Dig Dis Sci (2009) 54:321–327
DOI 10.1007/s10620-008-0352-5
ORIGINAL ARTICLE
Influence of Psychological Distress on Characteristics
of Symptoms in Patients with GERD: The Role of IBS
Comorbidity
Enrique Rey Æ Mónica Garcı́a-Alonso Æ Marta Moreno-Ortega Æ
Cristina Almansa Æ Angel Alvarez-Sanchez Æ Manuel Dı́az-Rubio
Received: 31 March 2008 / Accepted: 15 May 2008 / Published online: 23 July 2008
Ó Springer Science+Business Media, LLC 2008
Abstract A link between gastroesophageal reflux disease
(GERD) and psychological distress has been suggested;
psychological factors may modulate the characteristics of
symptoms. Besides, irritable bowel syndrome (IBS) fre-
quently coexists with GERD so it may be hypothesized that
psychological distress in GERD might be an epiphenomenon
of IBS comorbidity. Aims Evaluate the association of
psychological distress with GERD, the influence of psy-
chological factors on symptoms, whether psychological
distress is explained by a subset of GER patients, and if
coexistence with IBS would be a surrogate marker. Methods
We performed a prospective case–control study. Cases were
patients diagnosed with GERD reporting heartburn at least
2 days per week as the main complaint. Controls were
matched healthy subjects without or occasional symptoms.
All individuals completed a set of validated questionnaires
to evaluate GERD and IBS symptoms and psychological
distress (SCL-90R). Results Ninety-two patients and 92
controls were included. Fifty-seven patients and six controls
fulfilled Rome II criteria for IBS. Body mass index (BMI),
somatization, and IBS were independently related to GERD.
Patients with and without IBS were not different in any
measure of psychological distress. Characteristics of symp-
toms did not correlate to psychological measures. Cluster
analysis isolated a cluster of nondistressed from distressed
subjects. A higher proportion of GERD patients than controls
E. Rey
M. Garcı́a-Alonso
M. Moreno-Ortega
C. Almansa

A. Alvarez-Sanchez
M. Dı́az-Rubio
Division of Digestive Diseases, Hospital Clı́nico San Carlos,
Complutense University, Madrid, Spain
E. Rey (&)
Servicio de Aparato Digestivo, Hospital Clı́nico San Carlos,
c/Martin Lagos s/n, Madrid 28040, Spain
e-mail: erey.hcsc@salud.madrid.org
were classified as distressed (29.7% versus 7.7%). No vari-
able (including IBS) distinguished nondistressed from
distressed GERD patients, except for sex. Conclusions
Nearly one-third of GERD patients attending a gastroenter-
ologist office are psychological distressed; they cannot be
identified by features of symptoms or IBS comorbidity so a
specific anamnesis under the scope of a biopsychosocial
model is warranted.
Keywords Gastroesophageal reflux disease

