Martinucci et al. BMC Gastroenterology (2018) 18:116
RESEARCH ARTICLE Open Access
Gastroesophageal reflux symptoms
among Italian university students:
epidemiology and dietary correlates using
automatically recorded transactions
Irene Martinucci1* , Michela Natilli2,1, Valentina Lorenzoni4, Luca Pappalardo5,2 , Anna Monreale2,
Giuseppe Turchetti4, Dino Pedreschi2, Santino Marchi6, Roberto Barale3and Nicola de Bortoli6
Background: Gastroesophageal reflux disease (GERD) is one of the most common gastrointestinal disorders
worldwide, with relevant impact on the quality of life and health care costs.The aim of our study is to assess the
prevalence of GERD based on self-reported symptoms among university students in central Italy. The secondary aim is
to evaluate lifestyle correlates, particularly eating habits, in GERD students using automatically recorded transactions
through cashiers at university canteen.
Methods: A web-survey was created and launched through an app, ad-hoc developed for an interactive exchange of
information with students, including anthropometric data and lifestyle habits. Moreover, the web-survey allowed
users a self-diagnosis of GERD through a simple questionnaire. As regard eating habits, detailed collection of meals
consumed, including number and type of dishes, were automatically recorded through cashiers at the university
canteen equipped with an automatic registration system.
Results: We collected 3012 questionnaires. A total of 792 students (26.2% of the respondents) reported typical GERD
symptoms occurring at least weekly. Female sex was more prevalent than male sex. In the set of students with GERD,
the percentage of smokers was higher, and our results showed that when BMI tends to higher values the percentage
of students with GERD tends to increase. When evaluating correlates with diet, we found, among all users, a lower
frequency of legumes choice in GERD students and, among frequent users, a lower frequency of choice of pasta and
rice in GERD students.
Discussion: The results of our study are in line with the values reported in the literature. Nowadays, GERD is a common
problem in our communities, and can potentially lead to serious medical complications; the economic burden
involved in the diagnostic and therapeutic management of the disease has a relevant impact on healthcare costs.
Conclusions: To our knowledge, this is the first study evaluating the prevalence of typical GERD–related symptoms
in a young population of University students in Italy. Considering the young age of enrolled subjects, our prevalence
rate, relatively high compared to the usual estimates, could represent a further negative factor for the future
economic sustainability of the healthcare system.
Keywords: Gastroesophageal reflux disease, GERD, Heartburn, Regurgitation, Diet, Prevalence, University students
1Division of Gastroenterology–Versilia Hospital, Lido di Camaiore–Lucca, Italy
Full list of author information is available at the end of the article
© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 2 of 10
Gastroesophageal reflux disease (GERD) is a chronic con-
dition which develops when the reflux of gastric contents
into the esophagus causes troublesome symptoms and/or
complications [1,2]. It is well known that a wide and vary-
ing range of symptoms is associated with GERD. The two
most typical symptoms are heartburn and regurgitation;
however, patients may complain also other symptoms
including chest pain, as well as extra esophageal manifes-
tations such as chronic cough, asthma, and laryngitis .
GERD is one of the most common gastrointestinal dis-
orders worldwide, with relevant impact on the quality of
life and health care costs . According to population–
based studies, when defined as at least weekly heartburn
and/or regurgitation, prevalence estimates generally range
from 10 to 30% in Western populations, and only East Asia
shows estimates consistently lower than 10% . In addi-
tion, it is worth noting that evidence suggests an increase
in disease prevalence since 1995 [4–7].
The etiology of GERD is largely unknown, and its
pathogenesis is multifactorial in nature, mainly involving
dysfunctions of the esophagogastric junction, ineffective
esophageal acid and bolus clearance, increased intra-
gastric pressure, and esophageal hypersensitivity [8,9].
Moreover, the main established risk factors of GERD are
heredity, obesity and tobacco smoking. Thus, according
to a recent systematic review and current guidelines, the
first step in GERD management consists of lifestyle inter-
ventions, such as weight loss, tobacco smoking cessation,
avoiding late evening meals and head–of–the–bed eleva-
tion [10–13]. Along the same line, dietary modifications
have also been proposed as first–line therapy for patients
with GERD . However, few and heterogeneous ran-
domized clinical trials and observational studies have
shown inconsistent or conflicting results about the puta-
tive role of specific dietary items in development of reflux
symptoms [10,15,16]. In this context, the effect of the
overall dietary pattern of a population on the risk of GERD
has been scarcely evaluated. Recently, a cross–sectional
study by Mone et al. highlighted a beneficial effect of
a Mediterranean diet in the occurrence of GERD.
Based on the above considerations, the aim of our
study is to assess the prevalence of GERD based on self–
reported symptoms among university students in central
Italy. The secondary aim is to evaluate lifestyle corre-
lates, particularly eating habits, in GERD students using
data from a web survey and transactions automatically
recorded through cashiers at university canteen.
