Current Management of Upper Gastrointestinal Bleeding R. DOUGLAS YAJKO, M.D., LAWRENCE W. NORTON, M.D., BEN EISEMAN, M.D.
Over a four-year period, 585 patients were hospitalized for massive From the Department of Surgery, Denver General Hospital and the University of Colorado Medical Center, Denver, upper gastrointestinal bleeding. Endoscopy diagnosed the cause of bleeding in 80% of 200 patients so studied. Selective angiography Colorado 80204 localized the bleeding site in 12 of 20 patients, and infusion of vasopressor stopped hemorrhage in six. Barium studies were 90% raphy. This period was a transition between the past era accurate in diagnosing ulcer disease but failed to detect gastritis. of utilizing one operation for the control of upper gasOne hundred thirty (22%) patients were operated upon for medi- trointestinal bleeding and the present era of tailoring procally uncontrolled bleeding. The proportion of patients requiring cedures to the specific conditions causing hemorrhage. surgery fell from 33% in year one to 13% in year four. Benign ulcer disease caused bleeding in 51% of surgical patients, while gastritis Methods and Materials was found in 20%, esophageal varices in 15% and stress ulcer in 8%. During the four years, 1969 through 1973, a total of 585 Overall operative mortality was 29%. Among 38 duodenal ulcer with acute upper gastrointestinal bleeding were patients patients, mortality was 18%. Vagotomy and pyloroplasty were more effective than resection in this group. Resection for distal gastric treated in the Denver General Hospital. Such patients ulcers in 22 patients resulted in a mortality of 14% and no rebleed- comprised 1.1-1.2% of all hospitalizations during each ing. While V&P controlled bleeding in 12 alcoholics with gastritis, year of the study. five (42%) died postoperatively. Mortality among 20 patients with The diagnosis of upper gastrointestinal hemorrhage esophageal varices was 35%, although all five survived who had was based upon evidence of hematemesis or recovery of porto-caval shunts. Eight of 10 patients operated upon for stress blood from the stomach. Initial treatment under the comulcer bleeding died. Postoperative rebleeding occurred in 14 patients, eight of whom were again operated upon. In all but one a bined direction of both medical and surgical services new lesion was found to be responsible for hemorrhage. Increas- consisted of cold saline irrigation of the stomach via a ing use of gastroscopy and selective angiography can be expected nasogastric tube and intravenous administration of crysto improve diagnostic capabilities in patients with upper gastrointestinal bleeding. Infusing vasopressor into selected arteries talloid solutions. Whole blood was transfused when shed should reduce the need for surgical control of gastritis, variceal blood exceeded one liter in volume, when systolic blood and stress ulcer bleeding, conditions poorly managed by current pressure fell from normal to below 80 mmHg or when the operative techniques. hematocrit was less than 30%o.
Fiberoptic Gastroscopy A fiberoptic gastroduodenoscope was used to locate the site of active bleeding in 200 patients. A completely accurate diagnosis, as confirmed by gastrotomy, barium studies, subsequent elective gastroscopy or autopsy, was made in 80% of these patients (Fig. 1). Among 50 consecutive bleeders endoscoped during year four of the study, an actively bleeding lesion was identified in 46 (92%). More than half (55%) of this group had two or more potential bleeding sites. Erosive gastritis was seen in 31, gastric ulcer in 17, esophageal varices in 12, esophagitis in eight, duodenal ulcer in five and Submitted for publication July 18, 1974. Supported by National Institutes of Health Grants #GM20309 and Mallory-Weiss lesions of esophageal mucosa in five patients. #AM 17022.
TECHNIQUES of fiberoptic gastroscopy, selective angiography and intra-arterial infusion of vasopressors expand possibilities in the, diagnosis and treatment of massive upper gastrointestinal hemorrhage. Mortality after surgery for such bleeding remains high despite greater selectivity in the choice of operation. This is a review of our experience in diagnosing and treating upper gastrointestinal bleeding at a municipal hospital over a period of years coinciding with the development and use of fiberoptic gastroscopy and angiog-
474
VOl. 181 * NO. 4
FIG. 1. Fiberoptic gastroduodenoscopy provided a specific diagnosis of the cause of acute upper gastrointestinal bleeding in 160 of 200 patients (80%).
475
UPPER GASTROINTESTINAL BLEEDING
Li.iyio\i
Specific Diagnosis by
Endoscopy
FIG. 3. Of 585 patients with acute upper gastrointestinal hemorrhage, 130 (22%) required operation.
80%
/n200 During the first two years of study, occasional patients were examined with the gastroduodenoscope while massively bleeding. This proved frustrating and unrewarding. Subsequently, gastroscopy was performed only after profuse bleeding subsided, usually within 12 hours following hospitalization. Selective Angiography During the final study year (1973), 20 patients underwent selective angiography to determine the site of uppei gastrointestinal hemorrhage. Catheters were introduced via the femoral artery in all but one patient. Attempts to enter the left gastric artery were unsuccessful in three patients. A precise diagnosis was established in 12 (60%) patients (Fig. 2). Five had esophageal varices demonstrated without obvious loss of contrast media into the esophageal lumen. Subsequent findings confirmed that these patients had no other cause of bleeding. Gastric ulcers were diagnosed in two patients and multiple bleeding sites, typical of stress ulceration, in two others. Alcoholic gastritis and a Mallory-Weiss esophageal tear were found in one patient each. In two patients, angiography demonstrated esophageal varices but gastroscopy revealed other potential bleeding sites. A cause of bleeding was not established in six other patients with angiographic techniques. Four of these patients had stopped bleeding by the time contrast media was injected. One patient bleeding from stress ulcers and
another bleeding from gastric ulcer were not diagnosed by angiography. Of the 20 patients studied, one developed a hematoma at the site of femoral artery catheterization and one required removal of the catheter because of arterial spasm.
Intra-arterial Infusion With intra-arterial catheters selectively placed, vasopressin, 0.2-0.4 units per minute, was infused in 12 patients to control active hemorrhage. Bleeding stopped in six patients (50%) within 90 minutes of beginning infusion. Two of these patients had esophageal variceal hemorrhage. Two others had gastric ulcers. One patient with alcoholic gastritis and another with multiple stress ulcers responded to infusion. A patient with gastritis had stopped bleeding after infusion was begun but rebled when the catheter was removed accidentally five hours later. Five patients did not respond to infusion of vasopressor and required operation. Two were bleeding from varices, two from stress ulcers and one from gastritis. In neither of the stress ulcer patients was the left gastric artery catheterized successfully. Barium Roentgenographic Studies In only 11 patients (1.9%) was the exact cause of bleeding diagnosed during active hemorrhage by means of barium swallow or upper gastrointestinal series alone. Barium studies were obtained routinely in most patients after bleeding stopped. Peptic ulcer disease was diag-
100
FIG. 2. Selective angiography provided a specific diagnosis of the site of bleeding in 12 of 20 patients
(60%).
