Omeprazole delays gastric emptying in healthy volunteers: an effect prevented by tegaserod
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1 Aliment Pharmacol Ther 2005; 22: doi: /j x Omeprazole delays gastric emptying in healthy volunteers: an effect prevented by tegaserod G. TOUGAS*,,D.L.EARNESTà, Y. CHEN*, C. VANDERKOY* & M. ROJAVINà *McMaster University, Hamilton, ON, Canada; Novartis Pharma AG, Basel, Switzerland; ànovartis Pharmaceuticals, East Hanover, NJ, USA Accepted for publication 28 April 2005 SUMMARY Background: Proton-pump inhibitors effectively suppress stomach acidity. They are widely used for treating gastro-oesophageal reflux disease and related conditions. While generally safe, omeprazole and other proton-pump inhibitors can delay gastric emptying. Aim: To test the hypothesis that tegaserod can normalize or prevent omeprazole-induced delay in gastric emptying. Methods: This was a randomized, double-blind, placebocontrolled, parallel group study in 40 healthy male volunteers. After informed consent and screening, qualified volunteers were treated with unblinded omeprazole 20 mg b.d. and either blinded tegaserod 6 mg t.d.s. (active treatment group) or placebo-matching tegaserod t.d.s. (control group) for 14 days. Gastric emptying was assessed before and after treatment, using a scintigraphy method. Results: Omeprazole monotherapy significantly delayed gastric emptying expressed by duration of lag-phase (P < 0.007), time to gastric half-emptying (P < 0.003), and gastric retention of the meal at 60 (P < 0.002) and 120 min (P < 0.04) after its ingestion. Tegaserod taken together with omeprazole effectively prevented development of the above effects. Combined treatment was safe and well tolerated. Conclusion: Concomitant administration of tegaserod 6 mg t.d.s. prevented development of the delayed gastric emptying induced by omeprazole monotherapy. INTRODUCTION Proton-pump inhibitors (PPIs) are the most effective pharmacological agents for the treatment of patients with gastro-oesophageal reflux diseases (GERD). 1 While considered generally safe, omeprazole in daily doses of mg has been shown to significantly delay gastric emptying. 2 5 The magnitude of the delay in gastric emptying produced by omeprazole ranges from 15% to as much as 40%. 2, 3 Delayed gastric emptying has been associated with adverse effects including development of dyspeptic symptoms 6 8 and proximal gastrointestinal Correspondence to: Dr M. Rojavin, Novartis Pharmaceuticals, Gastroenterology, One Health Plaza, East Hanover, NJ 07936, USA. mikhail.rojavin@novartis.com (GI) tract bacterial overgrowth. 9, 10 A variable but substantial proportion of patients with symptomatic GERD who are candidates for treatment with a PPI already have delayed gastric emptying. 7, 11 Exacerbation of this abnormality may possibly contribute to causing or worsening GER and increase the prevalence of dyspeptic symptoms commonly reported by this patient group. 7, Drugs, which improve gastric emptying, can improve GERD symptoms, mucosal healing, and increase the efficacy of the antisecretory 15, 16 medications in chronic GERD management. Tegaserod is a peripherally acting partial 5HT 4 -receptor agonist, which is approved for the treatment of women with irritable bowel syndrome with constipation (IBS-C) and for the treatment of men and women with chronic constipation. It accelerates gastric emptying in Ó 2005 Blackwell Publishing Ltd 59
2 60 G. TOUGAS et al. healthy volunteers and in dyspeptic subjects with gastroparesis. 17, 18 We have conducted a randomized, double-blind, placebo-controlled, parallel group study in healthy male volunteers to test the hypothesis that tegaserod can normalize or prevent any delay in gastric emptying induced by omeprazole. RESEARCH SUBJECTS AND METHODS Study population Forty healthy male volunteers were studied. They were between 18 and 40 years of age and had a body mass index between 20 and 25. The protocol and informed consent were approved by the Independent Review Board of McMaster University, Hamilton, Ontario, Canada. Subjects older than 40 years were excluded to avoid age-related changes in gastric emptying and to make the population more homogenous. Women were excluded to avoid gastric emptying rate variations associated with the menstrual cycle and other genderrelated differences. 