Helicobacter pylori eradication and peptic ulcer healing: the impact of deleting the proton pump inhibitor and using a once-daily treatment

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1 Aliment Pharmacol Ther 2003; 18: doi: /j x Helicobacter pylori eradication and peptic ulcer healing: the impact of deleting the proton pump inhibitor and using a once-daily treatment T-U. WHEELDON*, T. T. H. HOANG à, D. C. PHUNG, A. BJÖRKMAN*, M. GRANSTRÖMà & M. SÖRBERG* *Division of Infectious Diseases, Department of Medicine, Karolinska Hospital, Karolinska Institutet, Stockholm, Sweden; National Institute of Hygiene and Epidemiology, Hanoi, Vietnam; àmtc, Clinical Microbiology, Karolinska Hospital, Karolinska Institutet, Stockholm, Sweden Accepted for publication 30 April 2003 SUMMARY Aim: To compare cheaper and simpler once-daily regimens, with and without a proton pump inhibitor, with standard, twice-daily, triple therapy. Methods: A randomized, placebo-controlled, treatment trial in Vietnam allocated 296 Helicobacter pyloriinfected patients with peptic ulcer of 5 mm to one of three regimens: (i) twice-daily: lansoprazole 30 mg, clarithromycin 250 mg and tinidazole 500 mg; (ii) once-daily: lansoprazole 60 mg, clarithromycin 500 mg and tinidazole 1000 mg; (iii) once-daily: placebo, clarithromycin 500 mg and tinidazole 1000 mg. H. pylori status was assessed by culture and immunoblot, ulcer healing by endoscopy and side-effects by structured questionnaires. Results: Per protocol eradication (N ¼ 256) was higher with standard therapy (87%) than with once-daily therapy (72%), and both were better than once-daily therapy without proton pump inhibitor (39%). Per protocol ulcer healing after standard therapy (83%) was not significantly better than that after once-daily therapy (73%), but better than that after therapy without proton pump inhibitor (65%). Side-effects were reported at similar rates in all groups. Conclusions: Proton pump inhibitor was needed for optimal eradication and ulcer healing. Twice-daily administration showed improved success rates when compared with once-daily therapies. Peptic ulcer healing was achieved even in patients treated with antibiotics only, confirming the central role of H. pylori in the pathophysiology of peptic ulcer disease. INTRODUCTION Helicobacter pylori infection is the principal cause of nonautoimmune chronic gastritis 1 and is associated with gastric cancer. 2 Eradication of H. pylori prevents the relapse of duodenal ulcer 3 and gastric ulcer, 4 and treatment of the infection has therefore become standard practice for peptic ulcer disease. 5 The most common treatment regimens for the eradication of H. pylori infection in the industrialized world are twice-daily Correspondence to: Dr T-U. Wheeldon, Division of Infectious Diseases, Karolinska Hospital, Stockholm, Sweden. Uyen@onetel.net.uk triple therapies, using a proton pump inhibitor or bismuth in combination with two antibiotics, such as clarithromycin or amoxicillin and metronidazole/ tinidazole. 6 9 A once-daily administration regimen could potentially improve patient compliance. In addition, our in vitro studies have suggested that high doses and long dosing intervals could prevent the development of antibiotic resistance. 10 The deletion of the proton pump inhibitor would benefit patients in terms of simplified treatment and cost reduction. The importance of the proton pump inhibitor for the eradication of H. pylori in patients with peptic ulcer disease has been shown in one clinical study, 11 Ó 2003 Blackwell Publishing Ltd 93

2 94 T-U. WHEELDON et al. but this study did not address whether eradication without a proton pump inhibitor may also lead to peptic ulcer healing. Considering the impact of these issues, especially for developing countries such as Vietnam in which H. pylori infection and peptic ulcer disease represent major public health problems, 12, 13 further studies are needed. Thus, in the present study, we compared the efficacy of an experimental once-daily treatment regimen with standard triple therapy administered twice daily. In addition, we investigated the relative importance of the proton pump inhibitor in H. pylori eradication and peptic ulcer healing by comparing an antibiotics-only