FIG. 4. The proportion of bleeding patients requiring surgery fell progressively from year one (33%) through year four (13%) of the study.
331 }
1
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YAJKO, NORTON AND EISEMAN
476
FIG. 7. The primary causes of bleeding in 130 operated patients were predominantly benign peptic ulcer disease and gastritis.
FIG. 5. A preoperative diagnosis of the cause and site of bleeding was made in 65% of patients.
nosed by such studies in 90%7o of patients subsequently have ulcers. Barium swallow showed esophageal varices in 72% of patients found to have varices on endoscopic examination. Of 44 patients with acute mucosal lesions diagnosed by endoscopy, barium studies were normal in all but one.
proven to
Laparotomy Of the entire 585 patients treated for upper gastrointestinal bleeding, 130 (22%) required laparotomy for 138 episodes of medically uncontrolled hemorrhage (Fig. 3). The proportion of those operated upon fell progressively from 33% in the first year of study to 13% in the fourth year (Fig. 4). Indications for operations were: 1) transfusion of whole blood exceeding 2500 ml in the first 24 hours; 2) transfusion exceeding 1500 ml in the second 24 hours; or 3) rebleeding after 24 hours of vigorous medical therapy. Average age of the 130 patients undergoing operation was 51 years (range 15-89 years). Ninety-seven were males and 33 were females. For 45 patients (35%) who underwent operation we did not have a precise, proven diagnosis of the cause or site of bleeding (Fig. 5). The proportion of such undiagnosed patients was less in year four (15%) when endoscopy and angiography were used commonly, than in year one (43%). When the site of bleeding was unknown at the time of laparotomy, a longitudinal pylorotomy was made for inspection of the duodenum and antrum. If necessary, this was followed by transverse gastrotomy at midstomach for inspection of the corpus, fundus, cardia and distal esophagus (Fig. 6). The latter was visualized in some cases by lateral traction on one or more nasogastric tubes passed through the cardia and fixed at the nose.
1
%
%%
FIG. 6. In patients without a preoperative diagnosis ofthe cause and site ofbleeding, pylorotomy(1)
%%%
,,was "
performed first followed by
transverse
gastrotomy (2).
Cause of Bleeding in Surgical Patients The etiology of primary bleeding in 130 surgical patients is summarized in Fig. 7. Benign peptic ulcers accounted for 51% of bleeding lesions (38 duodenal and 28 gastric ulcers). Diffuse gastritis was found in 26 patients (20%), of whom 18 had recently been drinking. Of the eight other patients with gastritis four (50%'o) had been taking aspirin, phenylbutazone or corticosteroids for one week or longer. Other causes of bleeding were esophageal varices in 20 patients (15%) and stress ulceration in 10 patients (8%).Eight others (6%) had miscellaneous lesions such as anastomotic (stomal) ulcer (3), Barrett's esophageal ulcer (2), aorto-duodenal fistula (1), gastrocolic fistula (1) and hemobilia secondary to carcinoma of the gall bladder (1).
Operative Procedures Three-quarters of the 138 operations performed were selected according to our established protocol which is summarized in Table 1. In the other 25%, the surgical residents, who performed all of the operations under the active operating room guidance of a faculty surgeon, chose to violate the protocol for reasons of the patient's critical condition (25%), technical difficulties (10%) or difference in preference (65%). Results
Duodenal Ulcer-Poor Risk Twenty-three of 38 patients operated upon for duodenal ulcer bleeding were judged to be poor surgical TABLE 1. Recommended Operationsfor Specific Causes ofAcute Upper Gastrointestinal Hemorrhage
Pathology Gastritis, Alcoholic Gastritis, Non-alcoholic Duodenal Ulcer (Poor Risk) Duodenal Ulcer (Good Risk) Gastric Ulcer (Corpus-Antrum) Gastric Ulcer (Fundus-Cardia) Stress Ulcer
Esophageal Varices *Ligate bleeding vessel.
Operation Vagotomy and Pyloroplasty Vagotomy and Hemigastrectomy Vagotomy and Pyloroplasty* Vagotomy and Hemigastrectomy Vagotomy and Hemigastrectomy Vagotomy and Pyloroplasty* Vagotomy and 75%-95% Gastrectomy Porto-Systemic Shunt
UPPER GASTROINTESTINAL BLEEDING
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477
TABLE 2. Results of Primary Operations for Acute Upper Gastrointestinal Hemorrhage
Pathology
Operations
Died
Rebled
Duodenal Ulcer-Poor Risk (23) Duodenal Ulcer-Good Risk (15)
V&P (23) V&P (4) V&Hemigastrectomy (11)
5 (22%) 0 2 (18%)
2 (9%) 1 (25%)
Gastric Ulcer-Resectable (22) Gastric Ulcer-Unresectable (6)
V&Hemigastrectomy (22) V&P (4) V&Hemigastrectomy (2)
3 (14%) 0 0
Gastritis-Alcoholic (18)
V&P (12) V&Hemigastrectomy (6) V&P (5)
V&Hemigastrectomy (3)
5 (42%) 5 (83%) 1 (20%o) 0
Stress Ulcer (10)
V&P (3) V&Hemigastrectomy (4) V&Near-total Gastrectomy (3)
2 (67%) 3 (75%) 3 (100%o)
Esophageal Varices (20)
Ligation (6) Portocaval Shunt (5) Mesocaval Shunt (7) Mesocaval (H) Shunt (2)
4 (67%) 0 2 (29%) 1 (50b)
Gastritis-Non-alcoholic (8)
risks (over 65 or another life-threatening disease). All such poor risk patients underwent vagotomy and Heineke-Mikulicz pyloroplasty. In 11 patients the bleeding vessel was oversewn but in 12 others bleeding stopped without direct vessel ligation. Two poor risk duodenal ulcer patients rebled after V&P and five (22%) died within 30 days (Table 2). Duodenal Ulcer-Good Risk Of 15 good risk patients bleeding from duodenal ulcer, 11 underwent the recommended operation of vagotomy and hemigastrectomy. Two of the 11 patients (18%) died postoperatively without rebleeding (Table 2). Four protocol variant patients, considered to be good risks, had vagotomy and pyloroplasty. One rebled and required gastric resection. Of the entire 38 patients with bleeding duode-nal ulcer, three (8%) rebled and seven (18%) died within one month of operation. Mortality was 18% following both V&P (27 patients) and vagotomy and hemigastrectomy (11 patients). These statistics lend no support to adding resection to vagotomy as a life-saving procedure for duodenal ulcer hemorrhage. Gastric Ulcer-Resectable In 22 of 28 patients with bleeding gastric ulcer, the ulcer crater was in the antrum or corpus of the stomach distal to the cardia. Such lesions were excised by partial gastrectomy. No patient rebled after this operation but three (14%) died in the hospital. Gastric Ulcer-Unresectable Six other patients had bleeding ulcers in the proximal
1 (20%o)
2 (33%) 1 (14%)
stomach where partial gastrectomy could not be done without trespassing on the esophagogastric junction. The advised operation per protocol in such patients was V&P with biopsy of the ulcer and oversewing of bleeding vessels. This was done in four patients all of whom survived and none of whom rebled. In two similar patients, vagotomy and hemigastrectomy were performed without complication (Table 2). The overall experience with bleeding gastric ulcers in 28 patients resulted in a mortality rate of 11% and no postoperative rebleeding.
