Ambulatory gastric ph monitoring: proper probe placement and normal values
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1 Aliment Pharmacol Ther 2001; 15: 1155±1162. Ambulatory gastric ph monitoring: proper probe placement and normal values W. K. FACKLER, M. F. VAEZI & J. E. RICHTER Center for Swallowing and Oesophageal Disorders, Cleveland Clinic Foundation, Cleveland, USA Accepted for publication 31 January 2001 SUMMARY Background: Gastric acid production may persist while patients are treated with proton pump inhibitors. Twenty-four-hour intragastric ph monitoring is being used to identify gastric acid in the stomach while on medical therapy. Aim: To identify the optimal region of the stomach to demonstrate the presence of gastric acid. Method: Probe locations con rmed with uoroscopy after placement and prior to removal. In experiment 1, ve volunteers underwent simultaneous, 24-h gastro-oesophageal ph monitoring with the ph sensors located in the gastric antrum, body, fundus and distal oesophagus. In experiment 2, ve volunteers underwent simultaneous 24-h ph monitoring with sensors located side by side in the gastric fundus assessing the reproducibility of gastric ph in this region. In experiment 3, 35 volunteers underwent 24-h ph monitoring with ph sensors located in the distal oesophagus and gastric fundus. The mean percentage time for which ph < 4 was calculated for total, upright, and supine time periods. Results: ph pro les for the gastric fundus and body are similarðthe mean percentage total time for which ph < 4 was 92.2% and 90.1%, respectively (P ˆ N.S.). These values are signi cantly different from the antrum; ph<4ˆ 54.6% (P < 0.01). ph values from the gastric fundus are highly reproducible (linear regression P ˆ 0.004, r 2 ˆ 0.96). The normal values (mean 95th percentile) for percentage time gastric ph < 4 in the fundus were: total %, upright %, and supine %. Conclusion: The fundus is the optimal location to evaluate the presence of gastric acid; ph values are highly reproducible in this area. Normal values for percentage time gastric ph < 4 for a healthy population are now de ned. INTRODUCTION The current gold standard for the diagnosis of gastrooesophageal re ux disease (GERD) is oesophageal ph monitoring. The technique of monitoring oesophageal acid has been standardized through numerous experiments describing appropriate ph cut-offs, proper positioning of oesophageal probes, and normal oesophageal acid exposure values in healthy volunteers. 1 Recently, Correspondence to: Dr J. E. Richter, Department of Gastroenterology, S-40, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195, USA. 1 richtej@cesmtp.ccf.org the practice of ambulatory gastric ph monitoring has gained popularity as an adjunctive diagnostic approach for patients with dif cult to manage GERD. 2 By placing a ph probe into the stomach, investigators are able to identify persistent gastric acid production when patients are being treated with potent acid suppressive medications such as proton pump inhibitors. 3 Additionally, gastric ph monitoring may have some utility in clarify- whether apparent otolaryngologic (ENT) manifesta- 2ing tions of GERD seen at laryngoscopy are actually related to acid re ux or are due to other etiologies, especially with the suboptimal performance of ph probes in the pharynx or proximal oesophagus. 4, 5 Currently, the most popular method of monitoring intragastric ph is Ó 2001 Blackwell Science Ltd 1155
2 1156 W. K. FACKLER et al. performed with a standard, dual ph electrode apparatus. The proximal sensor is placed above the manometrically de ned lower oesophageal sphincter and the distal sensor is located below the lower oesophageal sphincter in a section of the stomach, typically the cardia or fundus. Measurements are conducted over a 24-h period either with or without standardized meals. 6 While this approach seems simple, some question its validity. Early studies concluded that the stomach is best modelled as discrete compartments because the cardia, fundus, corpus and antrum demonstrate different ph pro les. 7±9 Some reports identi ed the antrum or body as the proper place to locate a ph probe to measure the ph of gastric contents; yet other authors determined 5 cm below the lower oesophageal sphincter to be the optimal site for gastric ph measurement. 9±11 Recently, Katzka et al. described the cardia, de ned as 5 cm below the proximal border of the lower oesophageal sphincter, as a region in the stomach with a distinct ph pro le, separate from the distal oesophagus with less acid exposure than the gastric body. 12 To characterize the re uxate entering the oesophagus, however, they suggested this as the prime location to place an acid sensitive probe. Finally, Fisher et al. replicated older experiments, nding that all regions of the stomach do not re ect the same acid exposure, and questioned the ability of a single ph electrode in the cardia to accurately assess overall gastric acidity. 