treatment with triple therapy. MATERIALS AND METHODS Study design The study was performed in Hanoi, Vietnam. All in- and out-patients routinely admitted to the endoscopy unit of the Bach Mai Hospital, a regional general hospital for the northern provinces, were eligible for the trial. Patients aged years with a peptic ulcer of 5 mm and positive rapid urease test were included. All patients gave informed consent. Exclusion criteria included allergy to the study medication, antibiotic consumption in the previous 2 weeks, pregnant or breast-feeding women, systemic or malignant disease and bleeding peptic ulcer. Patients were recruited between 31 May 1999 and 19 April The study was a randomized, prospective, three-arm, parallel-group, placebo-controlled clinical trial that was double blind between the two once-daily treatment groups. The allocation of patients to the treatment groups (Table 1) proceeded prospectively on the basis of a computer-generated randomization list in blocks of 10. The endoscopists and laboratory staff who carried out the analysis were blind to the treatment allocation. The study drugs were pre-packed and randomized by Apoteksbolaget AB, Stockholm, Sweden. The code was kept sealed until the trial was over and all statistical analyses had been completed. The medication was taken orally for 7 days. In order to prevent unnecessary discomfort, the once-daily medication was taken in the evening, before bedtime. The trial drug packages were returned at the follow-up visit and compliance was controlled by counting any remaining tablets and interviewing the patients. More than 10% of remaining medication was considered as non-compliance. Patients participating in the study were not allowed to take any antacid or antibiotic medication other than the trial medication until the follow-up visit. If treatment for any other condition occurred before the follow-up visit, or if any questions and concerns arose before this appointment, the patients were advised to contact the investigating team by telephone or through a personal visit. Treatment efficacy was evaluated by follow-up endoscopy, 30 days after the start of treatment. If an H. pylori-positive rapid urease test was found at followup, the patient was offered, free of charge, another treatment with amoxicillin, 1 g twice daily, tinidazole, 500 mg twice daily, and lansoprazole, 30 mg twice daily, for 7 days. Repeat follow-up endoscopy was offered after another 30 days. Endoscopic examination and sampling Nine gastroenterologists and experienced endoscopists at the Bach Mai Hospital carried out the upper endoscopic examinations on an alternate schedule. Therapy Table 1. Treatment regimens LCT 2 LCT 1 PCT 1 Dosage Twice daily Once daily in the evening PPI Lansoprazole Lansoprazole 30 mg 2 30 mg Antibiotics 1 Clarithromycin Clarithromycin 250 mg mg Antibiotics 2 Tinidazole Tinidazole 500 mg mg Once daily in the evening Placebo 2 Clarithromycin mg Tinidazole mg PPI, proton pump inhibitor.

3 EXPERIMENTAL TREATMENT OF H. PYLORI AND PEPTIC ULCER 95 Biopsy specimens from the corpus, 10 cm from the cardia, and from the antrum, 1 2 cm proximal to the pylorus, were taken for rapid urease test and culture of H. pylori at each endoscopy session. A venous blood sample was collected (Vacutainer with gel, Medicarrier, Spanga, Sweden) and the serum was stored at ) 20 C until analysis for antibodies against H. pylori. Samples were stored at the National Institute of Hygiene and Epidemiology, Hanoi, Vietnam. Culture and immunoblot analyses were performed at the Department of Microbiology, Karolinska Hospital, Stockholm, Sweden. Rapid urease test Urea solutions were pre-mixed and individually refrigerated in Eppendorf tubes. A drop of 1% phenol red (Lachema, Prague, Czech Republic) was added prior to use. One biopsy from the antrum and one from the corpus were immediately placed in the test solution. The result was read within 1 h. 14 Microbiology The antrum and corpus biopsies were placed into separate, labelled and sterile plastic tubes with 0.25 ml sterile transport medium containing casamino acid, bactopeptone, yeast extract, NaCl, agar, l-cysteine, glucose, Elga water and glycerol (in-house recipe, Department of Microbiology, Linköping University, Linköping, Sweden). The