Gastritis-Alcoholic Eighteen patients had diffuse, superficial mucosal erosions of the gastric corpus and fundus following a prolonged alcoholic debauch. Twelve were treated as per protocol by V&P. None of these continued to bleed but five (42%) died within 30 days (Table 2) of pulmonary disease or sepsis. Protocol was broken and vagotomy and hemigastrectomy performed in six other alcoholics with gastritis. Although none of these rebled, five (83%) died in the hospital. Survival was thus twice as good when V&P were performed than when the stomach was partially resected for alcoholic gastritis.
Gastritis-Non-alcoholic Among eight patients with non-alcoholic gastritis, operative treatment was V&P in five, of whom bne rebled and later died (20%), and vagotomy and hemigastrectomy in three, none of whom rebled or died (Table 2). The overall mortality of patients requiring surgery for
gastritis was 42% (11 patients). One death followed bleeding.
re-
Esophageal Varices
Twenty patients bleeding from esophageal varices did not respond to nonoperative forms of therapy such
as
esophageal balloon tamponade or infusion of vasopressin into the superior mesenteric artery. Six such patients had transthoracic suture ligation of varices alone. Four (67%) died, two after rebleeding. Two have survived without rebleeding for more than three years (Table 2). All five patients who underwent emergency end-toside portocaval shunting survived and none has rebled during a mean followup period of 22 months. A sixth portocaval shunt was constructed in a patient who rebled after ligation of esophageal varices. This patient did not rebleed but died of liver failure after three weeks. Seven patients had mesocaval shunting for bleeding varices. In each, the iliac vein was sutured end-to-side to the superior mesenteric vein. One of these patients rebled and two (29%) died postoperatively. The five survivors have not rebled during a mean 20 months of followup. Interposition H-type mesocaval shunts were constructed in two patients during the last year of study using the Teflon derivative Gore-Tex13 as prosthetic vein. Neither patient rebled but one died of hepatic failure 10 days after operation with an open graft. In the entire group of 20 patients operated upon for bleeding esophageal varices, mortality was 35%. Three patients (15%) continued to bleed after operation and two died. Stress Ulcer
of
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YAJKO, NORTON AND EISEMAN
478
Ten patients had multiple gastric ulcers after the stress surgery, trauma, or sepsis. Six of the 10 developed
1975
stress ulceration in relation to sepsis. None had duodenal stress ulcers.
Seven patients had the suggested vagotomy and resection of whom six (86%) died of either respiratory insufficiency or sepsis. None had rebled prior to death. Three of the seven had near-total (85-95%) gastrectomy in an effort to remove all involved mucosa and all died postoperatively. Three stress ulcer patients underwent V&P, of whom two (67%) died. The hospital mortality of the 10 patients requiring operation for stress bleeding was 80%. No patient rebled. Among other rebleeding patients, however, stress ulcer was encountered twice. Each patient survived after subtotal gastrectomy (1) and oversewing (1). Rebleeding Fourteen of 130 surgical patients, (11%), continued to bleed or rebled after operation. Only eight (6%) required reoperation to control persistant or recurrent hemorrhage. The average age of these patients was 56 years. Each received an average 12,000 ml of blood during hospitalization. Rebleeding was due to disease not previously diagnosed in seven of the eight patients (Table 3). Three patients with duodenal ulcers initially treated by V&P rebled postoperatively and each was found to have hemorrhagic gastritis as the cause of bleeding. Of two patients who continued to bleed after ligation of esophageal varices, one had hemorrhagic gastritis and the other had variceal bleeding. A third patient primarily diagnosed as esophageal varices developed stress ulceration following mesocaval shunt and required subtotal gastrectomy. Stress ulcer was also diagnosed in a patient with primary stomal ulcer bleeding. Three of the eight patients with rebleeding died although none exsanguinated.
Discussion Massive bleeding from the upper gastrointestinal tract
TABLE 3. Rebleeding After Primary Operation for Acute Upper Gastrointestinal Hemorrhage
Patient First Diagnosis 1
Doudenal Ulcer, poor risk
First Operation
Second Diagnosis
Second Operation
V&P
Gastritis, Non-
Subtotal Gastrectomy
Died
Subtotal Gastrectomy
Lived
Subtotal Gastrectomy
Lived
Subtotal Gastrectomy
Lived
Oversew Total Gastrectomy
Lived Died
Portocaval Shunt Subtotal Gastrectomy
Died Lived
Outcome
alcoholic 2
Duodenal Ulcer, poor risk
V&P
Gastritis, Nonalcoholic
3
Duodenal Ulcer, good risk
V&P
4
Gastritis, Non-alcoholic
V&P
5 6
Stomal Ulcer Esophageal Varices
Subtotal Gastrectomy
7 8
Esophageal Varices Esophageal Varices
Ligation
Ligation Mesocaval Shunt
Gastritis, Nonalcoholic Gastric Ulcer, Resectable Stress Ulcer Gastritis, Nonalcoholic Esophageal Varices Stress Ulcer
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UPPER GASTROINTESTINAL BLEEDING TABLE 4. Summary ofResults
Disease Duodenal Ulcer Gastric Ulcer Gastritis Esophageal Varices Stress Ulcer
Satisfactory Control of Bleeding yes yes yes yes no
Satisfactory Survival yes yes no no no
479
The role of vagotomy with resection for gastric ulcer is not established9 but we favor reducing gastric acidity as well as excising distal stomach.