Comorbidities
Irritable bowel syndrome

Psychological distress
Gastroesophageal reflux symptoms are frequent in Western
societies, with a prevalence ranging from 9% to 60% [1].
Somatization has been identified as a risk factor for suf-
fering gastroesophageal reflux disease (GERD) in the
general population [2, 3], and subjects with GERD showed
higher scores of anxiety and depression than subjects
without GERD in population-based studies [4, 5]. More-
over, community subjects recognized stress as one of the
leading aggravating factors of GERD symptoms [6, 7].
Despite epidemiological evidence of the potential rele-
vance of psychological factors in GERD, few studies have
focused on this relationship in clinical samples. Baker et al.
showed that GERD patients scored higher than controls
on scales of somatization, depression, and anxiety [8],
although data from Johnston et al. suggested that psycho-
logical factors were related to consultation behavior [9]. A
recent study in a sample of 4,600 consecutive patients
undergoing upper endoscopy has shown that psychological
distress and neuroticism is related to suffering GERD
symptoms [10]. However, it is unknown whether psycho-
logical factors modulate the characteristics of typical
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GERD symptoms (frequency, severity, nocturnal appear-
ance) or if they are related with suffering atypical
symptoms. Only Naliboff et al. have reported a relation-
ship between mood variables and the impact on quality of
life of GERD symptoms [11].
It has been suggested that the greater psychological
distress observed in GERD patients as a group is really
only due to a subset of patients [8], although this sugges-
tion has not been subsequently confirmed or rejected.
Among patients with GERD, 30–70% have been found to
suffer from irritable bowel syndrome (IBS) [12], which in
turn is known to be associated with psychological distress
[13, 14]. Moreover, somatization was shown to be a risk
factor for the association of IBS with GERD in a popula-
tion-based study [15]. Thus, it may be hypothesized that
psychological distress observed in GERD patients would
be an epiphenomenon of IBS comorbidity.
Therefore, we conducted a study to evaluate (1) the
association of psychological distress with GERD in a
Spanish clinical sample; (2) the influence of psychological
factors on frequency and severity of symptoms; (3) whether
psychological distress is suffered mainly by a subset of
GERD patients; and (4) whether suffering IBS symptoms
might identify the subgroup of GERD patients that are
psychologically distressed.
Material and Methods
Design and Participants
To achieve the objectives, we undertook a prospective case–
control study. Cases were defined as consecutive patients
referred to gastroenterologists because of typical GERD
symptoms (heartburn and/or regurgitation) at least 2 days
per week. Controls were subjects from the general popula-
tion who did not suffer symptoms of GERD or experienced
them less than weekly. Cases and controls were matched by
age (±5 years) and sex. Controls were not recruited among
patients or relatives attending medical facilities.
Instruments
All subjects completed a set of questionnaires to evaluate
symptoms of GERD, psychological distress, and quality of
life.
Symptoms of GERD and demographic variables were
evaluated with the GastroEsophageal Reflux Questionnaire
[16], an instrument validated for use in the Spanish popula-
tion [17]. In addition, all subjects completed a questionnaire
designed ad hoc to detail the characteristics of typical
symptoms of GERD. Frequency was evaluated as the num-
ber of days a week with heartburn and/or acid regurgitation;
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Dig Dis Sci (2009) 54:321–327
severity was evaluated through a 100 mm visual analogue
scale (VAS), anchored at the ends with the labels ‘‘nothing at
all’’ and ‘‘maximum imaginable’’. Two additional similar
VAS scales were included to evaluate the impact of GERD
symptoms on working activities and recreational activities.
Also, several atypical GERD symptoms (chest pain, hiccups,
belching, throat clearing, hoarseness, coughing, asthmatic
crisis) were evaluated by asking the subjects to report their
presence, frequency (days per week), and severity on seven-
point Likert scales from ‘‘nothing at all’’ to ‘‘unbearable’’ for
each symptom.
To evaluate IBS symptoms, all subjects completed a
clinical questionnaire, including questions about bowel
symptoms and related medical resource utilization. This
questionnaire has been successfully used in a population-
based IBS study [18] and enables Rome II criteria, as well
as previous diagnosis of IBS, to be verified.
Psychological factors were evaluated using state-trait
anxiety inventory (STAI) and SCL-90R inventories. STAI
is a widely used questionnaire with a validated Spanish
version. It is a 40-item self-report measure designed to
assess anxiety. Subjects indicate how they generally feel
(trait anxiety) by rating the frequency and intensity of their
feelings of anxiety on a four-point scale ranging from 1
(almost never) to 4 (almost always), and how they feel
right now (state anxiety), by rating the frequency and
intensity of their feelings of anxiety on a four-point scale
ranging from 1 (nothing) to 4 (a lot).
The symptom check list 90 (SCL-90R) is a widely used
measure of psychological distress with a validated Spanish
version. Subjects answer on a five-point scale how much
certain problems have bothered them over the past 7 days.
It allows nine scales and three global indexes. We evalu-
ated the somatization and depression scales and the three
global indexes (global symptom index, GSI; positive
symptoms total, PST; and positive symptom distress index,
PSDI). Raw scores were transformed to T-scores based on
the normative sample of Spanish nonpatient males and
females.
Statistical Analysis
We performed univariate comparisons (ANOVA) of psy-
chological variables (trait and state anxiety, T-scores of
somatization, depression, GSI, PST, and PSDI) between
cases and controls, with further stratification by IBS
symptoms. A logistic regression model was constructed to
predict suffering from GERD including psychological
factors and suffering from IBS as factors, adjusting for
potential confounders (age, sex, body mass index, smoking,
alcohol use, and family history of GERD).
Association of features of symptoms and psychological
factors was evaluated by Pearson’s correlation.
Dig Dis Sci (2009) 54:321–327 323