sealed tubes were immediately frozen to ) 70 C in CO 2 ice. Biopsies from the rapid urease test were also saved as back-up. The biopsies were homogenized with some of the transport medium and inoculated on to pre-reduced blood agar and Campylobacter agar base with 5% lysed horse blood supplemented with vancomycin, polymyxin B and para-2-trimetoprim. The plates were incubated under micro-aerobic conditions (CampyGen, Oxoid Ltd., Basingstoke, UK) and inspected on days 3 and 7. H. pylori growth was identified as Gram-negative curved rods producing catalase, urease and oxidase. Immunoblot All sera were tested by immunoblot analysis, using the commercially available HelicoBlot 2.1 (Genelabs, Singapore) for the detection of immunoglobulin G antibodies against H. pylori-specific antigens, including an unspecified current infection marker. All buffers, reagent, positive and negative controls were supplied with the kit and used according to the manufacturer s instructions. Positive results were interpreted according to the manufacturer s recommendations and sera not fulfilling the criteria were classified as negative. The accuracy of immunoblot has been evaluated and validated previously, showing a sensitivity of 95.8% and a specificity of 94.6%. 15 Per protocol definition of H. pylori status The presence of H. pylori was determined by rapid urease test, a positive reaction being an inclusion criterion. Confirmation of H. pylori infection was based on positive culture and, in cases in which the culture was negative, on positive immunoblot. If both culture and immunoblot were negative, the patient was considered to be H. pylori negative. At follow-up, the eradication end-point was a negative H. pylori status, based on both a negative culture and a negative rapid urease test. If culture was positive, the patient was considered to be H. pylori positive, irrespective of the rapid urease test result. In the case of a negative or missing culture result, but a positive rapid urease test, the result was considered to be inconclusive and the patient was included as H. pylori positive in the intention-to-treat analysis, but excluded from the per protocol analysis. Recording of adverse events The six most common adverse effects of the trial medication, i.e. burning sensation of the mouth, burning sensation in the reproductive areas, headache, bitter taste in the mouth, metallic taste in the mouth and skin rash, were explained to the study patients. The patients were given a diary in which the side-effects were pre-printed and were advised to tick the appropriate boxes if the events occurred during treatment, and also to note any other unexpected symptoms that might appear. The diary was returned to the investigators at the follow-up visit. Statistical considerations and analyses The number of patients was based on calculations using the chi-squared test for proportions to provide a power of 85%. Estimating an average eradication rate for the three independent groups of 85%, we considered a

4 96 T-U. WHEELDON et al. difference equal to or greater than from 75% to 90% as clinically important. The alpha level was defined as Data were analysed using the chi-squared test, with the eradication rates, ulcer healing rates and side-effects compared between the treatment groups. In order to explore the impact of possible confounding factors due to inequalities between the treatment groups with regard to prognostic indicators, we also performed multiple logistic regression analysis with the odds ratio (OR) as the measure of the effect. Ethical clearance The study was approved by the Karolinska Hospital Ethics Committee in Sweden (Dnr ), the Medical Products Agency in Sweden (Dnr 154:1/99) and the Ethical Committee of the National Institute of Hygiene and Epidemiology in Vietnam. RESULTS Study population An initial 296 patients were included and randomized to the respective treatments. One patient was later diagnosed with gastric cancer and excluded from all further analysis. The baseline characteristics of the remaining 295 patients were similar between the treatment groups (Table 2). H. pylori infection at inclusion was confirmed in 290 patients. Confirmation was based on positive culture for H. pylori in 273 