Gastritis
The high incidence of gastritis as a cause of massive upper gastrointestinal bleeding is increasingly recognized as endoscopy becomes more popular.1 4 Vagotomy and is a clinical manifestation of several diseases each of pyloroplasty stop bleeding in most patients with both which requires different operative and nonoperative alcoholic and non-alcoholic gastritis. Resection in the therapy. A mass reflex technical response, such as partial latter is not justified. Mortality among alcoholics with gastrectomy, no longer is sufficiently precise to be de- gastritis is high (56%) because of frequently associated sepsis, pulmonary insufficiency or metabolic disease. fensable. Sophisticated endoscopic and angiographic techniques Avoiding surgery by infusion of vasopressor into the left can now provide accurate diagnosis in the majority of gastric artery may reduce mortality. bleeders. As a result, management can be more accurately tailored to the responsible lesion. This review of Esophageal Varices our experience at the Denver General Hospital covers the period of transition in which these advances were Infusion of vasopressor into the superior mesenteric recognized and utilized. artery stops variceal bleeding in about 70% of patients.2 There can be no complacency in the management of a When infusion fails, porto-systemic shunting is indicated. disease where operative mortality is 29% even though Transthoracic suture ligation of varices is ineffective in our results are comparable to those reported from both stopping hemorrhage or reducing mortality. The shunt of municipal6 and private3 hospitals. Progress requires in- choice, on the basis of our experience, is end-to-side dentifying which lesions are treated relatively well and portocaval anastomosis. Recent use of a prosthesis as an which are managed poorly. Simplistically, both our re- interposition mesocaval shunt has been gratifying in sults and those of others could be summarized as in terms of technical ease and shortened operative time. In Table 4. a much larger group of patients, Drapanas7 has confirmed are fails often in which management present The areas this experience, making the interposition procedure our ulcer. stress and varices alcoholic gastritis, esophageal present choice in the operative treatment of varices. Rationale for choosing an operative procedure once the cause of upper gastrointestinal bleeding is known is Stress Ulcer based upon the following: Vagotomy and pyloroplasty control bleeding with acMortality after surgery for stress ulcer bleeding is ceptable mortality. It is a technically simple and rapid alarming.14 Results of Kirtley, et al.10 showing 65% surprocedure. The only argument is whether, in good risk vival after V&P have seldom been duplicated by others. patients, under ideal conditions, vagotomy and hemigas- Death after stress ulcer bleeding is often due to pretrectomy should not be perfprmed because of the lower existing disease. Thus, even near-total gastrectomy, rate of ulcer recurrence following this operation.8 Among which eliminates potential bleeding mucosa, does not our patients, mortality was the same (18%) after vag- improve survival. Still, vagotomy and high gastric resenotomy and resection as after vagotomy and pyloroplasty. tion seem more reasonable operations than V&P, which are followed by excessive rates of recurrent bleeding.11 Nonoperative management of stress ulceration by inGastric Ulcer travenous corticosteroids12 or infusion of vasopresson into the left gastric artery5 could be tried before surgery, of operative although ultimate mortality of the disease may not be Excision must remain the cornerstone Partial gastrectomy lessened. treatment of bleeding gastric ulcers. Diagnostic and therapeutic approaches to the upper and vagotomy effectively stop hemorrhage with good bleeder will continue to change in the gastrointestinal resected be which cannot survival (86%). Benign ulcers, as seventies endoscopy, angiography, infusion without destroying the cardio-esophageal junction, selective and surgery are more widely practechniques Our and drainage. should be treated first by vagotomy will be changed thereby remains Whether ticed. mortality that of number patients suggests experience in a small a that It is technique will benefit be seen. given to likely limited a such procedure. bleeding can be controlled by
YAJKO, NORTON AND EISEMAN
480
one type of bleeder but not another. Nevertheless, these new abilities make more hopeful the treatment of gastrointestinal hemorrhage in this decade.
References 1. Allen, H. M., Block. M. A. and Schuman, B. M.: Gastroduodenal Endoscopy. Management of Acute Upper Gastrointestinal Hemorrhage. Arch. Surg., 106:450, 1973. 2. Baum, S. and Nusbaum, M.: The Control of Gastrointestinal Hemorrhage of Selective Mesenteric Arterial Infusion of Vasopressin. Radiology, 98:497, 1971. 3. Connecticut Society of American Board of.Surgeons: Immediate Results of Emergency Operation for Massive Upper Gastrointestinal Hemorrhage. Am. J. Surg., 122:387, 1971. 4. Conn, H. 0. and Brodoff, M.: Emergency Esophagoscopy in the Diagnosis of Upper Gastrointestinal Hemorrhage. Gastroenterology, 47:505, 1964. 5. Conn, H. O., Ramsby, G. R. and Storer, E. H.: Selective IntraArterial Vasopressin in the Treatment of Upper Gastrointestinal
Hemorrhage.
Ann.
Surg.
*
April
1975
6. Crook, J. N., Gray, L. W., Nance, F. C. and Cohn, I.: Upper Gastrointestinal Bleeding. Ann. Surg., 175:711, 1972. 7. Drapanas, T.: Interposition Mesocaval Shunt for Treatment of Portal Hypertension. Ann. Surg., 176:435, 1972. 8. Goligher, J. G., Pulvertaft, G. N., Irvin, T. T., et al.: Five to 8 Year Results of Truneal Vagotomy and Pyloroplasty for Duodenal Ulcer. Br. Med. J., 1:7, 1972. 9. Kelly, H. G., Grant, G. W. and Elliot, D. W.: Massive Gastroduodenal Hemorrhage-Changing Concepts of Management. Arch. Surg., 87:112, 1963. 10. Kirtley, J., Scott, H., Sawyers, J., et al.: The Surgical Management of Stress. Ann. Surg., 169:801, 1969. 11. Menguy, R., Gadecz, T. and Zajtchuk, R.: The Surgical Management of Acute Gastric Mucosal Bleeding, Stress Ulcer, Acute Erosive Gastritis, and Acute Hemorrhagic Gastritis. Arch. Surg., 99:198, 1969. 12. Proudfoot, W. H., Bolick, R., Schoffstall, R., et al.: Dexamethasone Therapy for Stress Ulcer. Am. Surg., 38:638, 1972. 13. Soyer, T., Lempinen, M., Cooper, P., et al.: A New Venous Prosthesis. Surgery, 72:864, 1972. 14. Stremple, J. F., Mari, H., Lev, R. and Jerzy Glass, G. B.: The Stress Ulcer Syndrome. In Current Problems in Surgery. Chicago, Year Book Medical Publishers, 19, April 1973.
