Barrett s Esophagus in Females: A Comparative Analysis of Risk Factors in Females and Males

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1 American Journal of Gastroenterology ISSN C 2005 by Am. Coll. of Gastroenterology doi: /j x Published by Blackwell Publishing Barrett s Esophagus in Females: A Comparative Analysis of Risk Factors in Females and Males Farzaneh Banki, M.D., Steven R. DeMeester, M.D., Rodney J. Mason, M.D., Guilherme Campos, M.D., Jeffrey A. Hagen, M.D., Jeffrey H. Peters, M.D., Cedric G. Bremner, M.D., and Tom R. DeMeester, M.D. Departments of Surgery and Cardiothoracic Surgery, Keck School of Medicine, The University of Southern California, Los Angeles, California OBJECTIVES: METHODS: RESULTS: CONCLUSIONS: Gastroesophageal reflux symptoms occur with similar frequency in males and females, yet Barrett s esophagus is less common in females. The reason for this disparity is unknown. The aim of this study was to determine the factors related to Barrett s in females. The records of 796 patients (462 male, 334 female) evaluated from 1990 to 2000 for symptoms of reflux were retrospectively reviewed. Physiologic abnormalities based on results of endoscopic, motility, ph, and Bilitec testing were identified, and factors related to the presence of Barrett s were determined using univariate and multivariate analysis. Females with reflux symptoms were significantly less likely to have a positive 24-h ph test, a defective lower esophageal sphincter, or a hiatal hernia than males with reflux symptoms. Further, females with reflux on the basis of an abnormal 24-h ph test had significantly less esophageal acid exposure than males with reflux. In contrast, esophageal exposure to refluxed acid and bilirubin was similar in females (n = 50) and males (n = 136) with Barrett s. On multivariable analysis increased esophageal bilirubin exposure was the only significant factor associated with the presence of Barrett s in male and female patients with reflux disease. Females with reflux symptoms have less esophageal acid exposure on average than males. However, females and males with Barrett s have a similar severity of reflux, and the female gender does not protect against the development of Barrett s in the setting of advanced reflux disease. Esophageal bilirubin exposure is the major risk factor for the presence of Barrett s in patients with reflux disease. (Am J Gastroenterol 2005;100: ) INTRODUCTION Barrett s esophagus is defined by the presence of intestinal metaplasia within a columnar epithelium-lined distal esophagus. Although the etiology and risk factors for Barrett s are incompletely elucidated, the presence of Barrett s has been correlated with the frequency and duration of gastroesophageal reflux symptoms, the presence and size of a hiatal hernia, and the degree of lower esophageal sphincter incompetency (1 7). Further, there is increasing evidence that the nature of the refluxed material is also important, and particular attention has focused on the role of alkaline or mixed gastroduodenal reflux in the pathogenesis of Barrett s esophagus (7 10). Interestingly, while none of the above factors are specifically gender related, the male gender is also a risk factor for Barrett s (7, 11). In most series, the ratio of males to females with Barrett s is 2:1, yet the reasons for this disparity Presented as a Poster of Distinction at the Annual Scientific Meeting of Digestive Disease Week May 20, have been largely unexplored. One hypothesis is that the female gender protects against Barrett s, perhaps because the esophageal squamous mucosa is more resistant to injury in females, or that female hormones including estrogen induce a protective effect. Other explanations are that females have less severe reflux disease than males, or that the nature of the material they reflux is different. The aim of this retrospective study was to characterize the pathophysiology of Barrett s esophagus in females and to determine: (i) if the same factors are associated with Barrett s in males and females, (ii) if females and males with Barrett s have a similar severity of reflux disease, and (iii) if a similar prevalence of Barrett s is present in a subgroup of females and males with severe reflux disease. METHODS For this study, we retrospectively reviewed the charts of 796 consecutive patients (462 males, 334 females) who presented to the Division of Thoracic and Foregut Surgery at USC between 1990 and 2000 for evaluation of heartburn, 560