This work is part of a larger study aiming at studying
the nutritional habits of University of Pisa students and
the relation between these habits and gastrointestinal dis-
orders. The project consists of several phases covering
innovative aspects in terms of research and application of
Design and study population
In order to evaluate the correlation between eating habits
and gastrointestinal disturbances, a web–survey was cre-
ated and launched through an app, ad hoc developed for
an interactive exchange of information with students. Par-
ticipants were recruited among students of University of
Pisa and participation to the survey was voluntary. To
ensure adequate widespread of the project among the tar-
get population, information was diffused through various
means: the web portal of University of Pisa, the email
canteen area. The students were informed that they would
have been notified on the results of their questionnaire
and that a number of dietary recommendations suitable
for any detected disorder would have been available. Stu-
dents can access the survey only through the university’s
personal credentials and all individuals who agreed to par-
ticipate gave an informed consent through the web–app.
The survey was built (in Java) on Liferay Community
Edition, a Content Management System (CMS) that can
create the succession of questions and possible answers
with images and scores.
The survey included both qualitative and quantitative
questions devoted to the collection of anthropometric
data and lifestyle habits of the student (i.e., height, weight,
smoking, coffee consumption), as well as possible gas-
Data sources and data collection
To reach the project’s goals, three different sources of
data were used and merged to obtain the database for the
i. data from the University administrative archive;
ii. data collected with a web–app that allows users a
self–diagnosis for the gastrointestinal disturbances
through a simple questionnaire;
iii. data on meals consumption provided by the regional
company that manages the University canteen.
The University archive, used to identify the overall stu-
dents enrolled in the academic year 2016–17, provides
demographic and academic career data for all students
For those students participating into the web–survey
and/or using the university canteen additional informa-
tion was added as detailed below.
The web questionnaire comprises specific sections
to investigate the presence of gastrointestinal disor-
ders, with particular reference to GERD, and a general
section devoted to the collection of demographic and
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 3 of 10
anthropometric data (weight and height), daily coffee con-
sumption and the current smoking behavior.
Since one of the main attributes involved in the study is
the Body Mass Index (BMI), we calculated it as the weight
in kilograms divided by the square of the height in meters
(kg/m2), and, accordingly with WHO definition the class
where defined as show in Table 1. Questions on how many
cups of coffee were consumed by students and a question
in which we ask whether the student is a smoker or a non-
smoker were included.
Questions related to the assessment of the GERD were
formulated on the basis of a simplified version of a val-
idated questionnaire, the GERDq questionnaire, limiting
the questions only to typical reflux symptoms. [1,18–20].
In the questionnaire, heartburn was defined as a burn-
ing sensation or pain behind the breast bone in the chest,
and regurgitation was defined as the perception of back-
flow of gastric content coming into the throat or mouth.
In particular, the frequency and the intensity of typical
GERD-related symptoms were evaluated with a Likert
scale and a visual analog scale (VAS).
The survey was launched on October 2016 and it is still
online. The data used for the present work cover a period
of 200 days, from the 21st of October 2016 to the 10th of
The “Azienda Regionale per il Diritto allo Studio Univer-
sitario” (DSU), a public corporation operating throughout
the Region in order to offer food services to students as
well as accommodation, grants or scholarships to the most
deserving ones, administered the three University can-
teens students. Thanks to the personal magnetic cards
used to access the canteen, the DSU owns a dedicated
database collecting, for each transaction (i.e. a meal),
information about date and hours, type of meal, student
ID and price applied. Number and type of dishes are
also automatically recorded for meals consumed in one
of the canteens equipped with an automatic system for
the detailed collection of meals consumed. That source of
data was used in the present analysis to extract records
about meal consumption for those students accessing the
canteen and participating into the web survey.
Table 1 The International Classification of adult underweight,
overweight and obesity according to BMI
Normal range 18.50 −24.99
Overweight 25.00 −29.99
Obesity class I 30.00 −34.99
Obesity class II 35.00 −39.99
Extreme obesity ≥40.00
A Heckman–type selection model wasusedtoassess
the presence of selection bias in the sample of students
answering the survey, to determine whether the GERD
prevalence estimated among University students could
be obtained directly from the observed data, or whether
there is need of a correction for selection bias. Sample
selection occurs when the data at hand are not a ran-
dom sample from the population of interest. To deal with
that, Heckman—type selection models have been widely
used in economics and social science to evaluate whether
the mechanism determining the participation (selection)
into a survey is independent of the presence of the out-
come of interest. The selection model typically consists
in a bivariate regression comprising a selection equation,
which describes survey participation, and an outcome
equation, predicting the outcome of interest. The two
equations are linked through a correlation parameter, ρ,
representing the covariance between the outcome and the
participation conditional on observed covariates. A statis-
tically significant value of ρimplies a relation between the
process of participation into the study and the outcome,
thus providing evidence about the presence of selection
bias and hence the need to correct estimates coming from
the observed data. A negative estimate of ρmeans that
subjects in which the outcome is present are less prone to
participate, vice versa in case of a positive value.
A bivariate probit Heckman–type selection model was
used in the present analysis. Age and gender were used as
covariates in the selection equation, while, to comply with
exclusion restriction, only gender was used as covariate in
the outcome equation.
