Helicobacter pylori eradication in patients with peptic ulcer disease: clinical consequences and financial implications

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1 Quarterly Journal of Medicine, 1994; 87: Helicobacter pylori eradication in patients with peptic ulcer disease: clinical consequences and financial implications K.U. POWELL 1, CD. BELL 1, G.H. BOLTON 4, S.M. BURRIDGE 1, A.F. BOWDEN 1, B. RAMEH 1, L. HART 1, P. BRADLEY 7, G. HARRISON 2, P.W. GANT 5, P.H. JONES 5 J.E. TROWELL 3 and C. BROWN 6 From the Departments ov Medicine, 2 Medical Physics, 3 Histopathology, 4 Regional Drug Information Unit, 5 the PHLS, ^Suffolk Medical Audit Advisory Group Facilitator, 7 Audit Office, The Ipswich Hospital, Ipswich, UK Received 24 January 1994; Accepted 8 February Summary We assessed clinical consequences and financial implications of Helicobacter pylori eradication in 175 patients with peptic ulceration, of whom 106 had been free from H. pylori infection for a mean of 3.2 years, while 69 remained infected. We used quarterly questionnaires to examine consumption of ulcer-healing medication and antacids. In the 106 successfully treated patients, gastrointestinal haemorrhage as a complication of peptic ulcer complications during the 344 patient years after eradication (0.003 per patient year) was 18-fold lower than during the 912 patient years before eradication (0.056 per patient year). Of the H. py/oranegative patients, 12-18% used ulcer-healing medication during any one of the three-month periods of the survey, compared with % of the patients with residual H. pylori infection. The average cost of the ulcer-healing drugs consumed by the H. pylor'tnegative patients was during the 12 months of the survey, compared with for H. pyloripositive patients. Consumption of antacids was also lower in the H. pylori-negative group. Successful eradication of H. pylori significantly reduced the annual cost of ulcer-healing drugs consumed by the patients with ulcer disease. Maintenance of ulcer remission following successful eradication of H. pylori also significantly reduced ulcer complications. Introduction Approximately 10% of adults in westernized countries suffer from either a duodenal or gastric ulcer at some time in their lives. 1 ' 2 Moreover, four studies from the pre-h2-receptor antagonist era have demonstrated that ulcers do not 'burn ouf spontaneously, but remain active with unchanged potential for complications such as haemorrhage or perforation for several decades. 1 ' 3 ' 5 The outcome of ulcer disease is not changed by treatment with modern gastric secretory inhibitors, because peptic ulcers tend to relapse when treatment with anti-secretory drugs is stopped, even after many years of continuous therapy. 6 " 8 In order to keep ulcers in sustained remission, treatment with gastric secretory inhibitors must therefore be not only continuous but also very long-term, and is consequently very expensive. Even if compliance is satisfactory, some ulcers recur during adequate maintenance therapy. 9 In any case, most ulcer patients do not receive prophylactic continuous maintenance treatment but, instead, intermittently receive courses of treatment on recurrence of symptoms, or even use gastric secretory inhibitors as antacids are used, 'on demand' or as 'self-care', 10 for a few days while symptoms persist. The drug costs of intermittent therapy are less than those of continuous treatment, but ulcer complications are not prevented by intermittent courses of ulcer-healing therapy. 11 Helicobacter pylori and non-steroidal antiinflammatory drugs (NSAIDs) are currently thought Address correspondence to Dr CD. Bell, Department of Medicine, The Ipswich Hospital, Ipswich, Suffolk IP4 5PD Oxford University Press 1994