2 Comparative Analysis of Risk Factors of Barrett s Esophagus 561 regurgitation, dysphagia, or a combination of reflux symptoms. Information about the nature and duration of the patients symptoms was obtained from review of the detailed history taken at the time of presentation of the patient to one of the authors, and is based on the patient s best recollection. This study was approved by the IRB of the University of Southern California. Definitions Barrett s esophagus was defined as any endoscopically visible length of columnar epithelium above the gastroesophageal junction (GEJ) with intestinal metaplasia on biopsy. This definition excluded all patients with a normal upper endoscopy and intestinal metaplasia at the GEJ on biopsy (intestinal metaplasia of the cardia), as well as those with a nonintestinalized columnar-lined distal esophagus. Long-segment Barrett s was defined as a length of Barrett s 3 cm. Upper GI Endoscopy Upper endoscopy was performed in all patients, and biopsies were obtained using large-capacity biopsy forceps (Microvasive radial jaw or ). The GEJ was defined as the location where, with the stomach decompressed, the proximal extent of the gastric rugal folds joined the tubular esophagus. The location of the GEJ, the squamocolumnar junction (SCJ), and the crural impression were carefully noted in each patient. A hiatal hernia was diagnosed when the GEJ was located 2 cm above the crural impression. In all patients biopsies were obtained antegrade and retroflexed from the GEJ, from the gastric antrum and fundus, and from 4-quadrants every 2 cm starting at the GEJ and going up to the SCJ in patients with a columnar segment extending proximally into the esophagus. Manometry Technique Esophageal manometry was performed with an eight-channel water perfused catheter using a standard station pull-through technique as previously described (12). The lower esophageal sphincter (LES) was classified as manometrically defective on the basis of one or more of the following: a resting pressure of less than 6 mmhg, an overall length of less than 2 cm, and /or an abdominal length of less than 1 cm. Ambulatory Esophageal ph Monitoring Technique Ambulatory measurement of esophageal acid exposure was performed over a 24-h period with a ph probe placed 5 cm above the upper border of the manometrically determined LES. Acid-suppressing medications were discontinued before testing (2 wk for proton pump inhibitors, 2 days for H 2 blockers). A commercially available software program (Synectics Medical, Minneapolis, MN) was used to analyze the tracing. Increased (abnormal) esophageal acid exposure was defined as a total time ph < 4greater than 4.4%. Ambulatory Esophageal Bilirubin Monitoring Technique Bilirubin exposure was determined over a 24-h period using a Bilitec probe (Bilitec 2000, Medtronic Inc., Gastrointestinal Division, Minneapolis, MN) placed 5 cm above the upper border of the manometrically determined LES. Acid-suppressing and antacid medications were discontinued 48 h before testing, and patients were instructed to follow a specific diet that excluded food that would interfere with the probe s function as previously described (13). A commercially available software program was used to analyze the tracing (Bilitec 2000, Synectics Medical, Dallas, TX). An absorbance threshold of 0.2 was used, and increased (abnormal) esophageal bilirubin exposure was defined as an exposure >2.2% for the 24-h period. Measurement of esophageal bilirubin exposure with the Bilitec probe was used as a surrogate for alkaline or duodenogastro-esophageal reflux. Pathology Biopsy specimens were fixed in 10% formaldehyde, embedded in paraffin, sectioned, mounted on slides, and stained with hematoxylin and eosin using standard techniques. A single expert GI pathologist interpreted all slides. Specialized intestinal metaplasia was determined by the presence of well-defined goblet cells on routine sections, and confirmed in select cases by positive staining with Alcian blue at ph 2.5. Giemsa stained antral biopsies were used to determine the presence of H. pylori infection. Statistics Data are reported as median and interquartile range unless otherwise specified. Fisher s exact test was used for categorical data while continuous variables were analyzed using the Mann-Whitney test. Factors potentially predictive of the presence of Barrett s esophagus in patients proven to have reflux disease on the basis of an abnormal 24-h ph test were assessed using univariate analysis and included age, body mass index (BMI), the duration of symptoms, presence of hiatal hernia, number of reflux episodes, number of reflux episodes lasting greater than 5 min, longest reflux episode, presence of a defective LES, and bilirubin exposure. Significant factors were then entered into a multivariable