Over a four-year period, 585 patients were hospitalized for massive From the Department of Surgery, Denver General Hospital and the University of Colorado Medical Center, Denver, upper gastrointestinal bleeding. Endoscopy diagnosed the cause of bleeding in 80% of 200 patients so studied. Selective angiography Colorado 80204 localized the bleeding site in 12 of 20 patients, and infusion of vasopressor stopped hemorrhage in six. Barium studies were 90% raphy. This period was a transition between the past era accurate in diagnosing ulcer disease but failed to detect gastritis. of utilizing one operation for the control of upper gasOne hundred thirty (22%) patients were operated upon for medi- trointestinal bleeding and the present era of tailoring procally uncontrolled bleeding. The proportion of patients requiring cedures to the specific conditions causing hemorrhage. surgery fell from 33% in year one to 13% in year four. Benign ulcer disease caused bleeding in 51% of surgical patients, while gastritis Methods and Materials was found in 20%, esophageal varices in 15% and stress ulcer in 8%. During the four years, 1969 through 1973, a total of 585 Overall operative mortality was 29%. Among 38 duodenal ulcer with acute upper gastrointestinal bleeding were patients patients, mortality was 18%. Vagotomy and pyloroplasty were more effective than resection in this group. Resection for distal gastric treated in the Denver General Hospital. Such patients ulcers in 22 patients resulted in a mortality of 14% and no rebleed- comprised 1.1-1.2% of all hospitalizations during each ing. While V&P controlled bleeding in 12 alcoholics with gastritis, year of the study. five (42%) died postoperatively. Mortality among 20 patients with The diagnosis of upper gastrointestinal hemorrhage esophageal varices was 35%, although all five survived who had was based upon evidence of hematemesis or recovery of porto-caval shunts. Eight of 10 patients operated upon for stress blood from the stomach. Initial treatment under the comulcer bleeding died. Postoperative rebleeding occurred in 14 patients, eight of whom were again operated upon. In all but one a bined direction of both medical and surgical services new lesion was found to be responsible for hemorrhage. Increas- consisted of cold saline irrigation of the stomach via a ing use of gastroscopy and selective angiography can be expected nasogastric tube and intravenous administration of crysto improve diagnostic capabilities in patients with upper gastrointestinal bleeding. Infusing vasopressor into selected arteries talloid solutions. Whole blood was transfused when shed should reduce the need for surgical control of gastritis, variceal blood exceeded one liter in volume, when systolic blood and stress ulcer bleeding, conditions poorly managed by current pressure fell from normal to below 80 mmHg or when the operative techniques. hematocrit was less than 30%o.
Fiberoptic Gastroscopy A fiberoptic gastroduodenoscope was used to locate the site of active bleeding in 200 patients. A completely accurate diagnosis, as confirmed by gastrotomy, barium studies, subsequent elective gastroscopy or autopsy, was made in 80% of these patients (Fig. 1). Among 50 consecutive bleeders endoscoped during year four of the study, an actively bleeding lesion was identified in 46 (92%). More than half (55%) of this group had two or more potential bleeding sites. Erosive gastritis was seen in 31, gastric ulcer in 17, esophageal varices in 12, esophagitis in eight, duodenal ulcer in five and Submitted for publication July 18, 1974. Supported by National Institutes of Health Grants #GM20309 and Mallory-Weiss lesions of esophageal mucosa in five patients. #AM 17022.
TECHNIQUES of fiberoptic gastroscopy, selective angiography and intra-arterial infusion of vasopressors expand possibilities in the, diagnosis and treatment of massive upper gastrointestinal hemorrhage. Mortality after surgery for such bleeding remains high despite greater selectivity in the choice of operation. This is a review of our experience in diagnosing and treating upper gastrointestinal bleeding at a municipal hospital over a period of years coinciding with the development and use of fiberoptic gastroscopy and angiog-
474
VOl. 181 * NO. 4
FIG. 1. Fiberoptic gastroduodenoscopy provided a specific diagnosis of the cause of acute upper gastrointestinal bleeding in 160 of 200 patients (80%).
475
UPPER GASTROINTESTINAL BLEEDING
Li.iyio\i
Specific Diagnosis by
Endoscopy
FIG. 3. Of 585 patients with acute upper gastrointestinal hemorrhage, 130 (22%) required operation.
80%
/n200 During the first two years of study, occasional patients were examined with the gastroduodenoscope while massively bleeding. This proved frustrating and unrewarding. Subsequently, gastroscopy was performed only after profuse bleeding subsided, usually within 12 hours following hospitalization. Selective Angiography During the final study year (1973), 20 patients underwent selective angiography to determine the site of uppei gastrointestinal hemorrhage. Catheters were introduced via the femoral artery in all but one patient. Attempts to enter the left gastric artery were unsuccessful in three patients. A precise diagnosis was established in 12 (60%) patients (Fig. 2). Five had esophageal varices demonstrated without obvious loss of contrast media into the esophageal lumen. Subsequent findings confirmed that these patients had no other cause of bleeding. Gastric ulcers were diagnosed in two patients and multiple bleeding sites, typical of stress ulceration, in two others. Alcoholic gastritis and a Mallory-Weiss esophageal tear were found in one patient each. In two patients, angiography demonstrated esophageal varices but gastroscopy revealed other potential bleeding sites. A cause of bleeding was not established in six other patients with angiographic techniques. Four of these patients had stopped bleeding by the time contrast media was injected. One patient bleeding from stress ulcers and
another bleeding from gastric ulcer were not diagnosed by angiography. Of the 20 patients studied, one developed a hematoma at the site of femoral artery catheterization and one required removal of the catheter because of arterial spasm.
Intra-arterial Infusion With intra-arterial catheters selectively placed, vasopressin, 0.2-0.4 units per minute, was infused in 12 patients to control active hemorrhage. Bleeding stopped in six patients (50%) within 90 minutes of beginning infusion. Two of these patients had esophageal variceal hemorrhage. Two others had gastric ulcers. One patient with alcoholic gastritis and another with multiple stress ulcers responded to infusion. A patient with gastritis had stopped bleeding after infusion was begun but rebled when the catheter was removed accidentally five hours later. Five patients did not respond to infusion of vasopressor and required operation. Two were bleeding from varices, two from stress ulcers and one from gastritis. In neither of the stress ulcer patients was the left gastric artery catheterized successfully. Barium Roentgenographic Studies In only 11 patients (1.9%) was the exact cause of bleeding diagnosed during active hemorrhage by means of barium swallow or upper gastrointestinal series alone. Barium studies were obtained routinely in most patients after bleeding stopped. Peptic ulcer disease was diag-
100
FIG. 2. Selective angiography provided a specific diagnosis of the site of bleeding in 12 of 20 patients
(60%).
