Acidic and Non-Acidic Reflux During Sleep Under Conditions of Powerful Acid Suppression*

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1 Original Research SLEEP MEDICINE Acidic and Non-Acidic Reflux During Sleep Under Conditions of Powerful Acid Suppression* William C. Orr, PhD; Andrea Craddock, PhD; and Suanne Goodrich, PhD Background: During sleep, individuals are uniquely vulnerable to acid reflux. Acid reflux during sleep has been studied by a number of investigators, but non-acid reflux is largely unexplored. Methods: In this study, 15 individuals with significant subjective complaints of heartburn were treated with esomeprazole, 40 mg bid, and with placebo, in random order, for 1 week each. After 1 week of treatment, participants underwent combined impedence/ph monitoring and polysomnography. In both drug and placebo conditions, these procedures were done after participants consumed a meal designed to increase the likelihood of reflux events. Results: Total reflux events and acid reflux events were significantly decreased with proton-pump inhibitor (PPI) treatment as compared to placebo. Nonacid reflux events were more common with PPI treatment as compared to placebo, but this result was not statistically significant. The ratio of non-acidic to acidic events was significantly greater with PPI treatment, however. Similar results were found for reflux events that occurred only during sleep. Proximal migration of acidic vs non-acidic reflux events was found to be similar. There was no difference in sleep architecture between placebo and drug conditions. Conclusion: PPI treatment reduced overall reflux events, but non-acidic reflux events were relatively more likely to occur with PPI treatment. The occurrence of these non-acidic reflux events on PPI might conceivably explain why some individuals continue to have symptoms after PPI treatment. (CHEST 2007; 131: ) Key words: esophagus; gastroenterology; pharmacology Abbreviations: GER gastroesophageal reflux; MII multichannel intraluminal impedence; PPI proton-pump inhibitor; SRRE sleep-related reflux event; VAS visual analog scale; WASO wakefulness after sleep onset A number of factors that are critical in the acid clearance process are markedly suppressed during sleep. These include swallowing, salivary production, and suppression of a conscious response to acid mucosal contact (ie, heartburn). 1 Furthermore, sleep has been shown to facilitate the proximal migration of acid infused into the distal esophagus. 2 Supine *From the Lynn Health Science Institute, Oklahoma City, OK. This study was performed at the Lynn Health Science Institute. This study was supported by a research grant from Astra Zeneca. The authors have no conflicts of interest to disclose. Manuscript received May 22, 2006; revision accepted October 3, Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( org/misc/reprints.shtml). Correspondence to: Suanne Goodrich, PhD, Lynn Health Science Institute, 5300 N Independence, Suite 130, Oklahoma City, OK 73112; sgoodrich@lhsi.net DOI: /chest (during the sleeping interval) acid contact time is a major contributing factor to the development of the esophageal complications of acid reflux. 3,4 Although sleep-related acid reflux has been shown to be an important variable contributing to the complications of gastroesophageal reflux (GER), very few investigations have focused on the fact that under conditions of the usual treatment of GER with acid suppressing agents, non-acidic reflux persists. 5 Nonacidic reflux after acid suppression therapy has been linked to the persistence of symptoms and poor healing in a small percentage of patients. 6,7 Furthermore, non-acidic bile reflux has been documented to occur continuously during the nighttime No studies to date have actually monitored acidic and non-acidic reflux subsequent to powerful acid suppression with a proton-pump inhibitor (PPI) drug in order to access whether or not non-acidic 460 Original Research