19, 20 All volunteers gave informed consent prior to beginning the study and had to be able to communicate adequately with the investigator as well as comply with the requirements of the study. Major exclusion criteria were: use of disallowed medication(s) during the study (drugs which could potentially mask the effect of study medication, laxatives and any PPI other than omeprazole 20 mg twice daily); clinical evidence or history of significant cardiovascular, respiratory, renal, hepatic, GI, haematological, neurological disorders or of any disease or prior surgery that might interfere with the subject successfully completing the study; known sensitivity to study drug(s) or the class of study drug(s); known drug or alcohol abuse or tobacco smoking; evidence or recent history of diarrhoea defined as 2 or more day with loose or watery stools during 2 weeks prior to visit 1. Medication The subjects were given omeprazole 20 mg twice daily (b.d.) in combination with either tegaserod 6 mg three times a day (t.d.s.) or placebo t.d.s. for 14 days. Each medication was taken with a glass of water 30 min prior to meals (morning and evening for omeprazole and three times a day, with meals, for tegaserod). Blinded tegaserod 6 mg and matching placebo tablets were supplied by Novartis Pharmaceuticals. Open label omeprazole 20 mg capsules were obtained from local commercial sources. Visit schedule and assessments Figure 1 shows flow diagram of the study. During the first visit, after the volunteers had provided informed consent, medical personnel assessed inclusion and exclusion criteria, collected background medical information and recorded prior medications. Prohibited medications, if any, were discontinued. Physical examination was performed and weight and vital signs were measured. Blood and urine specimens were collected for routine laboratory analyses. Once the volunteers were determined to meet all inclusion/exclusion criteria and had normal laboratory tests results, qualifying subjects underwent the first gastric emptying study. They were then randomized into a 14-day double-blind treatment period, receiving omeprazole plus either placebo or tegaserod. After 14 days of drug treatment, all subjects returned for a second gastric emptying study. This visit also included assessment of treatment compliance by medication counting and of any reported adverse events. Physical examination and laboratory tests were repeated. Quantification of gastric emptying by scintigraphy Gastric emptying was assessed before and after the double-blind treatment period by a standardized scintigraphy method that has been previously validated. 21, 22 After an overnight fast, the subjects ingested a [99Tcm]-radiolabelled meal (250 ml EggBeater, the equivalent of two eggs, two slices of white bread, 30 cm 3 of strawberry jam and 120 ml of water). The Randomization Screening and baseline evaluations Omeprazole + placebo Omeprazole + tegaserod 2-4 weeks 2 weeks Figure 1. Study flow diagram. Scintigraphy Scintigraphy
3 OMEPRAZOLE AND TEGASEROD IN GASTRIC EMPTYING 61 content of the radioactive materials in the stomach was then measured by external scintigraphy immediately following completion of the meal and then at 60, 120 and 240 min after the end of the meal. The method has been extensively used previously and found to be well tolerated by patients and volunteers alike. 22 Gastric emptying was calculated as follows: the region of interest was drawn around the scintigraphic image of the stomach for each time frame and the geometric mean was calculated as the square root of the product of the counts measured on the anterior and posterior images. The main parameters measured were percentage gastric retention at 60, 120 and 240 min. Gastric retention curves were generated using a power exponential model defined as prop t ¼ )(j t) b, where prop t is the proportion of meal retention at time t. All data are expressed as a percentage of the isotope remaining in the stomach. The lag-phase was defined as the period before emptying of 5% of the gastric content measured