Finally, a hierarchical cluster analysis (average linkage 19.6%; P \ 0.001), and epigastric pain (66.3% versus
within groups using squared Euclidean distance, variables 8.7%; P \ 0.001), but not asthmatic crisis (6.5% versus
converted to Z scores) was performed, including state and 4.3%) or hoarseness (20.7% versus 16.3%).
trait anxiety, somatization, depression, GSI, PST, and
PSDI, without considering GERD or IBS. Clusters were
Psychological Factors
characterized by the mean scores of psychological vari-
ables and the prevalence of GERD and IBS symptoms in
As shown in Table 1, GERD patients showed higher scores
them was evaluated.
than controls in all psychological measures. Stratification
Statistical analysis was performed with SPSS v14.
of groups according to suffering from IBS (Fig. 1) showed
that patients with GERD and IBS symptoms clearly and
Ethics
statistically significantly differed from controls in all
psychological measures, while GERD patients without IBS
This study was approved by the Institutional Ethical
only showed statistically significant differences from
Committee of the Hospital Clı́nico San Carlos. All subjects
controls in somatization score and PSDI.
provided written informed consent before participation.
In the logistic regression model (Table 2), body mass
index, somatization score, and suffering from IBS were
independently related to suffering from GERD.
Results

One hundred and seven patients with GERD were invited Characteristics of GER Symptoms and Psychological
to participate and 92 (86%) accepted and completed all the Measures
questionnaires. Ninety-two matched controls were recrui-
ted and completed the study. Both groups included 58 Frequency and severity of typical GER symptoms did not
females and 34 males, with similar mean age (cases: correlate to any psychological measures (r \ 0.2; P [ 0.05).
40.0 ± 13.0 years; controls: 39.8 ± 13.2 years). There No differences were found in state and trait anxiety, soma-
were no differences between cases and controls regarding tization, depression, GSI, PST, or PSDI between those with
education level, civil status, working situation, and family and without nocturnal symptoms.
monthly income. Patients showed a higher body mass Frequency and severity of atypical GERD symptoms did
index than controls (25.6 ± 4.0 versus 23.0 ± 3.3 kg/m2; not correlate with any of the psychological variables
P \ 0.001; ANOVA), and a higher proportion reported measures.
family history of GERD (30.4% versus 21.7%; v2), but no
differences were found in smoking (current smokers: Cluster Analysis
48.9% versus 39.1%) or alcohol use (one drink or more per
week: 59.8% versus 60.9%). The best solution was provided by four clusters, composed
of cluster 1, which may be described as the nondistressed
GERD Symptoms group, cluster 2 as a distressed group, and two additional
clusters formed by one outlier subject each (a very high
Sixteen controls (17.4%) reported occasional GER symp- distress cluster and a very low distress cluster); these last
toms (less than weekly). Patients reported heartburn or acid two clusters were excluded from further analysis.
regurgitation a mean of 4.1 ± 1.9 days per week, with a
mean severity of 51.9 ± 24.0 on the VAS scale; 39.1%
referred nocturnal symptoms.
Table 1 Psychological measures in GERD patients and controls
Fifty-seven patients (62%) and six controls (6.5%) met
Rome II criteria for IBS (P \ 0.001; v2). Among them, 16 Controls GERD patients
GERD patients (17.4%) and one control (1.1%) had con-
State anxiety 33.9 ± 9.0 39.2 ± 13.0*
sulted because of bowel symptoms in the past and were
Trait anxiety 37.6 ± 9.4 42.8 ± 11.2*
diagnosed with IBS.
Somatization 51.3 ± 9.3 61.8 ± 8.9**
Patients with GERD reported more frequently than
Depression 48.9 ± 11.1 54.3 ± 11.6*
controls suffering from chest pain (42.4% versus 4.3%;
GSI 50.7 ± 11.6 57.7 ± 10.7**
P \ 0,001), hiccups (28.3% versus 13%; P \ 0.05),
PST 54.3 ± 12.6 60.0 ± 11.3*
belching (69.6 versus 27.2%; P \ 0.001), coughing (44.6%
PSDI 42.7 ± 8.1 49.5 ± 9.6**
versus 28.3%; P \ 0.05), throat clearing (45.7% versus
19.6%; P \ 0.001), postprandial fullness (79.3% versus * P \ 0.01; ** P \ 0.001

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324 Dig Dis Sci (2009) 54:321–327

Fig. 1 Psychological measures 80

in controls and GERD patients
Control (N=86)
stratified by suffering from IBS
* *
** *
symptoms. * P \ 0.05 versus Control with IBS (N=6)
70
controls without IBS in post hoc GERD (N=35) *
comparisons (Dunnet’s C test) GERD with IBS (N=57)
60 **
*
*
50