2 284 K.U. Powell etal. to be the two most important exogenous factors in the aetiology of peptic ulcer disease. 12 There is now strong evidence that H. pylori eradication reduces duodenal ulcer relapse, and may even cure the disease completely. 13 " 22 However, most of the studies have only followed the treated patients for one or two years after eradication, and many clinicians are reluctant to stop maintenance therapy in patients whose ulcers have been complicated by haemorrhage or perforation, 9 ' 23 despite some reassuring early reports. 24 In calculating the financial impact of H. pylori eradication, most authors, including ourselves, 25 have used some form of mathematical modelling to predict possible savings. Such models assume that the patients and their medical advisors are prepared to discontinue treatment with H2-receptor antagonists, and that symptoms of gastro-oesophageal reflux are not experienced, since the latter may require continuation of the gastric inhibitory therapy. We calculated that H. pylori eradication therapy should theoretically cost only about one-tenth as much as continuous maintenance therapy during a five-year period, but pointed out 25 that the overall cost of H. pylori eradication might be similar to intermittent therapy if a significant number of patients continued consumption of gastric inhibitory drugs. In August 1991, we decided to audit prospectively the ulcer-healing drug consumption of a group of 106 ulcer patients in whom confirmed H. pylori infection had been successfully eradicated at least one year before the study. For comparison, we also studied the consumption of ulcer-healing drugs by 69 ulcer patients in whom infection persisted. Methods Ethical approval for the study, and informed consent from all patients was obtained. The patients' general practitioners (GPs) were informed by letter of the nature of the study and permission was requested to study the patients during the ensuing 12 months. Patients and GPs were informed that if H. pylori infection had been successfully eradicated, the likelihood of ulcer relapse was greatly reduced. However, it was emphasized that the individual GPs were completely free to prescribe as and when they considered necessary throughout the period of the study. Two groups of patients were recruited between August 1991 and August All patients had originally suffered from a confirmed duodenal or gastric ulcer associated with a proven H. pylori infection. All were judged to be of sound mind, and capable and willing to complete a questionnaire every three months for a year. An explanatory letter was provided with each questionnaire including instructions on how to complete the forms, where to return them to and a contact telephone number to answer any queries. Group I was composed of patients with successful H. pylori eradication. The 106 patients comprising this study group had been shown to be persistently free from reinfection with H. pylori by use of the u C-urea breath test (UBT). Group II was composed of patients with persistent H. pylori infection. The criteria for inclusion of the 69 patients in this group included (1) failure of previously attempted eradication therapy or (2) absence of previous eradication therapy. Patients were asked to undergo a UBT at the beginning and end of their 12-month period of observation to document H. pylori status. A UBT result of <40 for the two-hour area under the curve (AUC) was considered to indicate absence of H. pylori infection while a two-hour AUC >40 indicated H. pylori infection. 26 Patients also completed a questionnaire every three months during the 12-month study period, detailing their use of (1) prescribed ulcer-healing drugs; (2) prescribed antacids; and (3) over-thecounter (OTQ antacids. Patients who had used ulcerhealing drugs during the 12-month study period were asked, at the end of the study year, to complete a further form as to the reason for taking the drug(s) (Table 1). Sufficient information was provided by the forms to calculate accurately the cost of each patient's prescribed ulcer therapy. Drug costs were calculated using community prices. For prescribed proprietary medications, prices were derived from the Monthly Index of Medical Specialties (MIMS) and for generic preparations, prices were obtained from the Drug Tariff. Prices were reviewed throughout the study period, and major changes were included in calculating the drug costs. The four questionnaires were supplied to each Table 1 End of year patient questionnaire You have reported that you have been using or are still using an ulcer-healing drug. I would be grateful if you could tick the reasons that best apply to you. 1. Recurrence of ulcer symptoms if tablets not taken regularly 2. Recurrence of heartburn/acid reflux 3. No symptoms but you want to take if anyway to prevent further trouble 4. You are also taking tablets for arthritis, steroids or warfarin 5. Your CP has advised you to take it regularly 6. Other reason