13 Because of these different observations, no consensus exists on the single best place to locate a ph probe to re ect the acidic nature of the entire stomach. From previous studies, we know that different gastric anatomical zones have individual acid characteristics. Therefore, the purposes of this study are: (i) to identify the gastric region which best represents the presence of acid in the stomach; (ii) test the reproducibility of ph measurements in this region; and (iii) develop a range for percentage time gastric ph < 4 in healthy volunteers represented by means with 95% con dence intervals. MATERIALS AND METHODS We prospectively evaluated 35 healthy subjects. Subjects were recruited to the Center for Swallowing and Oesophageal Disorders through an advertisement campaign. All volunteers answered a questionnaire to determine medical histories and demographics. No subjects carried a diagnosis of GERD, nor did they have symptoms suggestive of gastro-oesophageal re ux. Subjects were excluded from the trial if they had a history of peptic ulcer disease, were currently taking acid suppression medications or drugs affecting gastric motility, or were unable to tolerate a ph probe study. Women of child bearing potential were excluded from the study unless they were using contraceptive techniques or had undergone a surgical procedure to prevent pregnancy. Our study protocol was approved by the Institutional Review Board at the Cleveland Clinic Foundation in November All patients consented to the protocol procedures prior to their enrolment into the study. Oesophageal testing Oesophageal manometry. All subjects underwent oesophageal manometry after an overnight fast to locate the lower oesophageal sphincter. We used a round polyvinyl catheter (diameter 4 mm; Arndorfer Medical Specialties Inc., Milwaukee, WI) continuously perfused with distilled water at a rate of 0.5 ml/min by a low compliance pneumohydraulic capillary infusion system. The station pull-through technique was used to determine the location and length of the sphincter. The lower oesophageal sphincter pressures and locations were recorded by means of a computerized motility system (Synectics Gastrosoft Polygram, Milwaukee, WI). Ambulatory gastro-oesophageal ph monitoring. Immediately after manometry, 24-h ph monitoring was performed in all subjects. This was done using 2.1- mm monocrystalline ph catheters with two antimony electrodes separated by either 10 or 15 cm (Medtronic Functional Diagnostics Zinetics, Inc., Salt Lake City, UT). The reference electrode was internalized. The ph electrodes were calibrated at 37 C in ph 7 and ph 1 buffer solutions (Fisher Scienti c, Fairlawn, NJ) before each study was completed. After calibration, the ph probe apparatus was passed nasally and positioned according to the experimental arm to which the individual patient was assigned (see below). The probe apparatus was secured to the nose and cheek to prevent dislodgement. The ph electrodes were connected to a portable digital data recorder (Digitrapper Mark III Gold, Synectics) worn around the waist, which stored ph data samples every 4 s for up to 24 h. Subjects returned home with instructions to keep a diary recording meal
3 AMBULATORY GASTRIC ph MONITORING 1157 times, times of recumbent posture, and time of rising from the recumbent position. Subjects were encouraged to perform their normal daily activities and not restrict their diet. They returned the following day after a minimum of 18 h to have their probes removed and their diaries reviewed. Post-calibration of the ph probes was not performed. We performed three separate experiments to determine: (i) the optimum probe location to measure the presence of gastric acid; (ii) the reproducibility of ph values in this optimal gastric location; and (iii) the range of percentage time ph < 4 in this region to establish normal population values. Experiment 1Ðoptimal probe location. Five volunteers were studied with two dual channel 24-h ambulatory ph probes placed simultaneously. One dual 24-h ph probe with 10 cm separation between the sensors was inserted under uoroscopic guidance until the distal sensor was located in the region of the gastric antrum. Antral positioning was con rmed by locating the sensor either in the plane of the spine or to the right of the spine with an upward de ection at the end of the ph probe apparatus caused by abutting against the pylorus. The second sensor was located 10 cm proximal in the gastric body. A second dual channel 24-h ph probe with 15 cm separation between the sensors was inserted without the aid of uoroscopy such that the proximal sensor was 5 cm above the proximal border of the lower oesophageal sphincter in the distal oesophagus and the distal sensor was located 10 cm below the proximal border of the lower oesophageal sphincter in the gastric fundus. Repeat uoroscopy was performed after both ph probes were placed to con rm nal position and to ensure the rst probe apparatus did not migrate with insertion of the second (Figure 1). Fluoroscopy was conducted at the end of the 24-h testing period to document probe positions prior to removal. Experiment 2Ðreproducibility studies. A separate group of ve volunteers was evaluated with two dual channel 24-h