FIG. 4. The proportion of bleeding patients requiring surgery fell progressively from year one (33%) through year four (13%) of the study.
331 }
1
2Y Year
Ann. Surg. * April 1975
YAJKO, NORTON AND EISEMAN
476
FIG. 7. The primary causes of bleeding in 130 operated patients were predominantly benign peptic ulcer disease and gastritis.
FIG. 5. A preoperative diagnosis of the cause and site of bleeding was made in 65% of patients.
nosed by such studies in 90%7o of patients subsequently have ulcers. Barium swallow showed esophageal varices in 72% of patients found to have varices on endoscopic examination. Of 44 patients with acute mucosal lesions diagnosed by endoscopy, barium studies were normal in all but one.
proven to
Laparotomy Of the entire 585 patients treated for upper gastrointestinal bleeding, 130 (22%) required laparotomy for 138 episodes of medically uncontrolled hemorrhage (Fig. 3). The proportion of those operated upon fell progressively from 33% in the first year of study to 13% in the fourth year (Fig. 4). Indications for operations were: 1) transfusion of whole blood exceeding 2500 ml in the first 24 hours; 2) transfusion exceeding 1500 ml in the second 24 hours; or 3) rebleeding after 24 hours of vigorous medical therapy. Average age of the 130 patients undergoing operation was 51 years (range 15-89 years). Ninety-seven were males and 33 were females. For 45 patients (35%) who underwent operation we did not have a precise, proven diagnosis of the cause or site of bleeding (Fig. 5). The proportion of such undiagnosed patients was less in year four (15%) when endoscopy and angiography were used commonly, than in year one (43%). When the site of bleeding was unknown at the time of laparotomy, a longitudinal pylorotomy was made for inspection of the duodenum and antrum. If necessary, this was followed by transverse gastrotomy at midstomach for inspection of the corpus, fundus, cardia and distal esophagus (Fig. 6). The latter was visualized in some cases by lateral traction on one or more nasogastric tubes passed through the cardia and fixed at the nose.
1
%
%%
FIG. 6. In patients without a preoperative diagnosis ofthe cause and site ofbleeding, pylorotomy(1)
%%%
,,was "
performed first followed by
transverse
gastrotomy (2).
Cause of Bleeding in Surgical Patients The etiology of primary bleeding in 130 surgical patients is summarized in Fig. 7. Benign peptic ulcers accounted for 51% of bleeding lesions (38 duodenal and 28 gastric ulcers). Diffuse gastritis was found in 26 patients (20%), of whom 18 had recently been drinking. Of the eight other patients with gastritis four (50%'o) had been taking aspirin, phenylbutazone or corticosteroids for one week or longer. Other causes of bleeding were esophageal varices in 20 patients (15%) and stress ulceration in 10 patients (8%).Eight others (6%) had miscellaneous lesions such as anastomotic (stomal) ulcer (3), Barrett's esophageal ulcer (2), aorto-duodenal fistula (1), gastrocolic fistula (1) and hemobilia secondary to carcinoma of the gall bladder (1).
Operative Procedures Three-quarters of the 138 operations performed were selected according to our established protocol which is summarized in Table 1. In the other 25%, the surgical residents, who performed all of the operations under the active operating room guidance of a faculty surgeon, chose to violate the protocol for reasons of the patient's critical condition (25%), technical difficulties (10%) or difference in preference (65%). Results
Duodenal Ulcer-Poor Risk Twenty-three of 38 patients operated upon for duodenal ulcer bleeding were judged to be poor surgical TABLE 1. Recommended Operationsfor Specific Causes ofAcute Upper Gastrointestinal Hemorrhage
Pathology Gastritis, Alcoholic Gastritis, Non-alcoholic Duodenal Ulcer (Poor Risk) Duodenal Ulcer (Good Risk) Gastric Ulcer (Corpus-Antrum) Gastric Ulcer (Fundus-Cardia) Stress Ulcer
Esophageal Varices *Ligate bleeding vessel.
Operation Vagotomy and Pyloroplasty Vagotomy and Hemigastrectomy Vagotomy and Pyloroplasty* Vagotomy and Hemigastrectomy Vagotomy and Hemigastrectomy Vagotomy and Pyloroplasty* Vagotomy and 75%-95% Gastrectomy Porto-Systemic Shunt
UPPER GASTROINTESTINAL BLEEDING
Vol. 181 * No. 4
477
TABLE 2. Results of Primary Operations for Acute Upper Gastrointestinal Hemorrhage
Pathology
Operations
Died
Rebled
Duodenal Ulcer-Poor Risk (23) Duodenal Ulcer-Good Risk (15)
V&P (23) V&P (4) V&Hemigastrectomy (11)
5 (22%) 0 2 (18%)
2 (9%) 1 (25%)
Gastric Ulcer-Resectable (22) Gastric Ulcer-Unresectable (6)
V&Hemigastrectomy (22) V&P (4) V&Hemigastrectomy (2)
3 (14%) 0 0
Gastritis-Alcoholic (18)
V&P (12) V&Hemigastrectomy (6) V&P (5)
V&Hemigastrectomy (3)
5 (42%) 5 (83%) 1 (20%o) 0
Stress Ulcer (10)
V&P (3) V&Hemigastrectomy (4) V&Near-total Gastrectomy (3)
2 (67%) 3 (75%) 3 (100%o)
Esophageal Varices (20)
Ligation (6) Portocaval Shunt (5) Mesocaval Shunt (7) Mesocaval (H) Shunt (2)
4 (67%) 0 2 (29%) 1 (50b)
Gastritis-Non-alcoholic (8)
risks (over 65 or another life-threatening disease). All such poor risk patients underwent vagotomy and Heineke-Mikulicz pyloroplasty. In 11 patients the bleeding vessel was oversewn but in 12 others bleeding stopped without direct vessel ligation. Two poor risk duodenal ulcer patients rebled after V&P and five (22%) died within 30 days (Table 2). Duodenal Ulcer-Good Risk Of 15 good risk patients bleeding from duodenal ulcer, 11 underwent the recommended operation of vagotomy and hemigastrectomy. Two of the 11 patients (18%) died postoperatively without rebleeding (Table 2). Four protocol variant patients, considered to be good risks, had vagotomy and pyloroplasty. One rebled and required gastric resection. Of the entire 38 patients with bleeding duode-nal ulcer, three (8%) rebled and seven (18%) died within one month of operation. Mortality was 18% following both V&P (27 patients) and vagotomy and hemigastrectomy (11 patients). These statistics lend no support to adding resection to vagotomy as a life-saving procedure for duodenal ulcer hemorrhage. Gastric Ulcer-Resectable In 22 of 28 patients with bleeding gastric ulcer, the ulcer crater was in the antrum or corpus of the stomach distal to the cardia. Such lesions were excised by partial gastrectomy. No patient rebled after this operation but three (14%) died in the hospital. Gastric Ulcer-Unresectable Six other patients had bleeding ulcers in the proximal
1 (20%o)
2 (33%) 1 (14%)
stomach where partial gastrectomy could not be done without trespassing on the esophagogastric junction. The advised operation per protocol in such patients was V&P with biopsy of the ulcer and oversewing of bleeding vessels. This was done in four patients all of whom survived and none of whom rebled. In two similar patients, vagotomy and hemigastrectomy were performed without complication (Table 2). The overall experience with bleeding gastric ulcers in 28 patients resulted in a mortality rate of 11% and no postoperative rebleeding.