model as independent parameters. Forward stepwise logistic regression was performed to assess the joint effect of the variables and to define those that were independently associated with the presence of Barrett s esophagus in females and in males. The results are presented as adjusted odds ratios (OR) with 95% confidence limits (CL) and p-values from the adjusted Wald s test. The Wald test was computed in SPSS (Version 10) using the square of the coefficient divided by the standard error for the independent variables. All analyses were two-sided with significance set at 0.05 (α = 0.05). RESULTS Entire Population The characteristics of the entire population are shown in Table 1.Females evaluated for reflux symptoms were older and significantly less likely to have a positive 24-h ph test, a

3 562 Banki et al. Table 1. Characteristics of the Study Population Whole Population Females Males p-value n (42%) 462 (58%) Age (years) 52 (43 64) 54 (44 67) 51( ) 0.02 BMI (kg/m 2 ) 26.4 ( ) 26.7 ( ) 26.2 ( ) DOS (years) 6 (3 14) 6 (3 11) 6 (3 15) Number of patients with 24-h ph monitoring 769 (97%) 308 (92%) 461 (99%) Abnormal 24-h ph 506 (66%) 165 (49%) 341 (74%) Number of patients with manometry 776 (98%) 315 (94%) 461 (99%) Patients with defective LES 507 (65%) 185 (59%) 322 (70%) Number of patients with Bilitec probe 345 (43%) 132 (49%) 213 (46%) Abnormal Bilitec probe 164 (48%) 57 (43%) 107 (50%) Prevalence of hiatal hernia 441 (56%) 160 (48%) 281 (61%) Prevalence of H. pylori # 57 (12%) 18 (12.5%) 39 (11%) 0.74 Prevalence of Barrett s 209 (26%) 63 (18%) 146 (32%) Values are medians, (interquartile range) or (%). BMI: body mass index. DOS: Duration of symptoms. Females versus males. # Information on H. pylori status was available for 484 patients; 144 females and 340 males. defective LES, or a hiatal hernia than males evaluated for reflux symptoms during the same time period. Barrett s esophagus was present in 26% of the entire group, and was significantly more prevalent in males. From the 796 patients evaluated for reflux 263 patients were found to have normal esophageal acid exposure by 24-h ph monitoring, and 27 patients did not have a ph test. These 240 patients were excluded from further analysis. Comparison of Females and Males with Increased Esophageal Acid Exposure The characteristics of the 506 patients with increased esophageal acid exposure on 24-h ph monitoring are shown in Table 2. Compared to males, females with reflux disease were significantly older, had a greater body mass index, and had less esophageal acid exposure. Barrett s esophagus was present in 37% of patients with an abnormal 24-h ph test, and was significantly more prevalent in males. Long-segment Barrett s was more common in males while short-segment Barrett s predominated in females. Compared to patients with increased esophageal acid exposure but without Barrett s, females and males with Barrett s had significantly greater reflux of both acid and bilirubin (Figs. 1A, B), and were significantly more likely to have a positive Bilitec test (Table 3). There was no difference in the prevalence of an abnormal Bilitec test between females and males without Barrett s (p = 0.6), nor between females and males with Barrett s (p = 0.2). Lastly, we found that the overall length and pressure of the LES as well as the prevalence of a defective LES was significantly different in patients with and without Barrett s (Table 4). Comparison of Females and Males with Barrett s We found that females and males with Barrett s were remarkably similar. Females with Barrett s were older (median 57 vs 52 yr, p = 0.049), while males had a longer duration of symptoms (12 vs 10 yr, p = 0.049), but the differences were Table 2. Characteristics of the Population with Abnormal 24-h ph Test Whole Population Females Males p-value n (33%) 341 (67%) Age (years) 53 (44 64) 56 (47 67) 51(42 61) BMI (kg/m 2 ) 27.2 (24 30) 28.4 (26 33) 26.6 (24 29) DOS (years) 8 (3 16) 9 (3 13) 7 (3 17) Total % time ph < ( ) 9.2 ( ) 10.3 ( ) 0.03 Total % time bilirubin 6.0 ( ) 4.2 ( ) 7.7 ( ) 0.14 Prevalence hiatal hernia # 345 (85%) 113 (86%) 232 (85%) 0.77 Prevalence defective LES 383 (76%) 130 (79%) 253 (74%) 0.27 Barrett s esophagus 186 (37%) 50 (30%) 136 (40%) 0.04 Length of BE (cm) 3 (2 6) 2 (2 5.5) 4 (2 6) 0.35 <3cm; n = 72 (39%) 26 (52%) 46 (34%) cm; n = 114 (61%) 24 (48%) 90 (66%) 0.03 Values are medians, (interquartile range) or (frequency). BMI: body mass index (data available for 78%, 72%, and 81% of all patients, females, and males, respectively). DOS: Duration of symptoms. Females versus males. # Information available for 405 patients; 131 females and 274 males.