3 Consequences of H. pylori eradication 285 patient at the start of the study. Each questionnaire was dated and provided together with a stamped, addressed envelope, to be returned at the end of every three-month period. Compliance was excellent, but patients were reminded by telephone if the reply was late. The hospital case notes and GP referral letters, plus direct questioning of the patient, were used to establish as accurately as possible (1) when the patient first experienced symptoms; (2) when a firm diagnosis of ulcer disease was established either by barium meal or endoscopy; (3) the total length of ulcer history up to confirmation of H. pylori eradication, or, if the patient remained H. py/on-positive, up to the start of the study; (4) whether the patient's ulcer had at any time been complicated by haemorrhage or perforation; and (5) whether the ulcer had recurred despite previous gastric anti-ulcer surgery. The number of years of observation after H. pylori eradication was noted for each patient, and in both groups the total and mean number of years of observation were calculated. During the 12-month study period, all episodes of gastrointestinal bleeding, perforation or admission to hospital with ulcerrelated problems were recorded. In patients of Croup I, similar information was obtained for the entire post-eradication period. At the end of the 12-month period, those patients of Group II who remained H. py/on-positive were asked if they wished to attempt H. pylori eradication and, if successful, to complete further forms every three months for an additional six-month period to assess the impact of H. pylori eradication. Data handling A simple database (using Dbase IV) was constructed to record the patient details, diagnosis of duodenal ulcer, gastric ulcer, hiatal hernia, H. pylori status, ulcer-healing drug usage and drug costs. The database was divided into three-monthly sections for sequential analysis. Statistical methods Descriptive statistics or the /f 2 test with Yates correction were used to compare and contrast Group I and Group II patients. Results Clinical comparisons The return of the forms was excellent (100%) allowing for those patients who died, moved out of the area or, in one case, failed to complete one three-month form while he was an in-patient undergoing lobectomy for carcinoma of the lung. Croup I: peptic ulcer patients after eradication A total of 106 peptic ulcer patients (87 duodenal ulcer, 19 gastric ulcer) were studied, with M/F ratio of 75/31 and mean (SD) age of 59.8 (12.9) years. The mean length of ulcer history up to the time of H. pylori eradication was 8.6 years, and thus the total period of observation (ulcer symptoms) was 912 patient years. During this time, 32/106 (30.2%) patients had suffered from at least one episode of bleeding from a peptic ulcer. The total number of episodes of ulcer haemorrhage (diagnosed endoscopically) during the 912 patient years was 51, a rate of patients per year. Before eradication, two patients (1.9%) had suffered from ulcer perforation requiring surgery and one patient had had a bleeding ulcer oversewn. A further patient had previously undergone truncal vagotomy for duodenal ulceration. All four patients developed further ulceration after surgery. During the 12-month follow-up period, two patients died (one from a cerebrovascular accident and one from a myocardial infarction), both during the last three months of the study. One patient moved away from the area and was lost to followup. At the beginning of the 12-month study, all 106 patients had a negative UBT with a mean (SD) twohour AUC of 15.4 (5.6). After 12 months, 103 patients had a repeat UBT, and all remained unequivocally negative with a mean UBT (SD) AUC of 15.9 (6.8). The total number of years of observation after H. pylori eradication of the 106 patients (including the patients who died) was 344 years, with a mean post-eradication period of observation of 3.2 years (range 23 months to 6 years). During this time, no patient experienced either an ulcer perforation or required ulcer surgery. Only one patient had a confirmed peptic ulcer haemorrhage. He was a 61-year-old man with rheumatoid arthritis, who had originally had a bleeding duodenal ulcer oversewn in His second haemorrhage occurred in 1992, 3-4 years after H. pylori eradication, but he was still taking prednisolone, NSAIDs and a maintenance dose of cimetidine. A further patient with a history of both a duodenal ulcer and hiatal hernia suffered a small haematemesis not requiring transfusion, and was found at endoscopy to have oesophagitis. Two other patients had melaena while taking aspirin, and in both patients the bleeding was caused by gastric erosions and not recurrence of the peptic ulcer. One of these patients had also been taking a maintenance dose of ranitidine. The rate of haemorrhage from peptic ulcer was 18-fold lower following eradication of H. pylori,