at time 0 (immediately after the end of the meal). T 1/2 was defined as the time to emptying of 50% of the gastric content initially measured at time 0. Efficacy assessments Gastric emptying was assessed using the following endpoints: 1 time to half-emptying of gastric contents (T 1/2 ); 2 calculated lag-phase and 3 percentage of residual gastric contents at 60, 120 and 240 min after ingestion of a standard meal. These values were calculated from the scintigraphic gastric emptying data described above. Safety assessments Safety assessments included regular monitoring for and recording of all adverse events (with their severity and relationship to study drug), monitoring of results of haematology, blood chemistry and urine testing and assessment of vital signs, physical condition and body weight. Statistical analyses The primary objective of this trial was to test the following hypothesis. Null hypothesis. There is no difference in time to 50% emptying (T 1/2 ) between omeprazole 20 mg b.d. and omeprazole 20 mg b.d. + tegaserod 6 mg t.d.s. Alternative hypothesis. There is a difference in time to 50% emptying (T 1/2 ) between omeprazole 20 mg b.d. and omeprazole 20 mg b.d. + tegaserod 6 mg t.d.s. The primary efficacy parameter was T 1/2 at study endpoint. T 1/2 was estimated by a mixed-effect power exponential model. To control for type I error, a ¼ 0.05 was used. The primary analysis was performed on the per-protocol population. Treatment by baseline interaction was examined. Secondary efficacy end-points were the percentage of initial gastric contents remaining in the stomach at 60, 120 and 240 min. Comparisons of lag-phase duration between posttreatment and baseline were done using paired t-test (for omeprazole-treated group) and Wilcoxon signed rank test (for combined treatment group because of the fact that the data distribution in this group were not normal). RESULTS Sixty-two subjects were screened for the study. Forty of them met study entry criteria and were randomized into the study. All of these subjects completed the study. Grouping for analysis was by treatment only. There were 20 men in the omeprazole + placebo group, and 20 men in the omeprazole + tegaserod group. One subject allocated to the omeprazole + placebo treatment group was subsequently excluded from the analysis after it was discovered that he had severe asymptomatic gastroparesis at the baseline gastric emptying assessment. As a result, the number of patients in omeprazole monotherapy group was reduced to 19. Age, body weight and racial distribution of volunteers in both groups were well matched (Table 1). Gastric emptying results Results of comparisons of gastric emptying between post-treatment vs. baseline values for all the end-points T 1/2 and gastric retention at 60 and 120 min after ingestion of test meal are presented in Table 2. Additionally, more detailed representation of changes for each subject by treatment group and end-points can be found in Figures 2 4. Omeprazole treatment (20 mg b.d. for 14 consecutive days) significantly delayed
4 62 G. TOUGAS et al. Table 1. Demographic and background characteristics by treatment group (a) Omeprazole + tegaserod (n ¼ 20) Omeprazole + placebo (n ¼ 19) Sex, n (%) Male 20 (100) 19 (100) Race, n (%) Caucasian 15 (75) 17 (90) African-American 1 (5) 0 (0) Asian/Oriental 4 (20) 1 (5) Other 0 (0) 1 (5) Mean age (years) s.d Range Mean weight (kg) s.d Range Table 2. Changes in gastric emptying parameters by treatment group (b) Gastric emptying parameter Treatment Change from baseline (mean ± S.E.) P-value (paired t-test) T 1/2 Gastric retention (60 min) Gastric retention (120 min) Omeprazole (11.6 ± 5.8) min < tegaserod Omeprazole (16.9 ± 4.8) min <0.003 Omeprazole (3.4 ± 4.5)% <0.5 + tegaserod Omeprazole (10.7 ± 2.9)% <0.002 Omeprazole (6.3 ± 3.9)% <0.2 + tegaserod Omeprazole (9.3 ± 4.0)% <0.04 gastric emptying in healthy volunteers increasing the T 1/2 by 16.9 ± 4.8 min (from 75.1 ± 6.3 to 92.0 ± 5.7 min, P < by paired t-test; Figure 2a). The concomitant use of tegaserod during omeprazole treatment, largely prevented the delayed gastric emptying caused by omeprazole. In the group receiving tegaserod and omeprazole, the measured T 