40

30

20

10

0
State Anxiety Trait Anxiety Somatisation Depression GSI PST PSDI
(direct score) (direct score) (T-score) (T-score) (T-score) (T-score) (T-score)

Table 2 Factors associated

Factors Categories Adjusted OR P-value
with suffering from GERD in
the logistic regression model Age Continuous (years) 0.97 (0.93–1.01) NS
Sex Male 1
Female 0.77 (0.24–2.43) NS
Smoking Never 1
Current 1.43 (0.46–4.45) NS
Past 0.65 (0.17–2.55) NS
Alcohol use No or less than weekly 1
1–6 drinks weekly 1.30 (0.43–3.95) NS
7 or more drinks weekly 0.91 (0.16–5.30) NS
Relative with history No 1
Of GERD symptoms 1.27 (0.41–3.97) NS
Of other esophago-gastro-duodenal 0.78 (0.22–2.73) NS
(EGD) disease/symptoms
Body mass index Continuous (kg/m2) 1.28 (1.11–1.48) \0.001
State anxiety Continuous (direct score) 1.01 (0.95–1.07) NS
Trait anxiety Continuous (direct score) 1.04 (0.97–1.12) NS
Somatization Continuous (T score) 1.13 (1.04–1.24) \0.01
Depression Continuous (T score) 1.05 (0.93–1.18) NS
GSI Continuous (T score) 0.91 (0.67–1.23) NS
PST Continuous (T score) 0.98 (0.77–1.24) NS
Hosmer and Lemeshow PSDI Continuous (T score) 1.04 (0.92–1.18) NS
goodness-of-fit P = 0.88; IBS criteria No 1
Nagelkerke’s R2 = 0.65; Yes 32.40 (9.28–113.10) \0.001
OR, odds ratio

Among 91 GERD patients, 27 (29.7%) were classified higher proportion of females, distinguished nondistressed
into cluster 2 (distressed) compared with only 7 (7.7%) of GERD patients from distressed GERD patients, including
91 controls (P \ 0.001; v2). No variable, except for a suffering from IBS, as shown in Table 3.

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Dig Dis Sci (2009) 54:321–327 325

Table 3 Comparison of
Cluster 1: Cluster 2:
nondistressed and distressed
nondistressed distressed
GERD patients
GERD GERD
(N = 64) (N = 27)

Age (years) 40.2 ± 12.9 39.8 ± 13.4

Females (%) 54.7% 85.2%*
BMI (kg/m2) 25.5 ± 3.9 25.8 ± 4.4
Smoking Current 46.9% 51.9%
Past 18.7% 14.8%
Alcohol Fewer than one drink daily 51.6% 45.8%
One or more drinks daily 11.3% 4.2%
Family history Of GERD 32.8% 22.2%
Of other EGD symptoms/diseases 20.3% 22.2%
IBS 59.4% 70.4%
Diagnosis of IBS 12.5% 29.6%
Heartburn or acid Frequency (days weekly) 4.1 ± 2.0 4.1 ± 1.8
regurgitation Severity (VAS) 49.7 ± 25.4 58.1 ± 19.7
Interference with work (VAS) 25.1 ± 26.0 29.6 ± 19.6
Interference with social activities 31.8 ± 27.3 35.6 ± 25.3
(VAS)
Nocturnal appearance 40.6% 33.3%
Chest pain Prevalence 39.5% 51.9%
Frequency 2.8 ± 2.5 2.6 ± 2.0
Severity 3.7 ± 1.5 4.3 ± 1.3
Hiccups Prevalence 25% 37%
Frequency 2.1 ± 1.5 1.3 ± 0.5
Severity 3.2 ± 1.8 2.0 ± 0.9
Belching Prevalence 67.2% 77.8%
Frequency 5.0 ± 2.2 5.1 ± 2.1
Severity 3.7 ± 1.7 3.5 ± 1.7
Coughing Prevalence 42.2% 51.9%
Frequency 4.5 ± 2.3 5.1 ± 2.1
Severity 3.7 ± 1.8 3.7 ± 1.8
Throat clearing Prevalence 45.3% 48.1%
Frequency 4.7 ± 2.2 3.6 ± 2.4
Severity 3.6 ± 1.9 3.7 ± 1.8
Asthmatic crisis Prevalence 7.8% 3.7%
Frequency 3.9 ± 3.4 2
Severity 4.8 ± 1.9 3
Hoarseness Prevalence 18.8% 25.9%
Frequency 3.1 ± 2.5 1.6 ± 1.3
Severity 3.2 ± 1.9 4.1 ± 1.3
* P \ 0.01