4 286 K.U. Powelleta\. with the rate of haemorrhage falling from patients per year to a rate of patients bleeding per year (i.e. one bleed in 344 patient years of observation). Croup II: patients in whom H. pylori was not eradicated A total of 69 patients (58 duodenal ulcer, 11 gastric ulcer) were studied, with M/F ratio of 48/21 and a mean (SD) age of 59.5 (13.8) years. The mean length of the ulcer history to the beginning of the study was 10.2 years, and the total period of observation was 704 patient years. During this time, 18/69 patients (26.1%) had suffered from at least one haemorrhage from an ulcer. The total number of episodes of ulcer bleeding during the 704 patient years was 24, equivalent to a rate of patients per year. Before the start of the study one patient (1.4%) had suffered from an ulcer perforation requiring surgery. A further two patients had previously undergone either truncal vagotomy or highly selective vagotomy for a duodenal ulcer. All three patients developed recurrent ulceration after surgery. During the 12-month follow-up period, two patients died, one as a result of a ruptured aortic aneurysm and one from a cerebrovascular accident. Both events occurred during the first three months. Two patients moved away and were lost to followup. One patient had a pulmonary lobectomy for a bronchial neoplasm and his questionnaire form was not available for one three-month period. The latter was the only patient in whom the UBT changed from positive to negative during the study, perhaps as a result of the antibiotic cover for the operation. At the beginning of the study, all 69 patients had a positive UBT with a mean (SD) two-hour AUC of (74.4). At the end of the study, 64 patients had a repeat UBT and all but one remained strongly positive with a mean (SD) AUC of (72.9). During the 12-month follow-up period, representing a total of 66 patient years of observation, two patients bled from a peptic ulcer, one of whom required transfusion. Two further patients were admitted with severe abdominal pain and vomiting, in both cases with an endoscopically-confirmed active duodenal ulcer and no other cause for the symptoms. One of the latter patients subsequently had successful eradication therapy and was withdrawn from the study. No patient had an ulcer perforation and no ulcer surgery was required during the period of observation. The gastrointestinal bleeding rate from peptic ulcer thus remained unchanged during the year of observation from a rate of patients bleeding per year before observation compared with a rate of patients bleeding per year during the 12 months of observation. Financial comparisons The percentage of Croup I patients (H. pylorinegative) taking ulcer-healing drugs during any of the three-month periods of the study year was 12-18%, compared with 34-51% for Croup II (H. py/o/7-positive) (Figure 1). The average cost for one year's supply of these drugs for an H. pylori-negative patient was 30.59, compared with for an H. py/on'-positive patient (Figure 2). The percentage of H. pylori-negative patients taking prescribed antacids in any three-month period ranged from 6.6% to 13% and cost, on average, 2.95 for the year (Table 2). The percentage of H. py/on'-positive patients taking prescribed antacids ranged from 20% to 27% and cost, on average, 4.52 for the year. As a measure of symptomatology, it is interesting to note that self-administered OTC medications were 1-3 (106/65) 4-6 (106/61) 1-8 (106/64) 9-12 (103/64) Tiie 11 lobthi (Nutxr of pitienti in Group 1/11) Helicotucter pylori-ie{»tive Helicobtcter pylon-poutue Figure 1. Proportion of patients given ulcer-healing drugs per three-month period. Tmt it loathi Total Htlicobacter pylori-nfjitttt Helicobacter pylori-positive Figure 2. Mean cost per patient of ulcer-healing drugs per three-month period.