1/2 was statistically no different from the baseline T 1/2 measured in the same group prior to drug administration (Figure 2b). When examined sequentially over time, omeprazole increased gastric retention (i.e. delayed gastric emptying) by 10.7 ± 2.9% (P < 0.002) at 60 min (Figure 3a) following completion of the test meal and by 9.3 ± 4.0% (P < 0.04) at 120 min (Figure 4a) when compared with baseline. In contrast, for the group Figure 2. (a) Effect of omeprazole 20 mg b.d. for 14 days on time to gastric half-emptying (T 1/2 ). Connected pairs of points represent individual values of T 1/2 for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). (b) Effect of combined tegaserod 6 mg t.d.s. + omeprazole 20 mg b.d. therapy for 14 days on T 1/2. Connected pairs of points represent individual values of T 1/2 for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). receiving tegaserod + omeprazole, gastric retention of the test meal was not statistically different at 60 (Figure 3b) and 120 min (Figure 4b) from that observed at baseline in the same group of subjects (3.4 ± 4.5% at 60 min, P < 0.5 vs. baseline and 6.3 ± 3.9% at 120 min, P < 0.2 vs. baseline). Retention of food at 240 min after the test meal in both
5 OMEPRAZOLE AND TEGASEROD IN GASTRIC EMPTYING 63 (a) (a) (b) (b) Figure 3. (a) Effect of omeprazole 20 mg b.d. for 14 days on percentage of gastric retention at 60 min after test meal. Connected pairs of points represent individual values for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). (b) Effect of combined treatment with tegaserod 6 mg t.d.s. + omeprazole 20 mg b.d. for 14 days on percentage of gastric retention at 60 min after test meal. Connected pairs of points represent individual values for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). groups showed no significant differences between the treatments applied, but the amount retained was very small (approximately 1%). Analysis of the calculated lag-phase yielded similarly consistent results. There was a significant prolongation Figure 4. (a) Effect of omeprazole 20 mg b.d. for 14 days on percentage of gastric retention at 120 min after test meal. Connected pairs of points represent individual values for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). (b) Effect of combined treatment with tegaserod 6 mg t.d.s. and omeprazole 20 mg b.d. for 14 days on percentage of gastric retention at 120 min after test meal. Connected pairs of points represent individual values for each research subject before and after treatment. Vertical bars on each side of the graph are average group values (mean ± S.E.M.). in lag-phase (mean increase of 7.9 ± 2.5 min over baseline lag-phase values, P < 0.007) in subjects receiving omeprazole alone. In subjects who received omeprazole + tegaserod, there was virtually no prolongation in the lag-phase of gastric emptying (mean
6 64 G. TOUGAS et al. increase of 4.5 ± 3.0 min compared with baseline lagphase values, P < 0.2). Adverse events Neither group of volunteers reported any severe sideeffects or clinically significant adverse events after randomization and during drug treatment. All adverse events were mild and of short duration. None required a modification of a drug dose or withdrawal from the study. One subject initially included in the omeprazole + placebo group had to be excluded from the study after the result of his baseline gastric emptying evaluation was found to be markedly prolonged outside the normal range and compatible with gastroparesis. All registered adverse events were each reported by only a single participant. They included one patient with diarrhoea in the omeprazole + tegaserod group, and a single case of anorexia in the omeprazole-treated group. Other adverse events reported from subject questioning were all mild and self-limited. In the combined tegaserod + omeprazole treatment group, these included abdominal bloating (one occurrence), chest pain and heartburn (one occurrence), flu-like symptoms (one occurrence), joint pain (one occurrence) and vomiting (one occurrence). DISCUSSION In this study in healthy male volunteers, omeprazole treatment was associated with significant delays in gastric emptying as evidenced by the 22.7% prolongation in T 1/2 compared with baseline. In absolute terms this translates in an increase of nearly 17 min in the time required for half-emptying of the stomach following ingestion of the test meal. This observation is consistent with the 15 40% delay in T 1/2 for gastric emptying during omeprazole treatment reported by others. 