patients and on positive immunoblot in 17 patients. Table 2. Baseline characteristics Treatment group* LCT 2 (N ¼ 99) LCT 1 (N ¼ 97) PCT 1 (N ¼ 99) Age (years) Range Median Gender (%) Female Male Location of ulcer (%) Duodenal Gastric Multiple History of previous ulcer (%) * Treatment regimens given in Table 1. After treatment, 18 patients failed to return for followup. Three died from causes unrelated to peptic ulcer and its treatment (one of end-stage renal failure, one of liver cirrhosis and one of motor neurone disease). Five withdrew for other unrelated illnesses, eight had moved and two withdrew due to allergic reactions. Six sets of follow-up biopsies were lost by inadvertent thawing in Vietnam. Another 10 patients had inconclusive H. pylori results, i.e. negative culture but positive rapid urease test, after treatment. Thus, 256 patients remained for the per protocol analysis (Figure 1). All patients in the per protocol analysis reported having taken all of the prescribed study medication. H. pylori eradication The group receiving standard triple therapy (LCT 2) achieved the highest eradication rate of 86.9% in the per protocol analysis, followed by 72.3% for the once-daily treatment (LCT 1) and 39.3% for the once-daily treatment without proton pump inhibitor (PCT 1) (Table 3). The corresponding rates for the intentionto-treat analysis are also shown in Table 3. The unadjusted ORs [95% confidence interval (CI)] for H. pylori eradication (per protocol analysis), compared with the standard treatment, were 0.4 [0.2; 0.9] for treatment group LCT 1 and 0.1 [0.0; 0.2] for PCT 1. The corresponding ORs for the intention-to-treat analysis were 0.5 [0.3; 0.9] and 0.2 [0.1; 0.3], respectively. Age, gender, location of ulcer and history of previous ulcer were not found to be confounders by multiple regression analysis. Ulcer healing Ulcer healing, defined as the complete disappearance of visible ulcer, followed eradication closely in the two groups receiving proton pump inhibitor. In the per protocol analysis, ulcer healing was 83.0% for group LCT 2 and 73.3% for LCT 1 (Table 3). In the PCT 1 group, the ulcer healing rate was 65.2% and thus significantly higher (P < 0.01) than the H. pylori eradication rate (Tables 3 and 4). The intention-to-treat analyses for ulcer healing are also shown in Table 3. The unadjusted ORs [95% CI] for ulcer healing (per protocol), compared with the standard treatment group LCT 2, were 0.6 [0.3; 1.2] for LCT 1 and 0.4 [0.2; 0.8] for PCT 1. The corresponding ORs for the intention-to-treat analysis were 0.6 [0.3; 1.1]

5 EXPERIMENTAL TREATMENT OF H. PYLORI AND PEPTIC ULCER 97 Figure 1. Flow chart of the study. Hp, Helicobacter pylori; ITT, intention-to-treat; PP, per protocol. Table 3. Treatment results Eradication rate Ulcer healing rate Therapy* PP (%) (n/n) [95% CI] ITT (%) (n/n) [95% CI] PP (%) (n/n) [95% CI] ITT (%) (n/n) [95% CI] LCT (73/84) 76.8 (76/99) 83.0 (78/94) 78.8 (78/99) [79.7; 94.1] [68.5; 85.1] [75.4; 90.6] [70.7; 86.9] LCT (60/83) 61.9 (60/97) 73.3 (66/90) 68.0 (66/97) [62.7; 81.9] [52.2; 71.6] [64.2; 82.4] [58.7; 77.3] PCT (35/89) 36.4 (36/99) 65.2 (60/92) 60.6 (60/99) [29.1; 49.4]à [26.9; 45.9]à [55.5; 74.9] [51.0; 70.2] CI, confidence interval; ITT, intention-to-treat; PP, per protocol. * Treatment regimens given in Table 1. LCT 2 vs. LCT 1, P ¼ à LCT 2/LCT 1 vs. PCT 1, P < and 0.4 [0.2; 0.8], respectively. Age, gender, location of ulcer and history of previous ulcer were not found to be confounders by multiple regression analysis. Adverse events Two patients, both belonging to group PCT 1, were the only subjects to withdraw from the study due to adverse events. Both registered a generalized rash, observed after 2 days of medication. The condition resolved after discontinuation of the trial drugs. Another patient (group PCT 1) sought medical attention for a mild skin rash, but decided to continue taking the study drugs and to complete the trial. The most common side-effects reported, i.e. taste alterations (20 50%), burning sensation in the genital tract (13 18%), headache (44 55%) and skin rash (5 9%), showed no significant differences between the groups (P values between 0.18 and 1.00), were mild and did not result in other withdrawals from the study.