Gastritis-Alcoholic Eighteen patients had diffuse, superficial mucosal erosions of the gastric corpus and fundus following a prolonged alcoholic debauch. Twelve were treated as per protocol by V&P. None of these continued to bleed but five (42%) died within 30 days (Table 2) of pulmonary disease or sepsis. Protocol was broken and vagotomy and hemigastrectomy performed in six other alcoholics with gastritis. Although none of these rebled, five (83%) died in the hospital. Survival was thus twice as good when V&P were performed than when the stomach was partially resected for alcoholic gastritis.
Gastritis-Non-alcoholic Among eight patients with non-alcoholic gastritis, operative treatment was V&P in five, of whom bne rebled and later died (20%), and vagotomy and hemigastrectomy in three, none of whom rebled or died (Table 2). The overall mortality of patients requiring surgery for
gastritis was 42% (11 patients). One death followed bleeding.
re-
Esophageal Varices
Twenty patients bleeding from esophageal varices did not respond to nonoperative forms of therapy such
as
esophageal balloon tamponade or infusion of vasopressin into the superior mesenteric artery. Six such patients had transthoracic suture ligation of varices alone. Four (67%) died, two after rebleeding. Two have survived without rebleeding for more than three years (Table 2). All five patients who underwent emergency end-toside portocaval shunting survived and none has rebled during a mean followup period of 22 months. A sixth portocaval shunt was constructed in a patient who rebled after ligation of esophageal varices. This patient did not rebleed but died of liver failure after three weeks. Seven patients had mesocaval shunting for bleeding varices. In each, the iliac vein was sutured end-to-side to the superior mesenteric vein. One of these patients rebled and two (29%) died postoperatively. The five survivors have not rebled during a mean 20 months of followup. Interposition H-type mesocaval shunts were constructed in two patients during the last year of study using the Teflon derivative Gore-Tex13 as prosthetic vein. Neither patient rebled but one died of hepatic failure 10 days after operation with an open graft. In the entire group of 20 patients operated upon for bleeding esophageal varices, mortality was 35%. Three patients (15%) continued to bleed after operation and two died. Stress Ulcer
of
Ann. Surg. * April
YAJKO, NORTON AND EISEMAN
478
Ten patients had multiple gastric ulcers after the stress surgery, trauma, or sepsis. Six of the 10 developed
1975
stress ulceration in relation to sepsis. None had duodenal stress ulcers.
Seven patients had the suggested vagotomy and resection of whom six (86%) died of either respiratory insufficiency or sepsis. None had rebled prior to death. Three of the seven had near-total (85-95%) gastrectomy in an effort to remove all involved mucosa and all died postoperatively. Three stress ulcer patients underwent V&P, of whom two (67%) died. The hospital mortality of the 10 patients requiring operation for stress bleeding was 80%. No patient rebled. Among other rebleeding patients, however, stress ulcer was encountered twice. Each patient survived after subtotal gastrectomy (1) and oversewing (1). Rebleeding Fourteen of 130 surgical patients, (11%), continued to bleed or rebled after operation. Only eight (6%) required reoperation to control persistant or recurrent hemorrhage. The average age of these patients was 56 years. Each received an average 12,000 ml of blood during hospitalization. Rebleeding was due to disease not previously diagnosed in seven of the eight patients (Table 3). Three patients with duodenal ulcers initially treated by V&P rebled postoperatively and each was found to have hemorrhagic gastritis as the cause of bleeding. Of two patients who continued to bleed after ligation of esophageal varices, one had hemorrhagic gastritis and the other had variceal bleeding. A third patient primarily diagnosed as esophageal varices developed stress ulceration following mesocaval shunt and required subtotal gastrectomy. Stress ulcer was also diagnosed in a patient with primary stomal ulcer bleeding. Three of the eight patients with rebleeding died although none exsanguinated.
Discussion Massive bleeding from the upper gastrointestinal tract
TABLE 3. Rebleeding After Primary Operation for Acute Upper Gastrointestinal Hemorrhage
Patient First Diagnosis 1
Doudenal Ulcer, poor risk
First Operation
Second Diagnosis
Second Operation
V&P
Gastritis, Non-
Subtotal Gastrectomy
Died
Subtotal Gastrectomy
Lived
Subtotal Gastrectomy
Lived
Subtotal Gastrectomy
Lived
Oversew Total Gastrectomy
Lived Died
Portocaval Shunt Subtotal Gastrectomy
Died Lived
Outcome
alcoholic 2
Duodenal Ulcer, poor risk
V&P
Gastritis, Nonalcoholic
3
Duodenal Ulcer, good risk
V&P
4
Gastritis, Non-alcoholic
V&P
5 6
Stomal Ulcer Esophageal Varices
Subtotal Gastrectomy
7 8
Esophageal Varices Esophageal Varices
Ligation
Ligation Mesocaval Shunt
Gastritis, Nonalcoholic Gastric Ulcer, Resectable Stress Ulcer Gastritis, Nonalcoholic Esophageal Varices Stress Ulcer
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UPPER GASTROINTESTINAL BLEEDING TABLE 4. Summary ofResults
Disease Duodenal Ulcer Gastric Ulcer Gastritis Esophageal Varices Stress Ulcer
Satisfactory Control of Bleeding yes yes yes yes no
Satisfactory Survival yes yes no no no
479
The role of vagotomy with resection for gastric ulcer is not established9 but we favor reducing gastric acidity as well as excising distal stomach.