Different statistical analysis were performed: descriptive
statistics on the data collected, a study of the GERD preva-
lence and lifestyle correlates with both a monovariate and
a multivariate approach (logistic regression). The inde-
pendent variables used in the model are: Gender (Female),
a dummy variable that is equal to 1 when the student is a
female; Smoking habit (Smoker): dummy variable that is
equal to 1 when the student is a smoker; Number of coffee,
continuous variable; BMI Underweight, dummy variable;
BMI Overweight, dummy variable; BMI Obesity1,dummy
Eating habits of students were analysed and compared
based on food items automatically recorded from cashiers’
transactions at University canteens. All food was grouped
into 12 specific groups on the basis of the main dish and
fried food, sandwiches and pizza, pies and omelette.
The frequency of different food groups consumption was
described in terms of the number of times the specific
group is selected over the total number of accesses and
reported as percentage. The latter analysis was performed
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 4 of 10
on all users and also on the subgroups of frequent users.
Frequent users were defines as those students accessing
the canteens at least 20 times in the year on the basis of the
75th percentile of the distribution of the number of yearly
Continuous variables were described in terms of median
[25 −75th percentile] and Mann-Whitney U test was
used to perform comparisons between groups. Categor-
ical variables are presented as number of subjects and
percentage and Fisher or χ2tests were used to compare
the distribution of variables between groups.
All analyses were performed using Python, STATA a nd
During the 200 days the survey was online, 3012 question-
naires were collected, about 6.3% of the students enrolled
in the University of Pisa. In Table 2the details of the
62.4% of the respondents (n=1,884) were females and
the remaining 37.6% (1,136) were males. The median age
of respondents was 23 years (with a standard deviation of
3.6 years and an interquartile range of 5 years). Table 3
shows the distribution of respondents by gender and Body
Mass Index (BMI): while the “Normal Weight” is the mode
of the distribution, we observe that males have a tendency
toward overweight, while females have a tendency toward
Table 2 Descriptive characteristics of the respondents to the
Male 1136 37.6
Female 1884 62.4
Underweight 300 9.9
Normalweight 2268 75.1
Overweight 366 12.1
Class I obesity 65 2.2
Class II obesity 15 0.5
Extreme obesity 6 0.2
Age by gender
Median 24.0 24.0
Mean 26.7 25.9
Q1 22.0 22.0
Q3 27.0 27.0
IQR 5.0 5.0
Table 3 Respondent to the web-questionnaire by gender, BMI
and coffee consumption
F M Female (%) Male (%)
Underweight 256 44 13.6 3.9
Normal weight 1422 846 75.5 74.5
Overweight 163 203 8.7 17.9
Class I obesity 33 32 1.8 2.8
Class II obesity 5 10 0.3 0.9
Extreme obesity 5 1 0.3 0.1
Number of coffee consumed∗
None 439 301 23.3 26.5
1–2 966 539 51.3 47.4
3–4 437 256 23.2 22.5
5 + 42 40 2.2 3.5
Yes 370 226 19.6 19.9
No 1514 910 80.4 80.1
*P-value <0.05 for comparison between males and females distribution of the
The original numerical variable “number of coffee” was categorized for descriptive
underweight (statistically significant differences, with P-
Regarding coffee consumption, there is a statistically
significant difference in the coffee consumption (see
Tabl e 3), with a higher number of coffees per day for
the female population (P-value=0.023). Furthermore we
observe that for both males and females almost 20% of
the students are smokers, with no statistically significant
differences among gender.
GERD prevalence and lifestyle correlates
Based on the available evidence and the bivariate probit
Heckman–type selection model specification, estimate of
ρwas not significantly different from zero (Table 4). This
means that the hypothesis of the absence of selection bias
could not be rejected, accordingly prevalence estimates
and correlates were derived directly from the observed
Tabl e 5shows the distribution of students’ character-
istics and lifestyle habits according to the presence of
GERD. 792 students out of 3020 respondents (26.2%)
reported typical GERD symptoms occurring at least
weekly. In particular, heartburn and regurgitation were
reported by 47 and 53% of the students, respectively. As
reported in Fig. 1, most reflux symptoms which were
experienced only once a week were very mild in severity,
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 5 of 10
Table 4 Estimates from the Heckman–type selection model
Coef. Std. Err. P-value 95% CI
Outcome model: Presence of GERD
Gender 0.255 0.051 <0.001 (-0.354;-0.156)
(cons) 1.302 0.448 0.004 (-2.180;-0.424)
Selection model: Survey Participation
Gender 0.222 0.018 <0.001 (-0.257;-0.187)
Age 0.012 0.002 <0.001 (-0.015;-0.009)
(cons) 0.878 0.047 <0.001 (-0.971;-0.786)
ρ0.582 0.316 (-0.263;0.922)
and the severity increases with the increase of the weekly
frequency of the symptoms.
Female students are more affected by the symptoms,
28.2% versus 22.9%, with this difference statistically signif-
Furthermore, a cross tabulation between GERD and
BMI was performed. In Table 5the distribution of the two
Since the number of students in Class II obesity and
Extreme obesity are low they were merged in one cat-
egory to have a more precise idea of this distribution.