6 98 T-U. WHEELDON et al. Table 4. Eradication and ulcer healing in the antibiotics-only group Ulcer healing DISCUSSION Helicobacter pylori eradication Yes Yes 91.4% (32/35) 48.1% (26/54) No 8.6% (3/35) 51.9% (28/54) The present study is, to our knowledge, the first largescale, randomized, placebo-controlled trial to fully investigate the efficacy of a once-daily treatment regimen, with and without a proton pump inhibitor, on H. pylori eradication and peptic ulcer healing. We used endoscopy at follow-up and were therefore able to establish whether the eradication of H. pylori infection resulted in the healing of peptic ulcer, even without the use of proton pump inhibitors. In addition, we were able to show the usefulness of standard triple therapy in a developing country such as Vietnam. Our eradication rate of 86.9% (per protocol) in Vietnam for standard triple therapy is comparable with those obtained in other 16, 17 studies from the industrialized world: 93 95%. Once-daily treatment with a proton pump inhibitor resulted in an eradication rate of 72%, which is significantly lower than that of the standard, twicedaily, dosing regimen. This is consistent with two smaller, open studies using once-daily treatment regimens similar to ours, which reported eradication rates of %. 18, 19 Only one other large, single-blind, randomized trial has compared the efficacy of a oncedaily regimen with the standard twice-daily treatment. 20 In this study, Ström et al. reported eradication rates of 91% and 90% in the respective groups, suggesting that no difference exists between the oncedaily and twice-daily administrations. However, most patients in that study did not have peptic ulcer disease, whereas all of our patients had large ( 5 mm) peptic ulcers, a difference that could influence the eradication rates. Therefore, our study seems to suggest that, in patients with peptic ulcer disease, the twice-daily regimen achieves better H. pylori eradication than the once-daily administration. In the once-daily treatment group without a proton pump inhibitor, an eradication rate of 39.3% was found, significantly lower than those in the groups receiving lansoprazole. Very few studies have made such direct No comparisons of antibiotic treatments with and without proton pump inhibitors, especially in patients with peptic ulcer disease. An open study from the UK with H. pyloriinfected and mainly non-ulcer patients reported eradication rates of 63.8% without a proton pump inhibitor and 88% when omeprazole was added to the antibiotic regimen. 21 The large, double-blind, MACH 2 study with duodenal ulcer patients reported, for the antibiotics-only group (400 mg metronidazole and 250 mg clarithromycin given twice daily for 1 week), an eradication rate of 72%, compared with 91% when omeprazole was added. 11 It appears that the addition of a proton pump inhibitor generally increases the eradication rate in the different patient groups studied. In the present study, we have shown that the eradication of H. pylori by itself can be sufficient for ulcer healing, even without proton pump inhibitor treatment. This observation confirms the central role of H. pylori in the pathophysiology of peptic ulcer disease. This finding was made as all of our patients were followed up by endoscopy, whereas, in the previous study of ulcer patients treated with antibiotics only, the urea breath test was used to assess eradication and peptic ulcer healing was not investigated directly. 11 Unexpectedly, we also found that ulcer healing was possible even without the eradication of H. pylori. Selfmedication with antacids could be a possible but less likely explanation, as the treatment allocation was blind, the study was carefully monitored and the patients were highly motivated to follow the study protocol. It is more likely that antibiotic treatment resulted in a major reduction, if not eradication, of H. pylori in the gastric mucosa. As shown by El-Omar et al., H. pylori infection results in an increase in both the basal and meal-stimulated level of acid secretion, suggesting that this is the causative link between H. pylori infection and duodenal ulcer. 22 In consequence, we speculate that a greatly reduced bacterial load could lead to a normalization of acid secretion and hence to ulcer healing, even without eradication. In the developing world, there have been few large treatment trials, and all have used a variety of different designs and treatment regimens different from the standard therapy recommended in the industrialized world. A majority of the larger studies have used higher antibiotic dosages than ours, leading to higher treatment costs for the patients. In spite of the different designs, most studies have reported eradication rates around 90%, 23, 24 with the exception of an open, non-