2 4 Accordingly, we confirm in healthy volunteers this rarely discussed consequence of omeprazole treatment. In these normal subjects, the extent of the induced delay in gastric emptying was not accompanied by development of dyspeptic symptoms recorded as adverse events. The delaying effect of omeprazole on gastric emptying appears to be manifested at both the onset of gastric emptying, as evidenced by prolongation of the lagphase, and during the active or linear emptying phase as shown by the slope of the gastric emptying curve. Significant differences were observed in the percentage of the meal retained at 60 and 120 min, and consequently there was significant prolongation of the halfemptying time for the meal during omeprazole use compared with pre-treatment baseline values. The novel observation in this study is that the use of the gastric prokinetic drug tegaserod, when taken with omeprazole, effectively prevented the delay in gastric emptying observed during treatment with omeprazole only. In this study, omeprazole was administered in a dose clinically used for treatment of erosive oesophagitis, while tegaserod was dosed at 6 mg orally t.d.s. The dose of tegaserod is higher than that currently recommended (6 mg b.d.) for treatment of either chronic constipation or of IBS-C symptoms in women. However, it was chosen for evaluation in this study as we have previously shown that the 6 mg t.d.s. of tegaserod is more effective than the standard dose in correcting delayed gastric emptying associated with dyspeptic symptoms in patients with functional dyspepsia. 18 Whether different doses or dosing regimens of tegaserod would be effective in preventing the omeprazole-induced delay in gastric emptying observed in this study is unknown. In a clinical setting, heartburn in GERD patients is often accompanied by dyspeptic symptoms such as early satiety, postprandial fullness, nausea, or bloating. Because many GERD patients have delayed gastric emptying, 7, 11 such dyspeptic symptoms have occasionally been attributed to this abnormality. 7, 8, 23 This relationship, however, remains conjectural as the cause for dyspeptic symptoms occurring with GERD has not been defined. A number of studies have also implicated delayed gastric emptying as a possible contributing factor which promotes acidic GER. 12, 24 While PPIs such as omeprazole significantly decrease both gastric acid secretion and acid reflux, neither is completely inhibited by the PPI therapy and any delay in gastric emptying could still be a negative factor. In view of the very common use of PPIs to treat GERD symptoms, our results may also have important therapeutic implications for this patient group. For example, in those GERD patients who are treated with a PPI, such as omeprazole, and who develop new or worsening dyspeptic symptoms during PPI treatment, even if heartburn relief is achieved, one might consider that delayed gastric emptying related to PPI treatment may possibly contribute to the onset of dyspepsia. The results of our study show that treatment with tegaserod can normalize delayed gastric emptying caused by omeprazole use. However, a positive effect
7 OMEPRAZOLE AND TEGASEROD IN GASTRIC EMPTYING 65 on dyspeptic symptoms cannot be assumed from results of this small trial as only normal male volunteers without GERD or dyspepsia were research subjects in this study. The normalization of gastric emptying by tegaserod suggests that formal evaluation for a change in dyspeptic symptoms in GERD patients taking PPI therapy should be considered. CONCLUSIONS In healthy male volunteers, treatment with omeprazole 20 mg b.d. for 14 days caused a statistically significant delay in gastric emptying. Concomitant administration of tegaserod 6 mg t.d.s. prevented development of the delayed gastric emptying induced by omeprazole monotherapy. No significant adverse