As expected, overweight and obese were more frequent
among GERD (P-value =0.030). On the other side, in
the set of students with GERD, the percentage of smokers
is higher than the percentage of students without GERD
(P-value <0.001), and also coffee consumption play an
Table 5 Prevalence of GERD by BMI class, Smoking habits and
number of coffee consumed
No GERD GERD
Underweight 216 9.7 84 10.6
Normal weight 1694 76.0 574 72.5
Overweight 265 11.9 101 12.8
Class I obesity 42 1.9 23 2.9
Class II obesity or more 11 0.5 10 1.3
Non smoker 1827 82.0 597 75.3
Smoker 401 18.0 195 24.7
Number of coffee consumed∗
None 556 25.0 184 23.2
1–2 1131 50.8 374 47.2
3–4 483 21.7 210 26.5
5 or more 58 2.6 24 3.0
*P-value <0.05 for comparison in GERD prevalence among groups
important role in the prevalence of GERD (P-value =
Same results can be drawn looking at the odds ratios
(Table 6) of these correlates: smoking habits and over-
weight/obesity have a positive impact on the GERD preva-
lence. Being a female student also seems to be related to
GERD prevalence. These conclusions are based on uni-
variate analysis, but for having a more informative results
a multivariate logistic regression analysis was performed
on the data with the aim of explaining the relationship
between the dependent binary variable (GERD) and all
possible independent variables together.
AsshowninTable6, the variables Gender(F),
Smoker(Yes) and BMI Class Obesity (aggregation of the
3 different levels of obesity) are highly statistically sig-
nificant: smokers are more likely to experience GERD
symptoms, such as female students. The students in the
Obesity class have an odd ratio greater than one, which
means that Obesity can be considered a determinant of
GERD symptoms. The coffee consumption seems to have
a positive impact on GERD presence.
Dietary pattern in GERD
Overall, 32.5% (980) of all respondents accessed at least
once of the University canteen in the academic year
2016–17, and about 13.1% (395) were frequent users. The
prevalence of GERD among the subgroup of respondents
accessing the canteen was 25.9%, not statistically differ-
ent from the value in the overall group of respondents
(p=0.882). Characteristics and lifestyle of overall users are
reported in Additional file 1:TableS1.
When evaluating food choices, among all users a lower
frequency of legumes choice was observed in GERD stu-
dents (P-value =0.002) while, when considering frequent
users we find a significant (P-value=0.034) lower fre-
quency of choice of pasta and rice in GERD students (see
Tabl e 7).
No differences among students with and without GERD
were found also when distinguishing male and female, or
by distinguishing students by BMI category (i.e., normal
weight and overweight/obese) (see Additional file 1:Table
This is the first study evaluating the prevalence of typ-
ical GERD-related symptoms in a young population of
University students in Italy. Our data show a prevalence
rate of weekly symptoms in 26.2% of the total respon-
dents. In a previous population-based study performed in
Italy, 700 employers in Pavia answered a physician inter-
view about typical GERD-related symptoms. The results
showed a prevalence of heartburn and regurgitation of
7.7 and 6.6%, respectively . On the other hand, in
European population-based studies,the range of GERD
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 6 of 10
Fig. 1 Intensity of heartburn and regurgitation symptoms by their frequency
prevalence estimates (defined as at least weekly heartburn
and/or regurgitation) was 8.8%–25.9% . Since system-
atic reviews suggested that the prevalence of GERD is
increasing [4,5], the results of our study are in line
with the values reported in the literature. Nowadays,
GERD is a common problem in our communities, and
can potentially lead to serious medical complications (i.e.
Barrett’s esophagus, esophageal adenocarcinoma); more-
over,the economic burden involved in the diagnostic and
therapeutic management of the disease has a relevant
impact on healthcare costs. In this context, considering
the young age of enrolled subjects, our prevalence rate,
relatively high compared to the usual estimates, could rep-
resent a further negative factor for the future economic
sustainability of the healthcare system.
While to analyze GERD risk factors it was not the pri-
mary goal of this article, it is worth noting that female
sex was more prevalent than male sex. Moreover, in the
set of students with GERD the percentage of smokers
was higher. However, current evidence of associations
of GERD with sex or smoking habits are conflict-
ing and inconclusive. On the other hand, evidence
shows incontrovertibly a strong association between over-
weight/obesity and occurrence of GERD symptoms and
its complications, both analyzing data with a monovariate
approach or a multivariate approach,so that the global ris-
ing prevalence of GERD seems to be related to the rapidly
increasing prevalence of obesity, which has occurred in
the last few decades [23–27]. Moreover, much evidence
indicates the effectiveness of weight reduction on symp-
tom relief, at least in GERD patients who are overweight
or obese [28–30]. In line with these assumptions, our
results show that when BMI tends to higher values the
percentage of students with GERD tends to increase.
Our study has several limitations. First of all, the obser-
vational nature of the study and the groups included
Table 6 Odds ratio and confidence interval for lifestyle correlates with monovariate and multivariate analysis
Conf. Interval Conf. Interval
Oddsratio [ 0.025 0.975] Sig. OddsRatio [ 0.025 0.975] Sig.