2 reflux may persist during sleep. A study 11 from our laboratory has shown that acid mucosal contact during sleep leads to an arousal response that enhances the efficiency of acid clearance. It is not known whether non-acidic mucosal contact, being of more neutral ph, would also produce a similar arousal response. In the absence of this, one could speculate that the occurrence of non-acidic reflux during sleep might result in increased risk of prolonged mucosal exposure to bile salts and pancreatic enzymes, as well as increased risk of proximal migration and pulmonary aspiration. Although symptoms may persist postprandially with PPI treatment, and these may be attributed to non-acidic reflux, symptoms appear to change primarily from heartburn to regurgitation. 5 If the alteration in symptoms is a result of non-acidic reflux, questions remain: does non-acidic mucosal contact persist during sleep, and does it provide an adequate stimulus to awaken patients and prevent proximal migration and aspiration? In the present study, we examined the occurrence of acidic and non-acidic reflux during sleep under conditions of powerful acid suppression utilizing impedance and ph measurement techniques. Patients Materials and Methods A total of 15 individuals (9 men and 6 women; mean age, 45.3 years) were recruited to participate in the present study. All subjects endorsed symptomatic GER with complaints of heartburn occurring at least 4 d/wk and nocturnal heartburn occurring at least once a week. Subjects were excluded if they had a history of Barrett esophagus, any abdominal surgery involving the stomach or duodenum, significant history of neurologic or psychiatric disorders requiring the use of regular prescription medication, or any other significant medical conditions such as chronic renal or liver disease. It was requested that all subjects cease taking antacids, histamine type-2 blockers, PPIs, or other medications that alter acid content in the stomach at least 1 week prior to participating in the study. Procedure The Western Institutional Review Board approved the study, and all subjects gave written informed consent. During the initial visit, the study coordinator obtained the medical and medication history as well as vital signs. A physical examination was also performed. Eligible participants were then scheduled for two sleep studies that included multichannel intraluminal impedance (MII) and ph monitoring. They were also given enough study medication for 1 week, as well as a sleep log to chronicle their subjective sleep quality using a 100-point (millimeter) visual analog scale (VAS). The VAS is commonly used in many fields to assess symptom severity. Study medication was taken twice per day before breakfast and then again before dinner. It was advised that medication be taken at approximately 6 am and 6 pm. Approximately 1 week later, subjects returned to the laboratory for MII/pH catheter insertion, which occurred in the late afternoon. After going home for a few hours, participants returned to the sleep laboratory for complete polysomnography. MII/pH recording was conducted from lights out until lights on during the sleep study. One hour prior to lights out, subjects ate a provocative meal consisting of a large piece of pizza, a brownie, and grape juice. This was done in order to raise the baseline occurrence of reflux events in order to facilitate the assessment of a treatment effect. The next morning, the electrodes were removed and the MII/pH probe was extracted. The sleep technicians provided a new bottle of medication and another sleep log to each participant to be taken and filled out for the next week. After another week of taking medication twice daily and completing the sleep log, the patients returned for their final MII/pH session and polysomnography. In order to minimize order effects, patients were randomly exposed to either an oral dose of esomeprazole, 40 mg bid, or placebo for 1 week preceding each MII/pH sleep laboratory evaluation. Neither the patients nor the sleep technicians knew in what order drug vs placebo would be administered. Combined Intraluminal Electrical Impedance and ph Measurement MII used together with ph measurement is a novel technique that can detect both acid and non-acid reflux events. 5 This tool can differentiate between swallows and reflux because of its ability to detect both anterograde and retrograde bolus movement. This capacity to identify retrograde gastric material in the esophagus allows the MII to detect reflux events in general. By using a ph measurement in combination with the MII, one can determine whether the reflux is non-acid reflux vs acid reflux. MII was designed based on the principles of electrical impedance. Impedance (expressed in ohms) is the assessment of total resistance to current flow between two electrodes. Electrical conductivity is inversely related to impedance and is contingent on the ionic concentration of the bolus material in the esophageal lumen. Bolus material with a high ionic content (ie, refluxate, food, saliva) is more conductive (less