Discussion
Our study showed a higher prevalence of psychological
distress in patients compared with controls, mainly driven by
a subgroup of patients which represented one-third of those
with GERD with typical symptoms as the main complaint.
However, we cannot trust in the characteristics of symptoms
or IBS comorbidity to identify them in clinical practice.
Clinical studies in the USA [8] and Asia [10] have
previously shown that patients with GERD report high
scores of psychological distress; our results in a Spanish
population agree with them in spite of obvious cultural
differences between samples. Moreover our study repro-
duces in the clinical setting what has been found in
population-based studies: GERD patients showed higher
scores on anxiety and depression than controls [4, 5], and

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somatization score was specifically found to be an inde-
pendent risk factor for GERD [2, 3]. These pieces of
information strengthen the relevance of psychological
distress in GERD.
It may be argued that we cannot evaluate to what extent
psychological distress is related to seeking consultation, as
suggested by Johnston et al. [9], since we did not include
subjects with frequent GERD symptoms who did not
consult. However, a former study by our group did not find
a link between somatization and medical consultation by
GERD symptoms in a Spanish population [19].
Some studies have reported that stress and anxiety may
modulate the reporting of GERD symptoms according to
experimental data [20, 21], but it its relevance in the usual
clinical situation is unknown. Our data suggest that the
frequency, severity, and nocturnal appearance of typical
GER symptoms are not related to any psychological vari-
able. Although a type II error cannot be excluded for
heartburn severity, interference with activities, or nocturnal
occurrence, differences are quantitatively small and not
clinically relevant.
We did not classify our GERD patients according to
endoscopy or pHmetry so we cannot infer any information
in specific subgroups. However, esophagitis has not been
associated to anxiety or depression compared to non ero-
sive reflux disease (NERD) [10] and there is conflicting
data regarding differences between functional heartburn
and NERD patients [22, 23].
Cluster analysis shows that psychological distress is
present in one-third of patients with GERD, up to four
times more often than in controls. This fully agrees with
the results of Baker et al. [8] though in a culturally and
genetically different population including both males and
females patients. Thus, it seems clear that psychological
distress in GERD patients as a group is mostly due to a
subgroup of patients, accounting for around 30% of those
consulting a gastroenterologist.
The identification of this subgroup in clinical practice
may be important since psychological factors are predictors
of an incomplete response to proton pump inhibitor (PPI)
treatment [24]. Although patients with psychological dis-
tress showed slightly higher severity of heartburn, higher
impact of symptoms on activities, and higher prevalence of
chest pain, hiccups or coughing, none of these differences
reached statistical significance compared with nondi-
stressed patients, except for a higher proportion of females.
In the general population, association of IBS and GERD
occurs more often than by chance [15], and IBS is a risk
factor for suffering GERD [25]; the reasons for this asso-
ciation are unclear but recently psychological factors have
been found as a risk factor for suffering IBS among GERD
patients [15]. In clinical series, IBS symptoms are reported
by 30–70% of GERD patients [12]. We also found a high
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Dig Dis Sci (2009) 54:321–327
prevalence of IBS symptoms according to Rome II criteria
in GERD patients attending a gastroenterologist office. In
fact, IBS was a risk factor for GERD but, interestingly,
somatization and IBS were independent risk factors in
multivariate analysis; this suggest that both factors may act
by different pathways in GERD; moreover, although it is
true that GERD patients with IBS score slightly higher than
GERD patients without IBS and that the prevalence of IBS
is slightly higher in psychologically distressed GERD
patients, these differences did not reach statistically sig-
nificance. Thus, our data suggest that, in clinical settings,
the identification of IBS symptoms in patients with GERD
cannot be used as a clinical marker of psychological
distress.
It should be noted that our results are applicable
exclusively to those GERD patients with typical symptoms,
more severe disease or more difficult management, referred
from a general practitioner to a gastroenterologist.
Although IBS was not found to be an independent risk
factor for consultation among GERD patients in the general
population [26], it may still be a factor for referral to a
gastroenterologist.
In summary, our study shows that one-third of GERD
patients with typical symptoms as the main complaint
attending a gastroenterologist office are psychological
distressed; they cannot be identified by features of symp-
toms or IBS comorbidity so a specific anamnesis under the
scope of a biopsychosocial model is warranted.
Acknowledgments This study was supported by an unrestricted
grant from the Mutua Madrileña Foundation
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