Gender(F) 1.45 1.19 1.77 0.00 1.52 1.24 1.87 0.00
Smoker(Yes) 1.71 1.35 2.17 0.00 1.6 1.25 2.05 0.00
Number of coffee 1.1 1.03 1.18 0.01 1.04 0.97 1.12 0.25
BMI Underweight 1 0.72 1.39 0.99 0.97 0.69 1.37 0.88
BMI Overweight 1.17 0.89 1.55 0.27 1.26 0.94 1.69 0.12
BMI Obesity 2.04 1.19 3.49 0.009 1.97 1.14 3.43 0.02
Intercept 0.23 0.000
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 7 of 10
Table 7 Frequency (as percentage) of food group choice overall and by presence of GERD, among all users and the subgroup of
Overall (n=980) No GERD (n=726) GERD (n=254)
Sweets 0 [0-10.1] 0 [0-10.4] 0 [0-10]
Fruits 40 [10.1-73.3] 40.4[11.1-72.6] 40[8.2-75]
Vegetables and salad 36.8 [14.3-59] 36.9 [15.5-60] 36.2[10.3-57.3]
Soups 0 [0-6.5] 0 [0-6.3] 0 [0-7.1]
Seafood 0 [0-6.3] 0 [0-6.3] 0 [0-6.8]
Legumes∗0 [0-8.2] 1.1 [0-9] 0 [0-6.1]
Sandwiches and pizza 8.3 [0-27.7] 7.1 [0-26.7] 10 [0-33.3]
Meat 27.3[1-50] 27.8 [3.6-50] 25 [0-47.7]
Fried foods 20 [0-36.8] 20 [0-36.4] 28.9[0-37.7]
Pies and omelette 3.9 [0-11.8] 4.4 [0-11.8] 2.3 [0-12.1]
Pasta and rice 64.3 [33.3-90.6] 65.8 [33.3-89.9] 55.7 [30.1-93.6]
Potatoes 14 [0-25] 14.3 [0-25] 13.2 [0-25]
Overall (n=395) No GERD (n=304) GERD (n=91)
Sweets 5.15[1.01-12.5] 5.4[0.9-12.5] 4.8[1.5-12.5]
Fruits 44.3[22.1-70.0] 44.4[21.8-70] 40.4[22.8-67.7]
Vegetables and salad 37.3[24.5-53.2] 37.7[26.2-54.7] 35.7[17.8-50]
Soups 3.1[0-10] 3.1[0-10.1] 2.9[0-9.7]
Seafood 3.6[0-8.3] 3.6[0.8-8.3] 2.7[0-8.3]
Legumes 4.3[1.2-7.9] 4.4[1.46-8.3] 3.4[0-6.8]
Sandwiches and pizza 14.0[5.7-27.9] 13.6[5.4-26.8] 17.9[8.4-32.6]
Meat 30.7[17.2-43.0] 31.5[17.3-43.0] 29.7[17.1-44.1]
Fried foods 28.4[17.4-39.3] 28.57[17.7-39.1] 27.3[16.7-40]
Pies and omelette 7.5[4.05-12.5] 7.3[4.2-12.0] 7.7[3.5-14.1]
Pasta and rice∗62.5[40.2-80] 65.5[40.9-81.1] 54.8[35.2-75.7]
Potatoes 17.1[11.5-24.3] 17.2[12.0-24.5] 17.1[11.3-23.8]
*P-value <0.05 for comparison between groups
in the analyses that are represented by students using
the canteen and those participating into the survey thus
precluding the generalizability of results. The aforemen-
tioned limitations were considered when performing sta-
tistical analyses and while results from the Heckman–
type selection model suggested no presence of selec-
tion bias, caution is needed in interpreting results from
that model. As only few variables were available for the
inclusion as covariates, the model adapted could fail in
explaining the mechanism underling survey participa-
tion.Itiswellknownthat the choice of selection
variables can impact model estimates, thus despite sig-
nificance of the variables used in the present analysis,
poor fitting of the model suggested that other variables
than those collected in the present study may impact
on the survey participation. In particular, psychological
factors, as attitudes toward the compliance with survey
study and sensitivity to the theme investigated, proba-
bly play a key role in determining survey participation
and should be addressed in future studies. Anyway, to
support findings from the present study, hypothesizing
that possible differences and attitudes among students
could be reflected in the type of studies they attended,
verification of the presence of selection bias was also
performed in the subgroups of students using the Uni-
versity canteen for which other variables were available.
Including also University Department as covariate in
the selection model did not improve fitting and results
remained invariant, still indicating no presence of selec-
tion bias (data not shown). Moreover, prevalence estimate
obtained from our analysis is coherent with available
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 8 of 10
The second limitation of this study is related to the
intrinsic difficulty of identifying which patients actually
suffer from GERD. Indeed, it is well known that patients
with GERD may present with atypical symptoms, such
as cough, asthma, laryngitis, in the absence of typical
esophageal symptoms, and other patients with GERD
experience no symptoms at all [1,32]. As a consequence,
our estimates will include some students who have typ-
ical GERD symptoms generated by mechanisms other
than reflux (i.e., functional heartburn), as well as will not
include students whose symptoms are sporadic or absent.
However, such limitation represents a common problem
for all population-based studies aimed at investigating
GERD prevalence through questionnaires . Indeed, our
prevalence estimate is coherent with available evidence.
In this context, it must be underlined that we used a sim-
plified version of the GERDq questionnaire to assess the
presence of GERD, limiting the questions only to typical
The third limitation of our study is that this is an obser-
vational study in a very selected group of people (i.e.,
students eating at the canteen) whose results cannot be
directly applied to the general population.
