American Journal of Gastroenterology
C ?2005 by Am. Coll. of Gastroenterology
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: 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.
METHODS: 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.
RESULTS: 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.
CONCLUSIONS: 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
(Am J Gastroenterol 2005;100:560–567)
Barrett’s esophagus is defined by the presence of intestinal
related 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 at-
tention has focused on the role of alkaline or mixed gastro-
duodenal reflux in the pathogenesis of Barrett’s esophagus
Interestingly, while none of the above factors are specif-
ically gender related, the male gender is also a risk factor
for Barrett’s (7, 11). In most series, the ratio of males to fe-
males 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, 2001.
have been largely unexplored. One hypothesis is that the fe-
male 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 fac-
tors 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
For this study, we retrospectively reviewed the charts of
796 consecutive patients (462 males, 334 females) who pre-
sented to the Division of Thoracic and Foregut Surgery at
USC between 1990 and 2000 for evaluation of heartburn,
Comparative Analysis of Risk Factors of Barrett’s Esophagus 561
regurgitation, dysphagia, or a combination of reflux symp-
toms. Information about the nature and duration of the pa-
tients 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 recollec-
tion. This study was approved by the IRB of the University
of Southern California.
Barrett’s esophagus was defined as any endoscopically visi-
inition 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 nonintesti-
rett’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 (Microva-
sive®radial jaw 31263-20 or 1597-20). The GEJ was defined
as the location where, with the stomach decompressed, the
proximal extent of the gastric rugal folds joined the tubu-
lar esophagus. The location of the GEJ, the squamocolum-
nar 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.
water perfused catheter using a standard station pull-through
sphincter (LES) was classified as manometrically defective
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 be-
fore testing (2 wk for proton pump inhibitors, 2 days for
H2blockers). 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 < 4 greater than 4.4%.
Ambulatory Esophageal Bilirubin Monitoring Technique
and antacid medications were discontinued 48 h before test-
ing, 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 soft-
ware 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 pe-
Biopsy specimens were fixed in 10% formaldehyde, embed-
ded in paraffin, sectioned, mounted on slides, and stained
with hematoxylin and eosin using standard techniques. A
single expert GI pathologist interpreted all slides. Special-
ized 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.
Data are reported as median and interquartile range unless
otherwise specified. Fisher’s exact test was used for categor-
ical data while continuous variables were analyzed using the
ence of Barrett’s esophagus in patients proven to have reflux
disease on the basis of an abnormal 24-h pH test were as-
sessed 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
a defective LES, and bilirubin exposure. Significant factors
were then entered into a multivariable model as independent
parameters. Forward stepwise logistic regression was per-
formed 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% con-
fidence limits (CL) and p-values from the adjusted Wald’s
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).
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
562Banki et al.
Table 1. Characteristics of the Study Population
Number of patients with 24-h pH monitoring
Abnormal 24-h pH
Number of patients with manometry
Patients with defective LES
Number of patients with Bilitec probe
Abnormal Bilitec probe
Prevalence of hiatal hernia
Prevalence of H. pylori#
Prevalence of Barrett’s
796 334 (42%)
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 re-
flux symptoms during the same time period. Barrett’s esoph-
agus was present in 26% of the entire group, and was sig-
nificantly more prevalent in males. From the 796 patients
evaluated for reflux 263 patients were found to have nor-
mal 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,
Table 2. Characteristics of the Population with Abnormal 24-h pH Test
Total % time pH < 4
Total % time bilirubin
Prevalence hiatal hernia#
Prevalence defective LES
Length of BE (cm)
<3cm; n =
≥3cm; n =
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.
506 165 (33%)
Barrett’s was more common in males while short-segment
increased esophageal acid exposure but without Barrett’s, fe-
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
ably 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
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.
564 Banki et al.
Table 3. Prevalence of an Abnormal Bilitec Test in 24-h pH
Females (n = 45)
Males (n = 96)
marginally significant. The youngest female with Barrett’s
was 22 yr, while the youngest male was 20 yr old. Physi-
ologic 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
ence of hiatal hernia, number of reflux episodes, number
of reflux episodes lasting greater than 5 min, longest reflux
exposure as potentially predictive factors for the presence of
were not significant factors. Multivariable analysis demon-
strated 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 expo-
sure. 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 2.3–53, p =
0.006 for females; 1.7–9.8, p < 0.001 for males).