ambulatory ph probes. One dual 24-h ph probe with 15 cm separation between the sensors was placed with the proximal sensor 5 cm above and the distal sensor 10 cm below the proximal margin of the lower oesophageal sphincter. A second, identical, dual channel probe apparatus was then inserted to the same level. After both probes were positioned, uoroscopy was performed to con rm that the two distal sensors were well situated in the gastric fundus and separated by no more than 2 cm (Figure 2). The uoroscopic examination was repeated prior to removal of the probes to document that no migration occurred over the study period. Experiment 3Ðnormal gastric ph values. A total of 35 volunteers were evaluated with a dual 24-h ambulatory ph probe to record data for normal ph values in the gastric fundus. Ten subjects' values were obtained from the previous two studies, and 25 additional subjects were recruited for this arm of the study. After oesophageal manometry was performed to identify the location of the lower oesophageal sphincter, one dual channel 24-h ph probe with 15 cm separation between the sensors was placed with the distal sensor located Figure 1. Fluoroscopic con rmation of probes placed in three gastric regions.
4 1158 W. K. FACKLER et al. Figure 2. Fluoroscopic con rmation of probes placed in same gastric vicinity. 10 cm below the superior margin of the lower oesophageal sphincter in the gastric fundus and the proximal sensor 5 cm above the superior margin of the lower oesophageal sphincter in the distal oesophagus. Data analysis After each study, ph data were downloaded on to an IBM-compatible computer for analysis using a commercially available software package (Synectics Gastrosoft Esophagram, Milwaukee, WI). All ph data were reviewed and analysed both for the entire study period and with meal times (based on diary charting of starting and nishing a meal) excluded. The ph data (% time ph < 4) from all electrodes were individually analysed for the total, upright, and recumbent periods. The mean percentage time ph < 4 for the gastric fundus, body, and antrum probe locations were calculated. The optimum gastric region was identi ed based on the region with the greatest percentage time ph < 4. A paired, two-tailed Student's t-test was utilized to analyse differences between mean percentage time ph < 4 for these gastric regions. Reproducibility was determined by performing a linear regression analysis between the means of the ph data for the pair of electrodes placed concurrently in the same gastric location. The correlation coef cient was calculated based on these values. Normal values re ect the mean and associated 95% con dence intervals from the ph data for the total, upright, and recumbent periods. RESULTS Experiment 1Ðoptimal probe location All patients were able to tolerate the two simultaneous probes. Placement of the rst probe apparatus into the gastric antrum was noted to be more dif cult than positioning the second probe apparatus into the gastric fundus. The serial uoroscopy studies performed both before and after the 24-h study period demonstrated that no probes moved from their initial positions. The mean total percentage time intragastric ph < 4 for the fundus was 92.2%, body 90.1%, and antrum 54.6% (Figure 3). The differences between mean percentage time ph < 4 in the fundus and body were not signi cantly different for the total, upright, or supine time periods (P ˆ 0.50, P ˆ 0.62, and P ˆ 0.24, respectively). However, both the fundus and body demonstrated a mean percentage time ph < 4 that was signi cantly greater than the antrum for the total time period (P < 0.01). The antrum was not signi cantly different from either the fundus or the body for the upright time period: 88.6% vs. 56.1% (P ˆ 0.087) and 84.8% vs. 56.1% (P ˆ 0.15), respectively. The antrum was signi cantly less than the fundus and body for the recumbent period: 96.5% vs. 51.6% (P ˆ 0.002) and 93.2% vs. 51.6% (P < 0.001), respectively (Figure 4). Experiment 2Ðreproducibility studies The fundus served as the site for experiment 2 because no other gastric zone demonstrated a greater percentage
5 AMBULATORY GASTRIC ph MONITORING 1159 time ph < 4. The fundus was chosen instead of the body because the location was based on a more readily available objective measure, the lower oesophageal sphincter, as opposed to a uoroscopic image. The ph values from this location were highly reproducible in ve subjects (Figure 5). Linear regression analysis of the mean percentage time ph < 4 for the study period revealed signi cant agreement between side by side probes (r ˆ 0.98, r 2 ˆ 0.96, P ˆ 0.004). Figure 3. Five healthy volunteers studied with ph probes located concurrently in the gastric fundus, body and antrum. Experiment 3Ðnormal gastric ph values Thirty- ve sets of data were used to derive the normal values for mean percentage time gastric ph < 4. Our population consisted of 24 males (mean age 37.5 years, range 18±68) and 11 females (mean age 49.7 years, range 25±68). Normal values (mean 95th percentile) for percentage time gastric ph < 4 in the fundus were: total %, upright % and supine %. Data are presented with meal times excluded from the analysis (Figure 6). There were no signi cant differences between men and women for either the total, upright, or recumbent time periods and excluding meals from the analysis did not signi cantly alter the overall values (Table 1). DISCUSSION Figure 4. Comparison of fundus, body, and antrum mean percentage time ph < 4 during the supine periods for ve healthy volunteers in experiment 1. The need to de ne the location in the stomach which is most likely to demonstrate the presence of gastric acid is crucial when conducting intragastric ph monitoring, especially as clinicians begin utilizing this technique for different purposes, including to direct therapy for Figure 5. Reproducibility of ph measurements demonstrated by the mean percentage total time ph < 4 as measured by two side-by-side ph probes located in the gastric fundus.
6 1160 W. K. FACKLER et al. Figure 6. Mean percentage total, upright, and supine time ph < 4 in the gastric fundus as measured in 35 normal volunteers. patients with resistant GERD and to assess the diagnosis of acid-related extra-oesophageal complaints. 14, 15 We found that the gastric fundus was the optimal location to measure the intragastric ph. The advantages of studying this anatomic region of the stomach include: (i) no other zone in the stomach demonstrates the presence of ph < 4 for a greater period of time; (ii) the appearance of night-time alkaline tide rarely affects the gastric fundus; (iii) the area is easily accessible by advancing a ph probe 10 cm beyond the superior margin of the lower oesophageal sphincter without the necessity of uoroscopy; and (iv) the mean percentage time 24-h ph results are highly reproducible. It is not surprising that the fundus is the gastric region of greatest acidity. Here, the parietal cell mass is high with a predominance of oxyntic glands. Additionally, the fundus may serve as a storage zone, especially at night when an individual is supine, allowing for pooling of acidic gastric secretions. There appears to be little in uence in the gastric fundus from the night-time alkalization that occurs in the more distal stomach locations. We presume that this night-time elevation of gastric ph, because of its antral predominance and timing during sleep when gastric contractions are relatively nonexistent, is due to bile re uxate from the 16, 17 duodenum. In contrast, other studies have suggested the antrum as the location which best represents gastric acidity because of the effect that meals have on gastric ph. Ingestion of a meal typically produces a rise in fundic ph that is seen to a much lesser degree in the antrum, representing the buffering effect of food as it is digested. 18 We noted this pattern of gastric ph change in the fundus as well. Our data show, however, that whether or not the meal times are excluded, the fundus remains the optimal location to analyse for the presence of gastric acid. As for applying this technique to general use, we feel that intragastric ph analysis should be performed with the meal times excluded. By doing so, the immediate effects of a meal, whatever its size or constitution, upon the gastric ph pro le are minimized. This makes gastric ph monitoring more practical to perform on a daily basis because there is no need for a prede ned `standardized' diet that patients nd impractical and which may contribute to arti cial results. Another feature making the fundus the optimal location for placing the ph probe is accessibility. Using a well de ned landmark such as the lower oesophageal sphincter ensures that the ph probe can be placed reliably with little discomfort to the patient. The tendency is for the probe tip to migrate immediately into the fundus when it enters the stomach because of either de ecting off the lesser curvature or due to the angle of insertion when passing through the lower oesophageal sphincter. Fluoroscopy was never needed to assist with insertion of the probes into the fundus. On the other hand, the tendency of the probe to feed into the fundus made placement into the antrum or body more dif cult, requiring uoroscopic guidance, multiple manipulations of the probe, and frequent repositioning of the patients. Our method of executing concurrent gastric ph readings demonstrates that the ph probes are consistent in reporting the ph of the local environment of the fundus. Because both probes provided ph readings that were well correlated over the whole testing period, it is Total Upright Supine All patients 94.8% (93.0±96.4) 93.6% (91.4±95.7) 95.9% (93.5±98.3) (meals included) All patients 95.6% (94.1±97.1) 94.8% (93.0±96.6) 96.5% (94.2±98.8) (meals excluded) Males 95.1% (92.8±97.4) 94.3% (91.6±97.0) 96.0% (92.5±99.5) Females 96.6% (95.4±97.8) 95.9% (94.5±97.3) 97.5% (95.9±99.1) Table 1. Mean percentage time ph < 4 (95% CI) for the total, upright, and supine time periods for all patients, males and females