According to our secondary aim, we explored the pos-
sible association between different dietary patterns and
GERD to assess the effects of diet on disease risk. In this
regard, it is worth noting that a strength of this article is
that food items are automatically recorded from cashiers’
transactions at University canteen. Thus, these data are
not affected by the well-known problem of memory effect
, or by the bias due to the tendency in survey respon-
dents to answer questions in a way that will be viewed
favourably by others, the “social desirability” bias . Of
note, when evaluating food choices, among all users a
lower frequency of legumes choice was observed in GERD
students. However, this data was not confirmed when
considering food choices among frequent users. On the
other hand, when considering frequent users we found
a significant lower frequency of choice of pasta and rice
in GERD students. On the basis of the available litera-
ture and of the known pathophysiological mechanisms of
GERD, it is not currently possible to speculate on why this
low frequency of consumption and how this can affect the
symptoms[35–40]. For example, some studies have shown
that consumption of a high-fat diet was associated with
GERD, but several other studies reported conflicting data.
El-Serag et al. have demonstrated that fruits, vegetables,
and high-fiber diets are inversely associated with GERD
, whereas Zheng et al. found that none of these items
was associated with the risk of GERD symptoms . Fur-
thermore, high-fat foods and chocolate are empirically
indicated as foods able to reduce lower esophageal sphinc-
ter pressure or to prolong gastric emptying. Recently, an
interesting study by Keshteli et al.  found that higher
dietary glycaemic index and glycaemic load may be risk
factors for uninvestigated heartburn and uninvestigated
chronic dyspepsia in men, as well as normal-weight sub-
jects, but not in women and overweight individuals. Thus,
consuming a low-glycaemic index diet might be beneficial
in normal-weight patients with uninvestigated heartburn.
Obviously, these findings warrant evaluation in prospec-
tive studies to establish the potential role of carbohydrate
quality in the management of GERD. However, there
have been no cessation trials evaluating the impact on
GERD outcomes. However, our findings show an inter-
esting aspect to be kept in careful consideration and to
be reassessed, continuing to acquire objective data on the
choice of food over time. Overall, our results showed no
differences among students with and without GERD when
distinguishing male and female, or by aggregating stu-
dents by BMI category. A major concern of this analysis
is that the dietary intake information provided by DSU
might be not reflective of participant’s habitual dietary
intake. Indeed, we do not have a complete mapping of
what each student eats every day, outside the Univer-
sity canteen. However, this study might be considered as
pilot study to properly assess the possible influence of dif-
ferent dietary patterns on gastrointestinal diseases based
on real and objective data about eating habits. Moreover,
as regards GERD, according to current available litera-
ture, the effectiveness of dietary recommendations has
not been shown, and, thus, recommendations are to have
a generally healthy diet and to avoid food items that, in the
experience of the patient, trigger symptoms .
To our knowledge, this is the first study evaluating the
prevalence of typical GERD-related symptoms in a young
population of University students in Italy.Our data show a
prevalence rate of weekly symptoms of 26.2%. Consider-
ing the young age of enrolled subjects, our prevalence rate,
relatively high compared to the usual estimates, could rep-
resent a further negative factor for the future economic
sustainability of the healthcare system.
When assessing the effects of diet on disease risk, we
found, among all users, a lower frequency of legumes
choice in GERD students and, among frequent users, a
lower frequency of choice of pasta and rice in GERD stu-
dents. Since food items are automatically recorded from
cashiers’ transactions at University canteen, this study
might be considered as pilot study to properly assess the
possible influence of different dietary patterns on gas-
trointestinal diseases based on real and objective data
about eating habits.
1The 3 levels of obesity were aggregated due to the
reduced number of observations
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 9 of 10
Additional file 1:Supplementary tables. (TEX 11 kb)
BMI: Body mass index; CMS: Content management system; DSU: Azienda
Regionale per il Diritto allo Studio Universitario; GERD: Gastroesophageal reflux
disease; IQR: Inter quartile range
The author wishes to thank Beltos S.r.l. for providing expertise and support in
the development of the web-survey and the staff from "Azienda Regionale per
il Diritto allo Studio Universitario Toscana" for providing data and support for
data linkage as part of the RASUPEA consortium. We also thank the staff from
the University of Pisa for providing data and support for data linkage. Finally
the authors are grateful to all the students who participated in the study.
The work was part of RASUPEA project: “Le mense Universitarie: ricerca sulle
abitudini alimentari dei giovani e d’educazione e prevenzione alimentare". The
project was supported by a grant of the PRAF 2012-2015 REGIONE TOSCANA
program of the Tuscany Region.
Availability of data and materials
Availability of data is restricted to researchers from the academic institution
member of the RASUPEA consortium.
RB, IM and NdB contributed to the conception and design of the study; MN
contributed to the creation, development and management of the final
database for data storage and the statistical analysis of data from the survey;
VL performed statistical analysis for the assessment of selection bias and
description of eating habits; IM, MN, VL co-wrote the manuscript; LP, NdB, GT,
AM, DP and SM critically reviewed the manuscript and provided support in
interpreting data. All authors read and approved the final version of the
Ethics approval and consent to participate
Not applicable. The local ethics committee of the University and Azienda
Ospedaliera Pisana ruled that no formal ethics approval was required in this
A written informed consent was obtained from all participants before entering
the study through the web-app.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
1Division of Gastroenterology–Versilia Hospital, Lido di Camaiore–Lucca, Italy.