resistance) compared to other substances (ie, air) that have less ionic content. Thus, through its ability to monitor impedance changes, MII can determine the movement of a substance and its proximal migration within the esophagus. Using a MII/pH catheter (Sandhill Scientific; Highland Ranch, CO), data combining intraluminal electrical impedance and ph measurements were collected on each subject. Briefly described, the catheter has six pairs of electrodes that measure impedance: four pairs are located in the distal esophagus, and two pairs are located in the proximal esophagus. The catheter is passed into the esophagus transnasally and situated such that the ph sensor is 5 cm above the proximal border of the lower esophageal sphincter, and the impedance-measuring sites are positioned 3, 5, 7, 9, 15, and 17 cm above the lower esophageal sphincter. Analysis After the data were acquired, MII/pH tracings were analyzed using a specially designed software program (BioView Analysis; Sandhill Scientific). MII/pH tracings were analyzed in conjunction with the polysomnography data for the following: (1) number of acidic (ph 4.0 for at least 5 s) and non-acidic (MII-identified retrograde bolus movement without the drop in ph 4.0) reflux events; (2) proximal migration of acid and non-acid refluxate; (3) number of sleep-related acid and non-acid reflux events (sleeprelated reflux events [SRREs]) [reflux events occurring during polysomnography-documented sleep]; (4) reflux events that ocwww.chestjournal.org CHEST / 131 / 2/ FEBRUARY,

3 Figure 1. Total reflux events in placebo and drug conditions. *Total reflux events while receiving PPI vs placebo, p Acid events while receiving PPI vs placebo, p curred during an awakening from sleep or waking after sleep onset (WASO); (5) total sleep time during placebo and drug conditions; (6) sleep efficiency (total sleep time divided by time in bed 100) during placebo and drug conditions; (7) sleep onset latency (minutes from lights out until the participant fell asleep) during placebo and drug conditions; and (8) subjective sleep quality from the VAS obtained from the morning log. Since the MII/pH data and polysomnography data were collected on different systems, it was necessary to perform a time stamp on the MII/pH tracing and polysomnography just prior to the beginning of each study. Then, both studies could be examined simultaneously on side-by-side computers. When reflux events appeared on the MII/pH tracing, the polysomnography could be examined at the same point in time during the night to determine whether the patient was asleep or awake. Given the nonnormal distribution of the variables of interest, nonparametric statistics (ie, Wilcoxon signed-rank test) were employed, and an -level of 0.05 was deemed significant. Reflux Results Participants had a total of 73 reflux episodes (67 acidic, 6 non-acidic) on placebo vs 39 reflux episodes on esomeprazole (12 acidic, 27 non-acidic). As expected, both total reflux and acid reflux events were significantly decreased under drug conditions (p 0.05 and p 0.01, respectively; Fig 1). Nonacidic reflux events were increased substantially, but the result was not statistically significant. It is notable that under conditions of powerful acid suppression, nearly 70% of all reflux events were not acidic, while under placebo conditions, 10% were non-acidic. Thus, the ratio of non-acidic to acidic events was Figure 2. Percentage of reflux events occurring during sleep and WASO. *Acidic events in sleep vs WASO, p Original Research

4 Figure 3. Percentage of sleep-related acidic and non-acidic reflux events resulting in arousal from sleep. significantly greater with PPI treatment (p 0.05). The proximal migration of acid and non-acid refluxate was comparable (8.51 cm acidic vs 8.46 cm non-acidic). Reflux That Occurred During Sleep and During WASO SRREs were compared to reflux events that occurred during WASO. Reflux events were more likely to occur during periods of sustained sleep (SRRE more than WASO; p 0.05). There was a trend toward significance, in that acidic reflux events occurred more frequently during sleep than during WASO (p 0.055; Fig 2). Non-acidic reflux events occurred in similar frequency in both sleep and WASO (p 0.05; Fig 2). The above results suggest that acidic events are more common during sleep, while non-acidic events are about evenly split between periods of sleep and WASO. The percentage of acidic vs non-acidic reflux events resulting in arousal from sleep is shown in Figure 3. Although