7 AMBULATORY GASTRIC ph MONITORING 1161 unlikely that a sensor provided inaccurate readings from either being trapped in a local pool of acid or from being wedged deeply against the gastric mucosa. The most important feature of this experimental arm however, was the demonstration that probe migration did not occur during the course of our study as assessed by uoroscopy. Earlier, reproducibility was documented by performing sequential daily ph analyses. 9 Although illustrating the ability of the ph probe to document daily variations in gastric ph patterns, this technique does not address actual intra-subject gastric ph reproducibility. There is no way to ensure that the ph variations of the stomach are going to be the same on a day-to-day basis even when controlling for meals, because the investigator cannot control all the variables regulating acid production such as histamine, gastrin, and vagal stimulation. Later, Barlow et al. performed simultaneous gastric ph monitoring with two ph probes positioned concurrently at the same position below the lower oesophageal sphincter. 18 They reported results of ph variations between the two probes of less than 1 ph unit for more than 90% of the study period. Our ndings are in agreement with their results. Our data are reported as the mean percentage time for which gastric ph < 4. Many studies now display data as mean percentage time for which ph < 4 instead of the earlier practice of describing mean or median ph values. 19, 20 We agree with other authors that representing the ph through an arithmetic mean or median absolute ph value can hide variations of ph in the 21, 22 stomach. Changes in ph which are clinically important (e.g. a drop in ph from 4 to 3) but brief may be lost if an arithmetic median or mean ph is calculated. By describing the data around a cut-off ph value, we are able to extract the time periods where an injurious re uxate medium is present in the stomach. We selected our cut-off value as a ph of 4 because the activation of pepsinogen to pepsin takes place at this ph, and this value is the standard reference for oesophageal ph monitoring. Of course, none of these techniques presumes actual acidity of the stomach because gastric volumes are not measured with ph probes. This study establishes a set of normal values for the percentage time 24 h intragastric ph < 4. Because normal values for distal oesophageal ph monitoring are the cornerstone for diagnosing gastro-oesophageal re ux disease with ambulatory ph monitoring, normal values for percentage time gastric ph < 4 are important for comparison when describing a patient's response to acid suppression therapy. Variations between the mean percentage time ph < 4 when analysing different individuals may be accounted for by one of two factors. First, the presence of Helicobacter pylori can elevate the gastric ph by causing a chronic pangastritis which decreases parietal cell acid production. 23 This was not controlled for in our study. Second, parietal cell mass is somewhat dependent on size and gender. 24 Small women tend to have less acid production capacity than do large men. A smaller volume of acid may be more in uenced by the appearance of alkaline contents from the small intestine or from acid neutralizing saliva. In our study, we did not nd a difference between mean percentage time ph < 4 for men and women, suggesting that this effect may be of minor importance. In summary, recording continuous ph of the stomach is best performed by placing the probe in the fundus. This region demonstrates the presence of an injurious re uxate for a greater period of time than either the antrum or body. ph measurements are reproducible, and the probe is easily placed in this location. These studies con rm the scienti c validity of intragastric ph monitoring and standardize its application. REFERENCES 1 Richter JE, ed. Ambulatory Esophageal Ph Monitoring, Ed 2. Baltimore, MD: Williams & Wilkins, 1997: 77±94. 2 Castell DO. My approach to the dif cult GERD patient. Eur J Gastroenterol Hepatol 1999; 11(Suppl. 1): S17±23. 3 Leite LP, Just RJ, Castell DO, et al. Control of gastric acid with high dose H2-receptor antagonists after omeprazole failure: report of two cases. Am J Gastroenterol 1995; 90: 1874±7. 4 Koufman JA. The otolaryngologic manifestations of gastroesophageal re ux disease (GERD): a clinical investigation of 225 patients using ambulatory 24-hour ph monitoring and an experimental investigation of the role of acid and pepsin in the development of laryngeal injury. Laryngoscope 1991; 101(Suppl. 53): 1±74. 5 Vaezi MF, Schroeder PL, Richter JE. Reproducibility of proximal probe ph parameters in 24-hour ambulatory esophageal ph monitoring. Am J Gastroenterol 1997; 92: 825±9. 6 Mattioli S, Felice V, Pilotti V, et al. Indications for 24-hour gastric ph monitoring with single and multiple probes in clinical research and practice. Dig Dis Sci 1992; 37: 1793± Fisher RS, Sher DJ, Donahue D, et al. Regional differences in gastric acidity and antacid distribution: is a single ph electrode enough? Am J Gastroenterol 1997; 92: 263±70. 8 Krawiec J, Odes HS, Schwartz B, et al. Regional differences in ambient intraluminal gastric acidity after cimetidine monitored by intragastric ph-metry. Am J Gastroenterol 1983; 78: 272±5.