2Department of Computer Science–University of Pisa, Pisa, Italy. 3Department
of Biology–University of Pisa, Pisa, Italy. 4Institute of Management, Scuola
Superiore Sant’Anna of Pisa, Pisa, Italy. 5Institute of Information Science and
Technologies ISTI - Italian National Research Council (CNR), Pisa, Italy. 6Division
of Gastroenterology, Department of Translational Research and New
Technologies in Medicine and Surgery–University of Pisa, Pisa, Italy.
Received: 3 January 2018 Accepted: 22 June 2018
1. Vakil N, Van Zanten SV, Kahrilas P, Dent J, Jones R. The montreal
definition and classification of gastroesophageal reflux disease: a global
evidence-based consensus. Am J Gastroenterol. 2006;101(8):1900.
2. Savarino E, Bredenoord AJ, Fox M, Pandolfino JE, Roman S, Gyawali CP,
et al. Expert consensus document: Advances in the physiological
assessment and diagnosis of gerd. Nat Rev Gastroenterol Hepatol.
3. Peery AF, Dellon ES, Lund J, Crockett SD, McGowan CE, Bulsiewicz WJ,
Gangarosa LM, Thiny MT, Stizenberg K, Morgan DR, et al. Burden of
gastrointestinal disease in the united states: 2012 update.
4. El-Serag HB. Time trends of gastroesophageal reflux disease: a systematic
review. Clin Gastroenterol Hepatol. 2007;5(1):17–26.
5. El-Serag HB, Sweet S, Winchester CC, Dent J. Update on the
epidemiology of gastro-oesophageal reflux disease: a systematic review.
Gut. 2014;63(6):871–80. BMJ Publishing Group. https://doi.org/10.1136/
6. Ness-Jensen E, Lindam A, Lagergren J, Hveem K. Changes in prevalence,
incidence and spontaneous loss of gastro-oesophageal reflux symptoms:
a prospective population-based cohort study, the hunt study. Gut.
7. Savarino E, de Bortoli N, De Cassan C, Della Coletta M, Bartolo O,
Furnari M, Ottonello A, Marabotto E, Bodini G, Savarino V. The natural
history of gastro-esophageal reflux disease: a comprehensive review. Dis
8. Castell DO, Murray J, Tutuian R, Orlando R, Arnold R. Review article: the
pathophysiology of gastro-oesophageal reflux disease- oesophageal
manifestations. Aliment Pharmacol Ther. 2004;20(s9):14–25.
9. Bortoli N, Ottonello A, Zerbib F, Sifrim D, Gyawali CP, Savarino E.
Between gerd and nerd: the relevance of weakly acidic reflux. Ann N Y
Acad Sci. 2016;1380(1):218–29.
10. Ness-Jensen E, Hveem K, El-Serag H, Lagergren J. Lifestyle intervention
in gastroesophageal reflux disease. Clin Gastroenterol Hepatol.
11. Kahrilas PJ, Shaheen NJ, Vaezi MF. American gastroenterological
association medical position statement on the management of
gastroesophageal reflux disease. Gastroenterology. 2008;135(4):1383–91.
12. Kahrilas PJ, Shaheen NJ, Vaezi MF. American gastroenterological
association institute technical review on the management of
gastroesophageal reflux disease. Gastroenterology. 2008;135(4):
13. Katz PO, Gerson LB, Vela MF. Guidelines for the diagnosis and
management of gastroesophageal reflux disease. Am J Gastroenterol.
14. DeVault KR, Castell DO. Updated guidelines for the diagnosis and
treatment of gastroesophageal reflux disease. Am J Gastroenterol.
15. Martinucci I, de Bortoli N, Savarino E, Nacci A, Romeo SO, Bellini M,
Savarino V, Fattori B, Marchi S. Optimal treatment of laryngopharyngeal
reflux disease. Ther Adv Chron Dis. 2013;4(6):287–301.
16. Festi D, Scaioli E, Baldi F, Vestito A, Pasqui F, Di Biase AR, Colecchia A.
Body weight, lifestyle, dietary habits and gastroesophageal reflux disease.
World J Gastroenterol WJG. 2009;15(14):1690.
17. Mone I, Kraja B, Bregu A, Duraj V, Sadiku E, Hyska J, Burazeri G.
Adherence to a predominantly mediterranean diet decreases the risk of
gastroesophageal reflux disease: a cross-sectional study in a south
eastern european population. Dis Esophagus. 2016;29(7):794–800.
18. Bortoli N, Martinucci I, Savarino E, Bellini M, Bredenoord A, Franchi R,
Bertani L, Furnari M, Savarino V, Blandizzi C, et al. Proton pump inhibitor
responders who are not confirmed as gerd patients with impedance and
ph monitoring: who are they?. Neurogastroenterol Motil. 2014;26(1):
19. Jones R, Junghard O, Dent J, Vakil N, Halling K, Wernersson B, Lind T.
Development of the gerdq, a tool for the diagnosis and management of
gastro-oesophageal reflux disease in primary care. Aliment Pharmacol
20. Jonasson C, Wernersson B, Hoff D, Hatlebakk J. Validation of the gerdq
questionnaire for the diagnosis of gastro-oesophageal reflux disease.