Prevalence of Barrett’s in Patients with Multiple
Physiologic Abnormalities Suggesting Severe
Within the population of 796 patients who underwent eval-
uation for reflux symptoms, 98 patients (33 females and
Table 4. Physiologic Characteristics of Females and Males with Abnormal 24-h pH Tests
Total LES Length
Defective LES (%)
Prevalence of a
Hiatal Hernia (%)
Females without BE∗
n = 115
Females with BE‡
n = 50
Males without BE#
n = 205
Males with BE†
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 < 0.0001; 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).
6.4 (4.0–10.2)2.2 (1.8–3.1)7682
4.1 (1.6–8.4) 1.8 (0.8–3.2)90 93
6.8 (3.4–12.3)2.2 (1.4–3.2)63 84
4.0 (2.0–5.8) 1.8 (1.2–2.6)9185
65 males) had physiologic evidence of severe gastroe-
sophageal reflux disease based on the presence of all of the
increased esophageal acid and bilirubin exposure based on
24-h pH and Bilitec testing. In this subgroup of patients the
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).
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 up-
females compared to 8.2% of males (p = 0.04 by χ2). 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 symp-
Further, in a recent analysis of 4,684 people taking chronic
In contrast to the similar prevalence of reflux symptoms
and use of acid-suppression medication, complications from
reflux disease including esophagitis, Barrett’s, and adenocar-
cinoma of the esophagus are known to occur less commonly
factor associated with the female sex protects against re-
flux complications, or that despite the presence of symptoms
Comparative Analysis of Risk Factors of Barrett’s Esophagus 565
To answer this question we reviewed the records of 796 pa-
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 evalua-
tion demonstrated that compared to males, females with re-
mal 24-h pH test, a defective LES, or a hiatal hernia. Since
these abnormalities correlate with the severity of reflux dis-
symptoms, have less severe reflux disease on average than
males. Next, we looked specifically at the 506 patients with
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 with-
out Barrett’s, females with Barrett’s were similar to males
with Barrett’s in nearly all aspects. Specifically, the mano-
metric characteristics of the LES, the prevalence and size of
a hiatal hernia, and the degree of esophageal acid and biliru-
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.
patients with severe reflux disease less likely to develop Bar-
rett’s we compared the prevalence of Barrett’s in a subgroup
toms 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
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. How-
ever, 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 Bar-
exposure to bilirubin as determined by the Bilitec test. The
likelihood of finding Barrett’s was increased 11-fold in fe-
males and 5-fold in males with increased bilirubin reflux.
male group of patients with reflux (7). This does not imply
the presence of increased esophageal exposure to acid. Thus
all patients included in the multivariable analysis had abnor-
mal 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 abnor-
mal Bilitec study, indicating a high prevalence of duodeno-
gastro-esophageal reflux in patients with Barrett’s. This find-
esophageal acid exposure defines reflux disease and leads to
gastric 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 ex-
clude 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, simi-
lar to males, females with reflux are at risk for Barrett’s, and
females with Barrett’s are at risk for esophageal adnenocar-
Although to date this is the largest study that includes ex-
tensive physiologic evaluation of patients with reflux symp-
in 97% of patients), we recognize that there are limitations in
Bilitec monitoring. Bilitec testing was not available through-
unwilling to undergo the test. While 43% of all patients is a
high percentage to have Bilitec testing compared to most ret-
rospective 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 ex-
isted 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 mon-
itoring 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 cen-
ter all had reflux symptoms considered significant enough
566Banki 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 ex-
cellent 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 medi-
cal 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 Bar-
rett’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 symp-
tomatic 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 pa-
and males with reflux, the only significant risk factor for the
presence of Barrett’s esophagus was increased bilirubin ex-
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 Univer-
sity of Southern California, 1510 San Pablo St., Suite 514, Los
Angeles, CA 90033.
Received June 12, 2004; accepted September 24, 2004.
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