effects were observed during omeprazole or omeprazole + tegaserod treatment. ACKNOWLEDGEMENT This study was funded by a grant from Novartis Pharmaceuticals. REFERENCES 1 Berardi RR. Proton pump inhibition. An effective, safe approach to GERD management. Postgrad Med 2001; Oct; Spec No: Benini L, Castellani G, Bardelli E, et al. Omeprazole causes delay in gastric emptying of digestible meals. Dig Dis Sci 1996; 41: Parkman HP, Urbain JL, Knight LC, et al. Effect of gastric acid suppressants on human gastric motility. Gut 1998; 42: Rasmussen L, Qvist N, Oster-Jorgensen E, Rehfeld JF, Holst JJ, Pedersen SA. A double-blind placebo-controlled study on the effects of omeprazole on gut hormone secretion and gastric emptying rate. Scand J Gastroenterol 1997; 32: Rasmussen L, Oster-Jorgensen E, Qvist N, Pedersen SA. The effects of omeprazole on intragastric ph, intestinal motility, and gastric emptying rate. Scand J Gastroenterol 1999; 34: DeVault KR. Omeprazole may delay gastric emptying? Am J Gastroenterol 1996; 91: Buckles DC, Sarosiek I, McMillin C, McCallum RW. Delayed gastric emptying in gastro-oesophageal reflux disease: reassessment with new methods and symptomatic correlations. Am J Med Sci 2004; 327: Haag S, Talley NJ, Holtmann G. Symptom patterns in functional dyspepsia and irritable bowel syndrome: relationship to disturbances in gastric emptying and response to a nutrient challenge in consulters and non-consulters. Gut 2004; 53: Lewis SJ, Franco S, Young G, O Keefe SJ. Altered bowel function and duodenal bacterial overgrowth in patients treated with omeprazole. Aliment Pharmacol Ther 1996; 10: Guarner F, Malagelada JR. Gut flora in health and disease. Lancet 2003; 361: Soykan I, Lin Z, Jones S, Chen J, McCallum RW. Gastric myoelectrical activity, gastric emptying and correlations with dyspepsia symptoms in patients with gastro-oesophageal reflux. J Investig Med 1997; 45: Herculano JR Jr, Troncon LE, Aprile LR, et al. Diminished retention of food in the proximal stomach correlates with increased acidic reflux in patients with gastro-oesophageal reflux disease and dyspeptic symptoms. Dig Dis Sci 2004; 49: Metz DC. Managing gastro-oesophageal reflux disease for the lifetime of the patient: evaluating the long-term options. Am J Med 2004; 117 (Suppl. 5A): 49S 55S. 14 Tack J, Koek G, Demedts I, Sifrim D, Janssens J. Gastrooesophageal reflux disease poorly responsive to single-dose proton pump inhibitors in patients without Barrett s oesophagus: acid reflux, bile reflux, or both? Am J Gastroenterol 2004; 99: Vigneri S, Termini R, Leandro G, et al. A comparison of five maintenance therapies for reflux esophagitis. N Engl J Med 1995; 333: Chiba N, De Gara CJ, Wilkinson JM, Hunt RH. Speed of healing and symptom relief in grade II to IV gastro-oesophageal reflux disease: a meta-analysis. Gastroenterology 1997; 112: Camilleri M. Tegaserod. Aliment Pharmacol Ther 2001; 15: Tougas G, Chen Y, Luo D, Salter J, d Elia T, Earnest DL. Tegaserod improves gastric emptying in patients with gastroparesis and dyspeptic symptoms. Gastroenterology 2003; 124 (Suppl. 1): A Gryback P, Hermansson G, Lyrenas E, Beckman KW, Jacobsson H, Hellstrom PM. Nationwide standardisation and evaluation of scintigraphic gastric emptying: reference values and comparisons between subgroups in a multicentre trial. Eur J Nucl Med 2000; 27: Bennink R, Peeters M, Van den Maegdenbergh V, et al. Comparison of total and compartmental gastric emptying and antral motility between healthy men and women. Eur J Nucl Med 1998; 25: Tougas G, Chen Y, Coates G, et al. Standardization of a simplified scintigraphic methodology for the assessment of gastric emptying in a multicenter setting. Am J Gastroenterol 2000; 95: Tougas G, Eaker EY, Abell TL, et al. Assessment of gastric emptying using a low fat meal: establishment of international control values. Am J Gastroenterol 2000; 95: Richter J. Do we know the cause of reflux disease? Eur J Gastroenterol Hepatol 1999; 11 (Suppl. 1): S Holtmann G, Adam B, Liebregts T. Review article: The patient with gastro-oesophageal reflux disease lifestyle advice and medication. Aliment Pharmacol Ther 2004; 20 (Suppl. 8): 24 7.
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