Aliment Pharmacol Ther. 2013;37(5):564–72.
21. Heckman J. Sample selection bias as a specification error. Econometrica.
22. Valle C, Broglia F, Pistorio A, Tinelli C, Perego M. Prevalence and impact
of symptoms suggestive of gastroesophageal reflux disease. Dig Dis Sci.
Martinucci et al. BMC Gastroenterology (2018) 18:116 Page 10 of 10
23. Bredenoord AJ, Pandolfino JE, Smout AJ. Gastro-oesophageal reflux
disease. Lancet. 2013;381(9881):1933–42.
24. Nilsson M, Johnsen R, Ye W, Hveem K, Lagergren J. Obesity and
estrogen as risk factors for gastroesophageal reflux symptoms. Jama.
25. Ayazi S, Hagen JA, Chan LS, DeMeester SR, Lin MW, Ayazi A, Leers JM,
Oezcelik A, Banki F, Lipham JC, et al. Obesity and gastroesophageal
reflux: quantifying the association between body mass index, esophageal
acid exposure, and lower esophageal sphincter status in a large series of
patients with reflux symptoms. J Gastrointest Surg. 2009;13(8):1440–7.
26. Lagergren J. Influence of obesity on the risk of esophageal disorders. Nat
Rev Gastroenterol Hepatol. 2011;8(6):340–7.
27. Nocon M, Labenz J, Jaspersen D, Meyer-Sabellek W, Stolte M, Lind T,
Malfertheiner P, Willich SN. Association of body mass index with
heartburn, regurgitation and esophagitis: results of the progression of
gastroesophageal reflux disease study. J Gastroenterol Hepatol.
28. Bortoli N, Guidi G, Martinucci I, Savarino E, Imam H, Bertani L, Russo S,
Franchi R, Macchia L, Furnari M, et al. Voluntary and controlled weight
loss can reduce symptoms and proton pump inhibitor use and dosage in
patients with gastroesophageal reflux disease: a comparative study. Dis
29. Singh M, Lee J, Gupta N, Gaddam S, Smith BK, Wani SB, Sullivan DK,
Rastogi A, Bansal A, Donnelly JE, et al. Weight loss can lead to resolution
of gastroesophageal reflux disease symptoms: a prospective intervention
trial. Obesity. 2013;21(2):284–90.
30. Jacobson BC, Somers SC, Fuchs CS, Kelly CP, Camargo Jr CA. Body-mass
index and symptoms of gastroesophageal reflux in women. N Engl J Med.
31. Cuddeback G, Wilson E, Orme JG, Combs-Orme T. Detecting and
statistically correcting sample selection bias. J Soc Serv Res. 2004;30(3):
32. Carlsson R, Dent J, Watts R, Riley S, Sheikh R, Hatlebakk J, Haug K,
de Groot G, van Oudvorst A, Dalväg A, et al. Gastro-oesophageal reflux
disease in primary care: an international study of different treatment
strategies with omeprazole. Eur J Gastroenterol Hepatol. 1998;10(2):
33. Sudman S, Bradburn NM. Effects of time and memory factors on
response in surveys. J Am Stat Assoc. 1973;68(344):805–15.
34. Phillips DL, Clancy KJ. Some effects of “social desirability” in survey
studies. Am J Sociol. 1972;77(5):921–40.
35. El-Serag H, Satia J, Rabeneck L. Dietary intake and the risk of
gastro-oesophageal reflux disease: a cross sectional study in volunteers.
36. Shapiro M, Green C, Bautista J, Dekel R, RISNER-ADLER S, Whitacre R,
Graver E, Fass R. Assessment of dietary nutrients that influence
perception of intra-oesophageal acid reflux events in patients with
gastro-oesophageal reflux disease. Aliment Pharmacol Ther. 2007;25(1):
37. Meyer J, Lembo A, Elashoff J, Fass R, Mayer E. Duodenal fat intensifies
the perception of heartburn. Gut. 2001;49(5):624–8.
38. Colombo P, Mangano M, Bianchi P, Penagini R. Effect of calories and fat
on postprandial gastro-oesophageal reflux. Scand J Gastroenterol.
39. Zheng Z, Nordenstedt H, Pedersen NL, Lagergren J, Ye W. Lifestyle
factors and risk for symptomatic gastroesophageal reflux in monozygotic
twins. Gastroenterology. 2007;132(1):87–95.
40. Nandurkar S, Locke Gr, Fett S, Zinsmeister AR, Cameron A, Talley N.
Relationship between body mass index, diet, exercise and
gastro-oesophageal reflux symptoms in a community. Aliment
Pharmacol Ther. 2004;20(5):497–505.
41. Keshteli A, Haghighatdoost F, Azadbakht L, Daghaghzadeh H,
Feinle-Bisset C, Afshar H, Feizi A, Esmaillzadeh A, Adibi P. Dietary
glycaemic index and glycaemic load and upper gastrointestinal disorders:
results from the sepahan study. J Hum Nutr Diet. 2017;30(6):714–23.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at