4 Comparative Analysis of Risk Factors of Barrett s Esophagus 563 Figure 1. (A) Results of ambulatory 24-h ph and (B) bilirubin (Bilitec) monitoring in ph positive females and males with and without Barrett s. Females without Barrett s had significantly less esophageal acid exposure than males without Barrett s. Further, both females and males without Barrett s had significantly less esophageal acid and bilirubin exposure than their counterparts with Barrett s. However, esophageal acid and bilirubin exposure was similar in females and males with Barrett s.

5 564 Banki et al. Table 3. Prevalence of an Abnormal Bilitec Test in 24-h ph Positive Patients No Barrett s Barrett s p-value Females (n = 45) 24 (50%) 21 (95%) Males (n = 96) 51 (55%) 45 (82%) marginally significant. The youngest female with Barrett s was 22yr, while the youngest male was 20 yr old. Physiologic evaluation demonstrated that the LES characteristics and esophageal acid and bilirubin exposure in females and males with Barrett s were not significantly different, nor was there a difference in the prevalence or size (median 3 cm for females and 4 cm for males, p = 0.09) of a hiatal hernia (Figs. 1A, B, Table 4). Predictors of Barrett s Esophagus in Patients with Reflux Disease Univariate analysis identified the duration of symptoms, presence of hiatal hernia, number of reflux episodes, number of reflux episodes lasting greater than 5 min, longest reflux episode, presence of a defective LES, and abnormal bilirubin exposure as potentially predictive factors for the presence of Barrett s in patients with 24-h ph proven reflux. Age and BMI were not significant factors. Multivariable analysis demonstrated that in both females and males with abnormal 24-h ph tests, the only significant factor independently associated with the presence of Barrett s was abnormal bilirubin exposure. The odds ratio for the presence of Barrett s esophagus in the setting of increased esophageal bilirubin exposure was 10.8 for females and 4.8 for males (95% CL , p = for females; , p < for males). Prevalence of Barrett s in Patients with Multiple Physiologic Abnormalities Suggesting Severe Reflux Disease Within the population of 796 patients who underwent evaluation for reflux symptoms, 98 patients (33 females and 65 males) had physiologic evidence of severe gastroesophageal reflux disease based on the presence of all of the following abnormalities: a defective LES, a hiatal hernia, and increased esophageal acid and bilirubin exposure based on 24-h ph and Bilitec testing. In this subgroup of patients the overall prevalence of Barrett s was 54%. Importantly, in these patients with severe reflux disease the prevalence of Barrett s was similar in females and males (females: 17/33 (52%) vs males: 36/65 (55%), p = 0.88). DISCUSSION Although a common disorder, much remains unknown about the epidemiology of Barrett s esophagus. Most studies have found distinct racial and gender differences, with females and non-caucasians significantly less likely to have Barrett s (14 17). In a study by Rex and colleagues 961 subjects who presented for screening colonoscopy initially underwent upper endoscopy (18). Barrett s esophagus was found in 4.6% of females compared to 8.2% of males (p = 0.04 by χ 2 ). While the racial differences in Barrett s are readily explained by the reduced incidence of reflux disease among non-caucasian populations, the gender difference is less easily understood. Kennedy et al. noted that the prevalence of reflux symptoms is similar in males and females in Western populations, and a study from Finland reported that more women than men were referred for upper endoscopy to evaluate reflux symptoms (19, 20) (personal communication with Dr. Voutilainen). Further, in a recent analysis of 4,684 people taking chronic acid suppression medication, the majority (55%) were female (21). In contrast to the similar prevalence of reflux symptoms and use of acid-suppression medication, complications from reflux disease including esophagitis, Barrett s, and adenocarcinoma of the esophagus are known to occur less commonly in females (14, 16, 20, 22, 23). This suggests that either some factor associated with the female sex protects against reflux complications, or that despite the presence of symptoms Table 4. Physiologic Characteristics of Females and Males with Abnormal 24-h ph Tests LES Pressure Total LES Length Prevalence of Prevalence of a (mmhg) (cm) Defective LES (%) Hiatal Hernia (%) Females without BE 6.4 ( ) 2.2 ( ) n = 115 Females with BE 4.1 ( ) 1.8 ( ) n = 50 Males without BE # 6.8 ( ) 2.2 ( ) n = 205 Males with BE 4.0 ( ) 1.8 ( ) n = 136 Values are medians (interquartile range), or frequency. p-values significant for all comparisons between females without BE and females with BE except for prevalence of a hiatal hernia (LES pressure p = 0.001; LES length p = 0.03; prevalence of a defective LES p = 0.04; prevalence of a hiatal hernia p = 0.11). # p-values significant for all comparisons between males without BE and males with BE except for prevalence of a hiatal hernia (LES pressure p < 0.001; LES length p = 0.006; prevalence of a defective LES p < ; prevalence of a hiatal hernia p = 0.74). # p-values not significant for all comparisons between females and males without BE except for the prevalence of a defective LES (LES pressure p = 0.79; LES length p = 0.39; prevalence of a defective LES p = 0.03; prevalence of a hiatal hernia p = 0.85). p-values not significant for all comparisons between females and males with BE (LES pressure p = 0.41; LES length p = 0.84; prevalence of a defective LES p = 0.29; prevalence of a hiatal hernia p = 0.20).