non-acidic events revealed a higher percentage of arousal responses, the results were not significantly different. Also, of note is that the majority of reflux events that occurred during sleep, whether acidic or non-acidic, resulted in an arousal response within 2 min. Finally, it was found that sleep-related acidic reflux events occurred with greater frequency with placebo (p 0.01), whereas there was a trend for more sleep-related non-acidic events to occur with powerful acid suppression (p 0.07; Fig 4). For individual patient data on selected variables, refer to Table 1. Results From Sleep Parameters There were no significant differences on various objective sleep measures including total sleep time, sleep efficiency, and sleep onset latency for placebo Figure 4. Total number of reflux events during sleep in placebo and drug conditions. *Total events while receiving PPI vs placebo, p Acid events while receiving PPI vs placebo, p **Non-acid events while receiving PPI vs placebo, p CHEST / 131 / 2/ FEBRUARY,

5 Table 1 Individual Patient Data for Selected Variables* Placebo Drug Total Sleep WASO Total Sleep WASO MII/pH Total Recording Time, min Total Reflux Total During Sleep Total During WASO Non-Acidic on Drug Acidic on Drug Non-Acidic on Placebo Acidic on Placebo Patient No *Data are presented as No. unless otherwise indicated. Average for both nights of min, or approximately 7 h per night. vs drug conditions (Table 2). There was also no significant difference on the VAS measure of subjective sleep quality whether they were taking placebo or drug (Table 2). Discussion The present study has documented a decrease in total reflux events under conditions of powerful acid suppression during sleep. There was a trend for more non-acidic reflux events to occur with PPI treatment. These results during sleep are in contrast to two previous studies, 5,12 both conducted in the waking state, which indicated that the overall incidence of GER was not altered by treatment with a twice-daily dose of omeprazole, 20 mg. Arousals from sleep were equally likely to occur whether reflux was acidic or non-acidic. This finding was somewhat surprising and, to our knowledge, has not previously been documented in the literature. To the extent that arousals due to reflux are disruptive and theoretically might contribute to poorer sleep quality, this finding is important and should be verified in future investigations. Proximal migration of the refluxate was likewise similar regardless of its acidity. Also, it was found that reflux events were more frequent during sleep compared to sustained awakenings from sleep (WASO). A study by Freidin and colleagues 13 has shown that reflux events were most common in association with wakefulness or with brief arousals from sleep. Our finding was in contrast to this observation, and further research is needed to clarify whether or not reflux events do occur more commonly with arousals from sleep. Thus, our data indicate that both acidic and non-acidic reflux persists during sleep despite PPI treatment. However, there was a trend for non-acid reflux to increase under conditions of powerful acid suppression. These data should be assessed with the proviso that patients were subjected to a provocative meal prior to going to sleep. This was done in order to increase the frequency of reflux, which would be minimal under conditions of powerful acid suppres- Table 2 Sleep Parameters in Placebo and Drug Conditions* Sleep Parameters Placebo Drug Total sleep time, min (41.6) (51.9) Sleep efficiency, % 82.1 (9.9) 80.1 (10.5) Sleep onset latency, min 21.3 (23.2) 14.7 (11.6) Subjective sleep quality 54.6 (16.7) 54.8 (14.6) *Data are presented as mean (SD). No significant differences found. Using 100-point (millimeter) VAS. 464 Original Research

6 sion during sleep. These data may not generalize to the typical meals consumed by individuals with heartburn. It should also be noted that although participants were advised to take their study medication at the same times each day (ie, 6am and 6 pm), some patients did not strictly comply with this advice. Thus, there may have been some differences in the timing of study medication administration and therefore some variation in response efficacy. Also, subjects were studied approximately 7 days apart. This interval is considered more than adequate to wash out any drug effect. Although there are no data on a 40-mg-bid dose, 3 to 4 days is considered adequate to reduce blood levels of a 40-mg dose of esomeprazole to an insignificant