5 Consequences of H. pylori eradication 287 Table 2 Mean cost ( ) of prescribed antacids per patient for each three-month period Group Months Total (12 months) 1 (H. pylori ve) II (H. pylori +ve) Table 3 Group Proportion of patients buying OTC antacids during each three-month Months period No. No. No. No. I (H. pylori -ve) 26/106 25% 24/106 23% 20/106 19% 16/103 16% II (H. pylori +ve) 26/69 38% 16/67 24% 25/64 39% 31/64 48% taken by 16-25% of H. py/on-negative patients and by 24-48% of H. py/on-positive patients during the year (Table 3). Table 4 shows the frequency of use of the ulcerhealing drugs; 46% of H. py/on-negative patients and 40% of H. py/o/7-positive patients were on fulltime maintenance therapy. The remaining patients used drugs intermittently. Table 5 lists the reasons for taking ulcer-healing drugs at any time during the 12-month study period. Of the H. py/on-negative patients, 22.6% took these drugs, compared with 53.6% of H. py/on-positive patients; there was a statistically significant difference in the number of patients requiring drugs for recurrence of ulcer symptoms (12.5% and 51.3% of H. py/on-negative and -positive patients, respectively). Of the patients taking drugs for heartburn or reflux, the majority had hiatal hernias. A small minority took ulcer-healing drugs prophylactically because of concomitant warfarin, aspirin or NSAID therapy. Of the asymptomatic H. py/on-negative patients, 37.5% Table 4 Ulcer-healing drug usage One quarter Two quarters Three quarters Intermittent usage Continuous usage (All 4 quarters) Quarterly usage of ulcer-healing drugs Group I (H. pylori ve) No. % 33% 17% 4% 54% 46% Group II (/-/. pylori + ve) No. % % 20% 15% 60% 40% took anti-ulcer drugs for reassurance or on advice of their GPs. Follow-up of Group II patients after H. pylori eradication At the time of writing (November 1993), 49 of the H. py/on-positive patients who had completed the 12-month study have been followed up for at least three months following successful eradication and 36 of them have been followed up for six months. These patients were given additional forms to complete during the following six months. Table 6 shows the results to date. The percentage of patients taking ulcer-healing drugs and the costs involved approximate more closely to those of the H. py/on-negative patients in Group I than those in Group II {H. pyloripositive). Discussion In studies before 1976 (i.e. before the introduction of H2-receptor antagonists), the proportion of patients bleeding from peptic ulcers increased with the duration of the individual ulcer history. Within 10 years of the diagnosis, the percentage of bleeding from ulcers was approximately 15%, while after 20 years, the proportion affected 20-40%. 27 If a peptic ulcer patient had already suffered from ulcer haemorrhage, the risk of a second bleed was approximately 15% within three years and by 10 years might be as high as 50%. 9 Perforation of ulcers is less common, but pre-1976 data indicated that 5-10% of ulcer patients might suffer from perforation within 10 years. 27 In view of these dangers, many gastroenterologists have

6 288 K.U. Powell etal. Table 5 Reasons for use of ulcer-healing drugs Reason Croup 1 No. Croup II No. % Recurrence of ulcer symptoms 3/24* Heartburn/acid reflux 9/23 Asymptomatic but for reassurance 3/24 To cover usage of other drugs (e.g. aspirin or NSAIDs) 4/24 Asymptomatic but on GP's advice 6/24 Total usage of ulcer-healing drugs during the year 25/106* /37 10/37 0/37 4/37 5/37 37/ *p<0.01. **p< Table 6 Patients who had H. pylori successfully eradicated after study subsequently followed up at three and six months post-eradication Three months Six months Cost of ulcer-healing drugs ( ) Total cost Cost per patient Cost of prescribed antacids ( ) Total cost Cost per patient Patients taking ulcer-healing drugs Patients on prescribed antacids Patients taking OTC medication /49 (16%) 7/49 (H%) 6/49 (12%) strongly recommended long-term continuous (maintenance) therapy with gastric secretory inhibitors as the optimal treatment both for suppressing symptoms and reducing the risk of ulcer complications. 