o’clock) allows forceful tamponade by down flexing the instrument without losing site of the lesion. When a swirl of blood obscures its source, forceful tamponade of the suspected bleeding point with a large probe often results in prompt cessation of bleeding. Alterations in patient positioning can provide improved visualization with actively bleeding lesions or in the presence of large, gelatinous clots that cannot be suctioned or removed through gastric lavage. In the case of actively bleeding lesions, turning the patient to place the bleeding point in a superior position allows blood to drip away from the region of interest, leaving the field relatively clear (Fig. 4). In the presence of large clots, blood pools along the greater curvature and fundus when the patient is in the left lateral decubitus position. In the “roll over” maneuver, the patient is turned first from the left lateral to the supine position, and then to the right lateral decubitus position to shift the blood to the opposite wall (Fig. 5). This maneuver often clears the gastric fundus, the greater curvature, and other areas that were in the dependent location while the patient was in the left lateral decubitus position. Elevating the thorax of the patient (ie, reverse Trendelenberg) is recommended if the blood pressure is adequate, as patient manipulation may precipitate reflux of gastric contents and subsequent aspiration. Suctioning of all residual liquid is recommended before rolling patients.

Figure 4 Active bleeding gastric Dieulafoy lesion. Retroflexed view shows active spurting from high on lesser curve of stomach, in typical location.

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Figure 5 Rollover maneuver to examine fundus/greater curve. (A) In the left lateral position, blood and clots pool along the greater curve. (B) Rolling the patient onto the right side allows examination of the greater curve and fundus. Care must be taken to avoid reflux and aspiration of gastric contents during this maneuver. Adapted from Freeman.12

Compared with the stomach, with the angularis as a reliable anatomic landmark, the duodenum presents a challenge for anatomic localization of a lesion. Due to variation in anatomy and in the endoscopist’s stance, the endoscope may become rotated in passage through the pylorus. There is no reliable method of localizing an ulcer in the duodenum. but posterior lesions are usually at 3 o’clock, anterior lesions are at 9 o’clock, superior at 12 o’clock, and inferior at 6 o’clock. Rotation of the endoscope will alter these positions. Because of rotation, assessment of duodenal lesion orientation on entrance of the pylorus is more reproducible than on withdrawal from the distal duodenum. Pushing on the patient’s abdomen may locate the anterior wall of the stomach.

References 1. Rockall TA, Logan RFA, Devlin HB, et al: Risk assessment after acute upper gastrointestinal haemorrhage. Gut 38:316, 1996 2. Barkun A, Bardou M, Marshall J: Consensus recommendations for managing patients with nonvariceal upper gastrointestinal bleeding. Ann Intern Med 139:843-857, 2003 3. Lee JG, Turnipseed S, Romano PS, et al: Endoscopy-based triage significantly reduces hospitalization rates and costs of treating upper GI bleeding: a randomized controlled trial. Gastrointest Endosc 50:75561, 1999

4. Lipper B, Simon D, Cerrone F: Pulmonary aspiration during emergency endoscopy in patients with upper gastrointestinal hemorrhage. Crit Care Med 19:330, 1991 5. Rudolph S, Landsverk B, Freeman ML: Endotracheal intubation for airway protection during endoscopy for severe upper GI hemorrhage. Gastrointest Endosc 57:58-61, 2003 6. Aljebreen AM, Fallone CA, Barkun AN: Nasogastric aspirate predicts high-risk endoscopic lesions in patients with acute upper-GI bleeding. Gastrointest Endosc 59:172-178, 2004 7. Sung JJ, Chung SC, Lai CW, et al: Octreotide infusion or emergency sclerotherapy for variceal hemorrhage. Lancet 342:637-641, 1993 8. Frossard JL: Erythromycin intravenous bolus infusion in acute upper gastrointestinal bleeding: a randomized, controlled, double-blind trial. Gastroenterology 123:17-23, 2002 9. Coffin B, Pocard M, Panis Y, et al: Erythromycin improves the quality of EGD in patients with acute upper GI bleeding: a randomized controlled study. Gastrointest Endosc 56:174-179, 2002 10. Wu DC, Lu CY, Lu CH, et al: Endoscopic hydrogen peroxide spray may facilitate localization of the bleeding site in acute upper gastrointestinal bleeding. Endoscopy 31:237-241, 1999 11. Kalloo AN, Canto MI, Wadwa KS, et al: Clinical usefulness of 3% hydrogen peroxide in acute upper GI bleeding: a pilot study. Gastrointest Endosc 49:518-521, 1999 12. Freeman ML: Current ICU management and endoscopic diagnosis of severe nonvariceal upper gastrointestinal bleeding. Gastrointest Endosc Clin North Am 1:209-239, 1991