Gastritis
The high incidence of gastritis as a cause of massive upper gastrointestinal bleeding is increasingly recognized as endoscopy becomes more popular.1 4 Vagotomy and is a clinical manifestation of several diseases each of pyloroplasty stop bleeding in most patients with both which requires different operative and nonoperative alcoholic and non-alcoholic gastritis. Resection in the therapy. A mass reflex technical response, such as partial latter is not justified. Mortality among alcoholics with gastrectomy, no longer is sufficiently precise to be de- gastritis is high (56%) because of frequently associated sepsis, pulmonary insufficiency or metabolic disease. fensable. Sophisticated endoscopic and angiographic techniques Avoiding surgery by infusion of vasopressor into the left can now provide accurate diagnosis in the majority of gastric artery may reduce mortality. bleeders. As a result, management can be more accurately tailored to the responsible lesion. This review of Esophageal Varices our experience at the Denver General Hospital covers the period of transition in which these advances were Infusion of vasopressor into the superior mesenteric recognized and utilized. artery stops variceal bleeding in about 70% of patients.2 There can be no complacency in the management of a When infusion fails, porto-systemic shunting is indicated. disease where operative mortality is 29% even though Transthoracic suture ligation of varices is ineffective in our results are comparable to those reported from both stopping hemorrhage or reducing mortality. The shunt of municipal6 and private3 hospitals. Progress requires in- choice, on the basis of our experience, is end-to-side dentifying which lesions are treated relatively well and portocaval anastomosis. Recent use of a prosthesis as an which are managed poorly. Simplistically, both our re- interposition mesocaval shunt has been gratifying in sults and those of others could be summarized as in terms of technical ease and shortened operative time. In Table 4. a much larger group of patients, Drapanas7 has confirmed are fails often in which management present The areas this experience, making the interposition procedure our ulcer. stress and varices alcoholic gastritis, esophageal present choice in the operative treatment of varices. Rationale for choosing an operative procedure once the cause of upper gastrointestinal bleeding is known is Stress Ulcer based upon the following: Vagotomy and pyloroplasty control bleeding with acMortality after surgery for stress ulcer bleeding is ceptable mortality. It is a technically simple and rapid alarming.14 Results of Kirtley, et al.10 showing 65% surprocedure. The only argument is whether, in good risk vival after V&P have seldom been duplicated by others. patients, under ideal conditions, vagotomy and hemigas- Death after stress ulcer bleeding is often due to pretrectomy should not be perfprmed because of the lower existing disease. Thus, even near-total gastrectomy, rate of ulcer recurrence following this operation.8 Among which eliminates potential bleeding mucosa, does not our patients, mortality was the same (18%) after vag- improve survival. Still, vagotomy and high gastric resenotomy and resection as after vagotomy and pyloroplasty. tion seem more reasonable operations than V&P, which are followed by excessive rates of recurrent bleeding.11 Nonoperative management of stress ulceration by inGastric Ulcer travenous corticosteroids12 or infusion of vasopresson into the left gastric artery5 could be tried before surgery, of operative although ultimate mortality of the disease may not be Excision must remain the cornerstone Partial gastrectomy lessened. treatment of bleeding gastric ulcers. Diagnostic and therapeutic approaches to the upper and vagotomy effectively stop hemorrhage with good bleeder will continue to change in the gastrointestinal resected be which cannot survival (86%). Benign ulcers, as seventies endoscopy, angiography, infusion without destroying the cardio-esophageal junction, selective and surgery are more widely practechniques Our and drainage. should be treated first by vagotomy will be changed thereby remains Whether ticed. mortality that of number patients suggests experience in a small a that It is technique will benefit be seen. given to likely limited a such procedure. bleeding can be controlled by
YAJKO, NORTON AND EISEMAN
480
one type of bleeder but not another. Nevertheless, these new abilities make more hopeful the treatment of gastrointestinal hemorrhage in this decade.
References 1. Allen, H. M., Block. M. A. and Schuman, B. M.: Gastroduodenal Endoscopy. Management of Acute Upper Gastrointestinal Hemorrhage. Arch. Surg., 106:450, 1973. 2. Baum, S. and Nusbaum, M.: The Control of Gastrointestinal Hemorrhage of Selective Mesenteric Arterial Infusion of Vasopressin. Radiology, 98:497, 1971. 3. Connecticut Society of American Board of.Surgeons: Immediate Results of Emergency Operation for Massive Upper Gastrointestinal Hemorrhage. Am. J. Surg., 122:387, 1971. 4. Conn, H. 0. and Brodoff, M.: Emergency Esophagoscopy in the Diagnosis of Upper Gastrointestinal Hemorrhage. Gastroenterology, 47:505, 1964. 5. Conn, H. O., Ramsby, G. R. and Storer, E. H.: Selective IntraArterial Vasopressin in the Treatment of Upper Gastrointestinal
Hemorrhage.
Ann.
Surg.
*
April
1975
6. Crook, J. N., Gray, L. W., Nance, F. C. and Cohn, I.: Upper Gastrointestinal Bleeding. Ann. Surg., 175:711, 1972. 7. Drapanas, T.: Interposition Mesocaval Shunt for Treatment of Portal Hypertension. Ann. Surg., 176:435, 1972. 8. Goligher, J. G., Pulvertaft, G. N., Irvin, T. T., et al.: Five to 8 Year Results of Truneal Vagotomy and Pyloroplasty for Duodenal Ulcer. Br. Med. J., 1:7, 1972. 9. Kelly, H. G., Grant, G. W. and Elliot, D. W.: Massive Gastroduodenal Hemorrhage-Changing Concepts of Management. Arch. Surg., 87:112, 1963. 10. Kirtley, J., Scott, H., Sawyers, J., et al.: The Surgical Management of Stress. Ann. Surg., 169:801, 1969. 11. Menguy, R., Gadecz, T. and Zajtchuk, R.: The Surgical Management of Acute Gastric Mucosal Bleeding, Stress Ulcer, Acute Erosive Gastritis, and Acute Hemorrhagic Gastritis. Arch. Surg., 99:198, 1969. 12. Proudfoot, W. H., Bolick, R., Schoffstall, R., et al.: Dexamethasone Therapy for Stress Ulcer. Am. Surg., 38:638, 1972. 13. Soyer, T., Lempinen, M., Cooper, P., et al.: A New Venous Prosthesis. Surgery, 72:864, 1972. 14. Stremple, J. F., Mari, H., Lev, R. and Jerzy Glass, G. B.: The Stress Ulcer Syndrome. In Current Problems in Surgery. Chicago, Year Book Medical Publishers, 19, April 1973.