9 ' 27 In this study, the rebleeding rates for Group II patients were very similar before and after the 12-month study (0.033 and episodes of ulcer haemorrhage per patient year). However, the rate of haemorrhage for patients in Group I was significantly reduced after eradication of H. pylori (0.056 vs episodes per patient year before/after eradication, respectively). The latter rate is similar to that for ulcer haemorrhage during long-term continuous treatment with ranitidine. 28 Our group in Ipswich has studied H. pylori eradication since ' 30 As previously discussed, 29 we have used the non-invasive 14 C-UBT to monitor the success or failure of treatment designed to eradicate H. pylori infection. Although a negative UBT one month after treatment usually predicts true eradication of the organism, a few patients may show late recrudescences during the first year after apparently successful eradication. 31 If, however, the UBT is still negative one year after treatment, the reinfection rate is less than 0.5% per patient year of observation. To date, we have successfully eradicated /36 (22%) 7/36 (19%) 6/36 (16%) H. pylori infection from >700 patients with either peptic ulcer disease or non-ulcer dyspepsia. These patients have undergone further UBTs at 6 months, 12 months and then annually after eradication, so that it has been possible to recruit a relatively large group of H. py/ori-negative peptic ulcer patients during a period of one year. All H. py/on-negative patients remained negative during this study, confirming our previous results of low reinfection rates, and all except one H. py/on-positive patient remained positive, confirming that spontaneous eradication is rare. In this study, eradication of H. pylori infection reduced by two-thirds the cost in terms of annual prescription of ulcer-healing drugs ( compared with 99.05) and antacids ( 2.95 compared with 4.52) (Figure 2 and Table 2). The H. py/on-negative patients who did not receive prescribed ulcer-healing drugs or antacids appear not to have taken more OTC unprescribed medication, suggesting that these patients have generally been free from symptoms (Table 3). It is interesting that ulcer-healing drugs were still being used after eradication of H. pylori in a considerable proportion of patients (22.6%) (Table 5). Onethird of this usage was attributable to symptoms of

7 Consequences of H. pylori eradication 289 gastro-oesophageal reflux. Some of the prescribing of ulcer-healing drugs (37.5%) was for asymptomatic patients, and reflected fear of potential ulcer recurrence either by the patient or by the CP. Our previously published theoretical model of the financial savings attributable to therapeutic eradication of H. pylori infection 25 must therefore be modified in the light of the practical findings of the present study. In the extension of the study to Group II patients, following further treatment to ensure H. pylori eradication, the costs of drugs required for the first two three-month periods after eradication were 6.99 and 7.70, respectively. These values approximate closely to the costs for Group I patients. In conclusion, the present study has shown that eradication of infection with H. pylori significantly reduces the incidence of symptomatic ulcer recurrence during a three-year period, and is as effective as maintenance therapy at preventing complications such as ulcer bleeding and perforation during this time. We feel that further cost savings could be made as the confidence of patients and GPs in the long-term efficacy of eradication treatment increases. Acknowledgements We would like to acknowledge Mrs Pat Lamb in the Nuclear Medicine Department of the Ipswich Hospital for her help with the breath tests, and both the Suffolk Branch of the British Digestive Foundation (KUP) and the Astra Foundation for financial support. References 1. Pulvertaft CN. Incidence and natural history of gastric and duodenal ulcer. Postgrad MedJ 1968; 44: Monson RR, MacMahon B. Peptic ulcer in Massachusetts physicians. N EngI Med 1969; 281: Krause U. Long-term results of medical and surgical treatment of peptic ulcer. Acta Chir Scand 1963; 125: Krag E. Long-term prognosis in medically treated peptic ulcer. Acta Med Scand 1966; 180: Viskum A. A comparison of the course of the disease among patients with gastric ulcer, duodenal ulcer and ulcer dyspepsia without ulcer demonstrable by X-ray. Dan Med Bull 1976; 23: Salera M, Taroni F, Miglioli M, et al. Long-term effects and after-effects of cimetidine in