6 Comparative Analysis of Risk Factors of Barrett s Esophagus 565 females on average have less severe reflux disease than males. To answer this question we reviewed the records of 796 patients with reflux symptoms. We were unable to reliably assess the prevalence of esophagitis in our patients since most were taking proton pump inhibitors on a regular basis at the time they presented for evaluation. However, physiologic evaluation demonstrated that compared to males, females with reflux symptoms were significantly less likely to have an abnormal 24-h ph test, a defective LES, or a hiatal hernia. Since these abnormalities correlate with the severity of reflux disease, we conclude that females, despite the presence of reflux symptoms, have less severe reflux disease on average than males. Next, we looked specifically at the 506 patients with reflux disease proven by the presence of increased esophageal acid exposure on 24-h ph testing. Overall, females had less esophageal acid exposure than males, and in particular, the subgroup of females without Barrett s had significantly less esophageal acid exposure than males without Barrett s. This again suggests that reflux disease on average is less severe in females, even when comparing only patients with a positive 24-h ph test. A striking finding in this study was that in contrast to the differences between females and males with reflux but without Barrett s, females with Barrett s were similar to males with Barrett s in nearly all aspects. Specifically, the manometric characteristics of the LES, the prevalence and size of a hiatal hernia, and the degree of esophageal acid and bilirubin exposure were not significantly different between females and males with Barrett s. Thus, by physiologic assessment females with Barrett s had a similar severity of reflux and a similar frequency of physiologic abnormalities associated with reflux as males with Barrett s. Consequently, our data would suggest that in a patient with Barrett s the physiologic derangements are similar regardless of gender. To address the question of whether female gender rendered patients with severe reflux disease less likely to develop Barrett s we compared the prevalence of Barrett s in a subgroup of females and males with similar physiologic derangements. From the initial 796 patients who presented with reflux symptoms we selected all patients with the following combination of abnormalities: an abnormal 24-h ph test, an abnormal Bilitec test, a defective LES, and a hiatal hernia. This group would be expected to have severe reflux disease, and indeed 54% of the 98 patients who met these criteria had Barrett s esophagus. We found that within this subset of patients the prevalence of Barrett s was similar in females and males (52% of females and 55% of males), indicating that severe reflux produced Barrett s in a more than one-half of these patients regardless of gender. Importantly, there was no evidence of a protective effect or factor against Barrett s in females. However, why approximately one-half of the patients with severe reflux disease did not have Barrett s remains an important and unanswered question, and future investigations should perhaps focus on these patients. Lastly, we used multivariable analysis to determine which factors were independently associated with the presence of Barrett s in patients with 24-h ph proven reflux disease. The only significant factor associated with the presence of Barrett s in patients with reflux disease was abnormal esophageal exposure to bilirubin as determined by the Bilitec test. The likelihood of finding Barrett s was increased 11-fold in females and 5-fold in males with increased bilirubin reflux. This finding confirms what we previously reported in a largely male group of patients with reflux (7). This does not imply that acid is not important. Indeed, we defined reflux disease by the presence of increased esophageal exposure to acid. Thus all patients included in the multivariable analysis had abnormal esophageal acid exposure, but what separated those with reflux without Barrett s from those with reflux and Barrett s was abnormal esophageal bilirubin exposure. In fact, 95% of females and 82% of males with Barrett s had an abnormal Bilitec study, indicating a high prevalence of duodenogastro-esophageal reflux in patients with Barrett s. This finding is in line with the developing concept that while increased esophageal acid exposure defines reflux disease and leads to columnarization of the distal esophagus, alkaline or duodenogastric juice