8 1162 W. K. FACKLER et al. 9 Cilluffo T, Armstrong D, Castiglione F, et al. Reproducibility of ambulatory gastric ph recordings in the corpus and antrum. Scand J Gastroenterol 1990; 25: 1076± McLauchlan G, Fullarton GM, Crean GP, et al. Comparison of gastric body and antral ph: a 24 hour ambulatory study in healthy volunteers. Gut 1989; 30: 573±8. 11 Fuchs KH, DeMeester TR, Hinder RA, et al. Computerized identi cation of pathologic duodenogastric re ux using 24-hour gastric ph monitoring. Ann Surg 1991; 213: 13± Katzka DA, Gideon RM, Castell DO. Normal patterns of acid exposure at the gastric cardia: a functional midpoint between the esophagus and stomach. Am J Gastroenterol 1998; 93: 1236± Fisher RS, Sher DJ, Donahue D, et al. A single intragastric electrode does not accurately measure intragastric acidity. Am J Gastroenterol 1996; 91: 1167± Leite LP, Johnston BT, Just RJ, et al. Persistent acid secretion during omeprazole therapy: a study of gastric acid pro les in patients demonstrating failure of omeprazole therapy. Am J Gastroenterol 1996; 91: 1527± Fackler WK, Hunter JG, Waring JP. Does gastric ph monitoring add to the utility of esophageal ph monitoring in patients with atypical GERD failing medical therapy. Am J Gastroenterol 1998; 93: 1615 (Abstract). 16 Bjornsson ES, Abrahamsson H. Nocturnal antral ph rises are related to duodenal phase III retroperistalsis. Dig Dis Sci 1997; 42: 2432±8. 17 Verdu EF, Fraser R, Murphy GM, et al. The origin of nocturnal intragastric ph rises in healthy subjects. Scand J Gastroenterol 1995; 30: 935± Barlow AP, Hinder RA, DeMeester TR, et al. Twenty-four-hour gastric luminal ph in normal subjects: In uence of probe position, food, posture, and duodenogastric re ux. Am J Gastroenterol 1994; 89: 2006± Emde C, Garner A, Blum A. Technical aspects of intraluminal ph-metry in man: current status and recommendations. Gut 1987; 28: 1177± Fimmel CJ, Etienne A, Cilluffo T, et al. Long-term ambulatory gastric ph monitoring: validation of a new method and effect of H 2 -antagonists. Gastroenterology 1985; 88: 1842± Mela GS, Savarino V, Sumberaz A, et al. Continuous acidity monitoring in the study of gastric antisecretory drugs: ph or antilog transformation of ph, mean or median? Am J Gastroenterol 1990; 85: 1105±8. 22 van Herwaarden MA, Samson M, Smout AJPM. 24-h recording of intragastric ph: technical aspects and clinical relevance. Scand J Gastroenterol 1999; 34(Suppl. 230): 9± El-Omar EM, Oien K, El-Nujumi A, et al. Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterology 1997; 113: 15± Prewett EJ, Smith JTL, Nwokolo CU, et al. Twenty-four hour intragastric acidity and plasma gastrin concentration pro les in female and male subjects. Clin Sci 1991; 80: 619±24.
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