duodenal ulcer patients. Ital J Castroenterol 1979; 11: Boyd EJS, Wilson JA, Wormsley KG. Safety of ranitidine maintenance treatment of duodenal ulcer. Scand J Castroenterol 1984; 19: Penston JC, Dixon JS, Boyd EJS, Wormsley KG. A placebocontrolled investigation of duodenal ulcer recurrence after withdrawal of long-term treatment with ranitidine. Aliment Pharmacol Ther 1993; 7: Penston JG, Wormsley KG. Review article: maintenance treatment with H2-receptor antagonists for peptic ulcer disease. Aliment Pharmacol Therap 1992; 6: Pounder RE, Festen H, Korman M. The long-term management of duodenal ulceration using an H2-antagonist: symptomatic self-care compared with maintenance treatment. Aliment Pharmacol Ther 1992; 6: Damman HG, Walter TA. Efficacy of continuous therapy for peptic ulcer in controlled clinical trials. Aliment Pharmacol Trier 1993; 7: Taha AS, Russell Rl. Helicobacter pylori and non-steroidal anti-inflammatory drugs: uncomfortable partners in peptic ulcer disease. Cut 1993; 34: Coghlan JG, Gilligan D, Humphries H, era/. Campylobacter pylori and recurrence of duodenal ulcers: a 12-month follow-up study. Lancet 1987; ii: Lambert JR, Borrmeo M, Korman MG, Hansky J, Eaves ER. Effect of colloidal bismuth (DeNol) on healing and relapse of duodenal ulcers: role of Campylobacterpyloridis. Gastroenterology 1987; 92: Marshall BJ, Goodwin CS, Warren JR, et al. Prospective double-blind trial of duodenal ulcer relapse after eradication of Campylobacter pylori. Lancet 1988; ii: Borody TJ, Cole P, Noonan S, er al. Recurrence of duodenal ulcer and Campylobacter pylori infection after eradication. Med J Ausf\989; 151: Rauws EA, Tytgat GNJ. Eradication of Helicobacter pylori cures duodenal ulcer. Lancet 1990; i: George L, Hyland L, Morgan A, ef al. Smoking does not contribute to duodenal ulcer relapse after eradication. Gastroenterology 1990; 98:A Coelho LGV, Passos MCF, Chausson Y, et al. Duodenal ulcer and eradication of Helicobacter pylori in a developing country. An 18-month follow-up study. Scand J Castroenterol 1992; 27: Graham DY, Lew GM, Klein PD, et al. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer: a randomized, controlled study. Ann Intern Med 1992; 116: Bayerdorffer E, Mannes G, Sommer A, ef al. Longterm follow-up after Helicobacter pylori eradication with combined omeprazole and amoxycillin treatment Vth Workshop on Gastroduodenal Pathology and Helicobacter pylori. 5-7th July 1992, Dublin, Ireland. Irish J Med Sci 1992; T Hentschel E, Brandsttter G, Dragosics B, et al. Effect of ranitidine and amoxicillin plus metronidazole on the eradication of Helicobacter pylori and the recurrence of duodenal ulcer disease. N Eng) Med 1993; 328: Boyd EJS, Penston JG, Wormsley KG. Maintenance therapy in duodenal ulcer and gastric ulcer disease. A survey of practice among British gastroenterologists. Aliment Pharmacol Ther 1992; 6: Hepps KS, Ramirez FC, Lew GM, Saeed JA, Graham DY. Treatment of Helicobacter pylori reduces the rate of rebleeding in complicated peptic ulcer disease. Castrointest Endosc 1992; 38:234 (abstract). 25. Bell GD, Powell KU, Bolton G, Richardson PDI. Clinical and pharmoeconomical evaluation of management strategies for duodenal ulcer disease. Brit] Med Econ 1993; 6:45-58.

8 290 K.U. Powell et al. 26. Weil J, Bell CD, Harrison G. 14C-urea breath test for Campylobacterpylon. Cut 1989; 30: Dobrilla C, Zancanella L, Amplatz S. The need for longterm treatment of peptic ulcer. Aliment Pharmacol Ther 1993; 7: Penston JC, Wormsley KG. Nine years of maintenance treatment with ranitidine for patients with duodenal ulcer disease. Aliment Pharmacol Ther 1992; 6: Bell GD, Powell KU, Burridge SM, etal. Helicobacter pylori eradication: efficacy and side effect profile of a combination of omeprazole, amoxycillin and metronidazole compared with four alternative regimens QJ A-)ecM993; 86: Bell GD, Powell KU, Burridge SM, etal. Does a previous course of tripotassium dicitrato bismuthate affect the subsequent chances of successful Hehcobacter pylori eradication? Aliment Pharmacol Ther 1992; 6: Bell GD, Powell KU, Burridge SM, etal. Reinfection or recrudescence after apparently successful eradication of Helicobacter pylor'r. implications for treatment of patients with duodenal ulcer disease. QJ /Wed 1993; 86:

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