7 EXPERIMENTAL TREATMENT OF H. PYLORI AND PEPTIC ULCER 99 controlled study from Brazil, which used the same regimen as ours and reported an eradication rate of only 65%. 25 A recent, non-blind trial from Vietnam found an eradication rate of 91% with a regimen of amoxicillin, clarithromycin and omeprazole for 10 days. 26 This study used 500 mg of clarithromycin and a high dose of amoxicillin. Our study has shown that high eradication rates can be achieved in a developing country, even with lower dosages and a shorter treatment time, thus making treatment more affordable and simpler. The side-effects showed no significant differences between the treatment groups, and the treatment regimens were generally well tolerated. Theoretically, the once-daily dosage could entail higher rates of sideeffects than the split dosage of twice-daily administration. As tinidazole, in particular, is associated with increased side-effects at high doses, we believe the good tolerability in our study and in that by Ström et al. 20 could be due to the administration of the medication as an evening dose, thus avoiding the discomfort the same medication would have caused if administered in the morning. The strength of our study lies in the balanced and unpredictable central randomization. The size of the study groups permitted the detection of even small differences in treatment efficacy. The caveats include the fact that the standard treatment consisted of twicedaily administration of the drugs, whereas the experimental regimens were taken once daily; this rendered the blinding process incomplete. In addition, the patients lost to follow-up represent a limitation, but are acceptable for a treatment trial conducted in a developing country. In conclusion, our study has shown that the twice-daily administration of the drugs and the addition of a proton pump inhibitor for the eradication of H. pylori in peptic ulcer patients significantly increase the success rate and represent a valid treatment option in a developing country such as Vietnam. We also found that peptic ulcer healing could be achieved with antibiotics-only treatment, confirming the central role of H. pylori in the pathophysiology of peptic ulcer disease. ACKNOWLEDGEMENTS The study received support from the Swedish International Development Agency SIDA/SAREC and the Swedish Association for Tropical Medicine. Wyeth, Abbott and Pfizer provided study medication and placebos. Dr Scott M. Montgomery (Clinical Epidemiology Clinic, Karolinska Hospital, Karolinska Institute, Stockholm, Sweden) provided epidemiological advice on the analysis and preparation of the manuscript. We also wish to thank the doctors and staff at the Department of Gastroenterology and Endoscopy at the Bach Mai Hospital and the National Institute of Hygiene and Epidemiology in Hanoi, Vietnam, and Eivor Norström and Carina Bengtsson at the Department of Clinical Microbiology, Karolinska Hospital, Stockholm, Sweden, for their assistance and dedication. REFERENCES 1 Dixon M, Sobala G. Gastritis and duodenitis: the histopathological spectrum. Eur J Gastroenterol Hepatol 1992; 4: S Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001; 345: Hentschel E, Brandstatter G, Dragosics B, et al. Effect of ranitidine and amoxicillin plus metronidazole on the eradication of Helicobacter pylori and the recurrence of duodenal ulcer. N Engl J Med 1993; 328: Sung JJ, Chung SC, Ling TK, et al. Antibacterial treatment of gastric ulcers associated with Helicobacter pylori. N Engl J Med 1995; 332: NIH Consensus Conference. Helicobacter pylori in peptic ulcer disease. NIH Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease. J Am Med Assoc 1994; 272: Labenz J, Idstrom JP, Tillenburg B, Peitz U, Adamek RJ, Borsch G. One-week low-dose triple therapy for Helicobacter pylori is sufficient for relief from symptoms and healing of duodenal ulcers. Aliment Pharmacol Ther 1997; 11: Bell GD, Powell KU, Burridge SM, et al. Rapid eradication of Helicobacter pylori infection. Aliment Pharmacol Ther 1995; 9: Bazzoli F, Zagari R, Fossi S, et al. Short-term low-dose triple therapy for the eradication of Helicobacter pylori. Eur J Gastroenterol Hepatol 1994; 6: Laine L, Estrada R, Trujillo M, Emami S. Randomized comparison of ranitidine bismuth citrate-based triple therapies for Helicobacter pylori. Am J Gastroenterol 1997; 92: Sorberg M, Hanberger H, Nilsson M, Bjorkman A, Nilsson LE. Risk of development of in vitro resistance to amoxicillin, clarithromycin, and metronidazole in Helicobacter pylori. Antimicrob Agents Chemother 1998; 42: Lind T, Megraud F, Unge P, et al. The MACH2 study: role of omeprazole in eradication of Helicobacter pylori with 1-week triple therapies. Gastroenterology 1999; 116: Megraud F, Brassens-Rabbe MP, Denis F, Belbouri A, Hoa DQ. Seroepidemiology of Campylobacter pylori infection in various populations. J Clin Microbiol 1989; 27: Tran V, Ta L, Bui L, Ha M. H. pylori and gastritis and peptic ulcers (a histology study). Vietnam Military Med 1993; 7: 23 4.