level. Previous studies 4,11 in our laboratory have noted the prolongation of esophageal acid contact time during sleep, and the importance of an arousal from sleep in the acid clearance process. In short, an arousal from sleep invokes swallowing and salivation that facilitate acid clearance and neutralization. Our study 14 documented that the higher the percentage of wakefulness during the acid clearance process, the faster acid in the distal esophagus is neutralized. We have also documented 15 that stimulation of the esophagus during sleep by increasing concentrations of hydrogen ions (ie, ph values of 5.0, 3.0, and 1.2) resulted in much shorter acid clearance times. There are also data to suggest that pulmonary aspiration may be prevented by arousals from sleep in response to provocative stimulation of the pharynx. 16 This raises the question as to whether non-acidic reflux (having a relatively low concentration of hydrogen ions) would be able to adequately stimulate the esophagus and produce these protective arousal responses. Our data, however, suggest that the esophagus is equally responsive to acidic and nonacidic reflux, in that arousal responses to non-acidic stimulation were as frequent as with acidic stimulation, and proximal migration was not significantly different between acidic and non-acidic reflux events. In summary, this study documents a trend for an increase in non-acid reflux during sleep subsequent to powerful acid suppression with esomeprazole. Total reflux events were significantly diminished during sleep, but non-acidic reflux events were somewhat increased under conditions of acid suppression. The esophagus was equally responsive to acidic and non-acidic reflux events in terms of both eliciting arousal responses, and preventing significant proximal migration. Although the esophagus does appear to recognize and respond to non-acid reflux events, the relative increase in non-acidic reflux events may explain the persistence of symptoms in some patients treated with PPIs. References 1 Orr WC, Heading R, Johnson LF, et al. Sleep and its relationship to gastro-oesophageal reflux. Aliment Pharmacol Ther 2004; 20(suppl9): Orr WC, Elsenbruch S, Harnish MJ, et al. Proximal migration of esophageal acid perfusions during waking and sleep. Am J Gastroenterol 2000; 95: DeMeester TR, Johnson LF, Joseph GJ, et al. Patterns of gastroesophageal reflux in health and disease. Ann Surg 1976; 184: Orr WC, Allen MI, Robinson M. The pattern of nocturnal and diurnal esophageal acid exposure in the pathogenesis of erosive mucosal damage. Am J Gastroenterol 1994; 89: Vela MF, Camacho-Lobato L, Srinivasan R, et al. Simultaneous intraesophageal impedance and ph measurement of acid and nonacid gastroesophageal reflux: effect of omeprazole. Gastroenterology 2001; 120: Vaezi MF, Richter JE. Synergism of acid and duodenogastroesophageal reflux in complicated Barrett s esophagus. Surgery 1995; 117: Wetscher GJ, Glaser K, Hinder RA, et al. Respiratory symptoms in patients with gastroesophageal reflux disease following medical therapy and following antireflux surgery. Am J Surg 1997; 174: Gotley DC, Morgan AP, Cooper MJ. Bile acid concentrations in the refluxate of patients with reflux oesophagitis. Br J Surg 1988; 75: Champion G, Richter JE, Vaezi MF, et al. Duodenogastroesophageal reflux: relationship to ph and importance in Barrett s esophagus. Gastroenterology 1994; 107: Kauer WKH, Peters JH, DeMeester TR, et al. Composition and concentration of bile acid reflux into the esophagus of patients with gastroesophageal reflux disease. Surgery 1997; 122: Orr WC, Robinson MG, Johnson LF. The effect of esophageal acid volume on arousals from sleep and acid clearance. Chest 1991; 99: Tamhankar AP, Peters JH, Portale G, et al. Omeprazole does not reduce gastroesophageal reflux: new insights using multichannel intraluminal impedance technology. J Gastrointest Surg 2004; 8: Freidin N, Fisher MJ, Taylor W, et al. Sleep and nocturnal acid reflux in normal subjects and patients with reflux oesophagitis. Gut 1991; 32: Orr WC, Johnson LF, Robinson MG. Effect of sleep on swallowing, esophageal peristalsis, and acid clearance. Gastroenterology 1984; 85: Orr WC, Johnson LF. Responses to different levels of esophageal acidification during waking and sleep. Dig Dis Sci 1998; 43: Huxley EJ, Viroslav J, Gray WR, et al. Pharyngeal aspiration in normal adults and patients with depressed consciousness. Am J Med 1978; 64: CHEST / 131 / 2/ FEBRUARY,

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