may be more important in the development of intestinalization (7, 9, 24 26). The findings in this study have several important clinical implications. First, females with significant reflux are at risk for Barrett s, and endoscopy should not be omitted in the evaluation of these patients. Further, although females with Barrett s tended to be older than males with Barrett s, the youngest female with Barrett s in our study was 22 yr old. Consequently, age, like gender, cannot be used to reliably exclude the potential for Barrett s to be present in a patient with reflux. Lastly, females and males with Barrett s have been shown to have a similar risk of cancer (23). Therefore, similar to males, females with reflux are at risk for Barrett s, and females with Barrett s are at risk for esophageal adnenocarcinoma. Although to date this is the largest study that includes extensive physiologic evaluation of patients with reflux symptoms (esophageal manometry in 98% and 24-h ph monitoring in 97% of patients), we recognize that there are limitations in our study. First, only about one-half of the patients underwent Bilitec monitoring. Bilitec testing was not available throughout the entire timeframe of this study, and some patients were unwilling to undergo the test. While 43% of all patients is a high percentage to have Bilitec testing compared to most retrospective clinical series, ideally all patients would have had all the tests. This is of course unrealistic in clinical practice. However, we cannot exclude the possibility that a bias existed in the selection of patients to undergo Bilitec testing. We believe though that our findings are valid since a similar percentage of females (49%) and males (46%) had Bilitec monitoring, more patients without Barrett s had Bilitec monitoring than did patients with Barrett s, and overall less than one-half of the patients studied by Bilitec were found to have abnormal bilirubin exposure in the esophagus. Another limiting factor is that patients referred to our center all had reflux symptoms considered significant enough

7 566 Banki et al. to warrant thorough evaluation and potentially antireflux surgery. The severity of reflux is reflected by the 26% overall prevalence of Barrett s in our patient population. While the overall severity of reflux disease in our patients represents a potential limitation of this study, it also provides an excellent opportunity to determine the factors associated with Barrett s, since reflux disease is a prerequisite for Barrett s esophagus. The frequency of Barrett s in our population is probably higher than would be expected in a general medical practice, but we found that Barrett s was more prevalent in males, and our male/female ratio of 2.7/1 is similar to what others report (14). This would suggest that although the severity of reflux disease may be skewed in our population, the demographics are probably not. Further, the finding by Gerson et al. that 25% of asymptomatic veterans have Barrett s demonstrates that the true prevalence of this disease in the general population is poorly understood (27). In conclusion, we found that symptomatic females tend to have less severe reflux by physiologic testing than symptomatic males. Even among patients with an abnormal 24-h ph test but without Barrett s females on average had less esophageal acid exposure. However, regardless of gender patients with Barrett s had severe reflux disease. In both females and males with reflux, the only significant risk factor for the presence of Barrett s esophagus was increased bilirubin exposure in the esophagus, indicating abnormal alkaline reflux. Importantly, we found no evidence of a protective factor in females against Barrett s. Rather, given a similar severity of reflux disease males and females were equally likely to have Barrett s esophagus. Consequently, the reason fewer females have Barrett s is that on average females have less severe reflux than males. Reprint requests and correspondence: Steven R. DeMeester, M.D., Associate Professor of Cardiothoracic Surgery, The University of Southern California, 1510 San Pablo St., Suite 514, Los Angeles, CA Received June 12, 2004; accepted September 24, REFERENCES 1. Winters CJ, Spurling TJ, Chobanian SJ, et al. Barrett s esophagus. A prevalent, occult complication of gastroesophageal reflux disease. Gastroenterology 1987;92(1): Eisen GM, Sandler RS, Murray S, et al. The relationship between gastroesophageal reflux disease and its complications with Barrett s esophagus. (See comments). Am J Gastroenterol 