8 100 T-U. WHEELDON et al. 14 Katelaris PH, Lowe DG, Norbu P, Farthing MJ. Field evaluation of a rapid, simple and inexpensive urease test for the detection of Helicobacter pylori. J Gastroenterol Hepatol 1992; 7: Monteiro L, de Mascarel A, Sarrasqueta AM, et al. Diagnosis of Helicobacter pylori infection: noninvasive methods compared to invasive methods and evaluation of two new tests. Am J Gastroenterol 2001; 96: Labenz J, Stolte M, Ruhl GH, et al. One-week low-dose triple therapy for the eradication of Helicobacter pylori infection. Eur J Gastroenterol Hepatol 1995; 7: Jaup BH, Norrby A. Low dose, short-term triple therapy for cure of Helicobacter pylori infection and healing of peptic ulcers. Am J Gastroenterol 1995; 90: Laine L, Estrada R, Trujillo M, et al. Once-daily therapy for H. pylori infection: a randomized comparison of four regimens. Am J Gastroenterol 1999; 94: Chu KM, Kwok KF, Law SY, Wong J. One-week oncedaily triple therapy for Helicobacter pylori a pilot study. Hepatogastroenterology 2000; 47: Ström M, Befrits R, Kindvall-Nilsson B, Ohlsson A, Svensson M, Sörberg M. Helicobacter pylori eradication rate: once daily pantoprazole + clarithromycin and tinidazole is adequate. Scand J Gastroenterol Suppl 2001; 233: Moayyedi P, Sahay P, Tompkins DS, Axon AT. Efficacy and optimum dose of omeprazole in a new 1-week triple therapy regimen to eradicate Helicobacter pylori. Eur J Gastroenterol Hepatol 1995; 7: El-Omar EM, Penman ID, Ardill JE, Chittajallu RS, Howie C, McColl KE. Helicobacter pylori infection and abnormalities of acid secretion in patients with duodenal ulcer disease. Gastroenterology 1995; 109: Choi IJ, Jung HC, Choi KW, et al. Efficacy of low-dose clarithromycin triple therapy and tinidazole-containing triple therapy for Helicobacter pylori eradication. Aliment Pharmacol Ther 2002; 16: Fock KM, Chelvam P, Lim SG. Triple therapy in the eradication of Helicobacter pylori in patients with duodenal ulcer disease: results of a multicentre study in South-East Asia. South-East Asia Multicenter Study Group. Aliment Pharmacol Ther 2000; 14: Silva FM, Zaterka S, Eisig JN, Chehter EZ, Chinzon D, Laudanna AA. Factors affecting Helicobacter pylori eradication using a seven-day triple therapy with a proton pump inhibitor, tinidazole and clarithromycin, in Brazilian patients with peptic ulcer. Rev Hosp Clin Fac Med Sao Paulo 2001; 56: Mao HV, Lak BV, Long T, et al. Omeprazole or ranitidine bismuth citrate triple therapy to treat Helicobacter pylori infection: a randomized, controlled trial in Vietnamese patients with duodenal ulcer. Aliment Pharmacol Ther 2000; 14:

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