1997;92(1): Lieberman DA, Oehlke M, Helfand M. Risk factors for Barrett s esophagus in community-based practice. GORGE consortium. Gastroenterology Outcomes Research Group in Endoscopy. Am J Gastroenterol 1997;92(8): Loughney T, Maydonovitch CL, Wong RK. Esophageal manometry and ambulatory 24-hour ph monitoring in patients with short and long segment Barrett s esophagus. Am J Gastroenterol 1998;93(6): Oberg S, DeMeester TR, Peters JH, et al. The extent of Barrett s esophagus depends on the status of the lower esophageal sphincter and the degree of esophageal acid exposure. J Thorac Cardiovasc Surg 1999;117(3): Cameron AJ. Barrett s esophagus: Prevalence and size of hiatal hernia. Am J Gastroenterol 1999;94(8): Campos GM, DeMeester SR, Peters JH, et al. Predictive factors of Barrett esophagus: Multivariate analysis of 502 patients with gastroesophageal reflux disease. Arch Surg 2001;136(11): Menges M, Muller M, Zeitz M. Increased acid and bile reflux in Barrett s esophagus compared to reflux esophagitis, and effect of proton pump inhibitor therapy. Am J Gastroenterol 2001;96(2): Kaur BS, Ouatu-Lascar R, Omary MB, et al. Bile salts induce or blunt cell proliferation in Barrett s esophagus in an acid-dependent fashion. Am J Physiol Gastrointest Liver Physiol 2000;278(6):G Martinez de Haro L, Ortiz A, Parrilla P, et al. Intestinal metaplasia in patients with columnar lined esophagus is associated with high levels of duodenogastroesophageal reflux. Ann Surg 2001;233(1): Cameron AJ, Lomboy CT. Barrett s esophagus: Age, prevalence, and extent of columnar epithelium. (See comments). Gastroenterology 1992;103(4): Bremner CG, DeMeester T, Bremner R, et al. Esophageal motility testing made easy. St Louis, MO: Quality Medical Publishing, Kauer WK, Burdiles P, Ireland AP, et al. Does duodenal juice reflux into the esophagus of patients with complicated GERD? Evaluation of a fiberoptic sensor for bilirubin. (See comments). Am J Surg 1995;169(1):98 103; discussion Hirota WK, Loughney TM, Lazas DJ, et al. Specialized intestinal metaplasia, dysplasia, and cancer of the esophagus and esophagogastric junction: Prevalence and clinical data. Gastroenterology 1999;116(2): Gerson LB, Edson R, Lavori PW, et al. Use of a simple symptom questionnaire to predict Barrett s esophagus in patients with symptoms of gastroesophageal reflux. Am J Gastroenterol 2001;96(7): Conio M, Cameron AJ, Romero Y, et al. Secular trends in the epidemiology and outcome of Barrett s oesophagus in Olmsted County, Minnesota. Gut 2001;48(3): Conio M, Filiberti R, Blanchi S, et al. Risk factors for Barrett s esophagus: A case-control study. Int J Cancer 2002;97(2): Rex D, Cummings O, Shaw M, et al. Screening for Barrett s esophagus in colonscopy patients with and without heartburn. Gastroenterology 2003;125: Kennedy TM, Jones RH, Hungin AP, et al. Irritable bowel syndrome, gastro-oesophageal reflux, and bronchial hyper-responsiveness in the general population. Gut 1998;43(6): Mantynen T, Farkkila M, Kunnamo I, et al. The impact of upper GI endoscopy referral volume on the diagnosis of gastroesophageal reflux disease and its complications: A 1- year cross-sectional study in a referral area with 260,000 inhabitants. Am J Gastroenterol 2002;97(10): Jacobson BC, Ferris TG, Shea TL, et al. Who is using chronic acid suppression therapy and why? Am J Gastroenterol 2003;98(1): Avidan B, Sonnenberg A, Schnell TG, et al. Risk factors for erosive reflux esophagitis: A case-control study. Am J Gastroenterol 2001;96(1): Solaymani-Dodaran M, Logan R, West J, et al. Risk of oesophageal cancer in Barrett s oesophagus and gastrooesophageal reflux. Gut 2004;53:

8 Comparative Analysis of Risk Factors of Barrett s Esophagus Csendes A, Maluenda F, Braghetto I, et al. Location of the lower oesophageal sphincter and the squamous columnar mucosal junction in 109 healthy controls and 778 patients with different degrees of endoscopic oesophagitis. Gut 1993;34(1): Kauer WK, Peters JH, DeMeester TR, et al. Mixed reflux of gastric and duodenal juices is more harmful to the esophagus than gastric juice alone. The need for surgical therapy reemphasized. (See comments). Ann Surg 1995;222(4):525 31; discussion Fitzgerald RC, Omary MB, Triadafilopoulos G. Dynamic effects of acid on Barrett s esophagus. An ex vivo proliferation and differentiation model. J Clin Invest 1996;98(9): Gerson LB, Shetler K, Triadafilopoulos G. Prevalence of Barrett s esophagus in asymptomatic individuals. (comment). Gastroenterology 2002;123(2):461 7.

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