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Irritable Bowel Syndrome Is Positively Related to
Metabolic Syndrome: A Population-Based Cross-
Sectional Study
Yinting Guo
1,2
, Kaijun Niu
1
*, Haruki Momma
3
, Yoritoshi Kobayashi
3
, Masahiko Chujo
3
, Atsushi Otomo
3
,
Shin Fukudo
2
, Ryoichi Nagatomi
3
1Nutritional Epidemiology Institute and School of Public Health, Tianjin Medical University, Tianjin, China, 2Department of Behavioral Medicine, Tohoku University
Graduate School of Medicine, Sendai, Japan, 3Division of Biomedical Engineering for Health & Welfare, Tohoku University Graduate School of Biomedical Engineering,
Sendai, Japan
Abstract
Irritable bowel syndrome is a common gastrointestinal disorder that may affect dietary pattern, food digestion, and nutrient
absorption. The nutrition-related factors are closely related to metabolic syndrome, implying that irritable bowel syndrome
may be a potential risk factor for metabolic syndrome. However, few epidemiological studies are available which are related
to this potential link. The purpose of this study is to determine whether irritable bowel syndrome is related to metabolic
syndrome among middle-aged people. We designed a cross-sectional study of 1,096 subjects to evaluate the relationship
between irritable bowel syndrome and metabolic syndrome and its components. Diagnosis of irritable bowel syndrome was
based on the Japanese version of the Rome III Questionnaire. Metabolic syndrome was defined according to the criteria of
the American Heart Association scientific statements of 2009. Dietary consumption was assessed via a validated food
frequency questionnaire. Principal-components analysis was used to derive 3 major dietary patterns: ‘‘Japanese’’, ‘‘sweets-
fruits’’, and ‘‘Izakaya (Japanese Pub) ‘‘from 39 food groups. The prevalence of irritable bowel syndrome and metabolic
syndrome were 19.4% and 14.6%, respectively. No significant relationship was found between the dietary pattern factor
score tertiles and irritable bowel syndrome. After adjustment for potential confounders (including dietary pattern), the odds
ratio (95% confidence interval) of having metabolic syndrome and elevated triglycerides for subjects with irritable bowel
syndrome as compared with non-irritable bowel syndrome are 2.01(1.13–3.55) and 1.50(1.03–2.18), respectively. Irritable
bowel syndrome is significantly related to metabolic syndrome and it components. This study is the first to show that
irritable bowel syndrome was significantly related to a higher prevalence of metabolic syndrome and elevated triglycerides
among an adult population. The findings suggest that the treatment of irritable bowel syndrome may be a potentially
beneficial factor for the prevention of metabolic syndrome. Further study is needed to clarify this association.
Citation: Guo Y, Niu K, Momma H, Kobayashi Y, Chujo M, et al. (2014) Irritable Bowel Syndrome Is Positively Related to Metabolic Syndrome: A Population-Based
Cross-Sectional Study. PLoS ONE 9(11): e112289. doi:10.1371/journal.pone.0112289
Editor: Andreas Zirlik, University Heart Center Freiburg, Germany
Received January 27, 2014; Accepted October 14, 2014; Published November 10, 2014
Copyright: 2014 Guo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by a Grant-in-Aid for ‘‘Knowledge Cluster Initiative’’ from the Ministry of Education, Culture, Sports, Science and Technology
of Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: All the authors have no conflicts of interest exists to disclose.
* Email: nkj0809@163.com
Introduction
Irritable bowel syndrome (IBS) is a common gastrointestinal
disorder characterized by episodes of recurrent abdominal pain or
discomfort related to disturbed bowel habits [1,2]. The majority of
subjects with IBS are conscious that diet may play a role in
triggering these episodes and therefore may avoid certain foods
and changes in their dietary pattern [3–8]. Furthermore, IBS
disrupts the digestion of food, or directly interferes with nutrient
absorption [9–11].
Metabolic syndrome (MS) is a well-recognized constellation of
risk factors for cardiovascular disease (CVD) [12], which remains a
major cause of mortality and morbidity worldwide [13]. Accu-
mulated evidence suggests that dietary factors are the cornerstone
for the prevention and treatment of MS [14–16]. Furthermore,
with respect to dietary factors studies, researchers have usually
focused predominantly on the effects of individual nutrients and
sometimes foods, but rarely on dietary patterns. However, daily
diets are composed of a wide variety of foods containing complex
combinations of nutrients. The surveys that examine a single
nutrient in foods, or a single food, may not adequately account for
complicated interactions and cumulative effects on human health.
Therefore, compared with a single nutrient in foods or a single
food, a dietary pattern study may be a more important tool for
evaluation of the effects of diet on health [17,18].
Irritable bowel syndrome status may affect the dietary pattern,
food digestion, and nutrient absorption, which are important
factors for the prevention and treatment of MS and/or its
components. Therefore, it is speculated that IBS may be a
potential risk factor for MS. However, few epidemiological studies
have assessed the relationship between IBS status and MS and its
components in an adult population.
At present, we have designed a cross-sectional study to
determine whether IBS is related to MS among middle-aged
people.
PLOS ONE | www.plosone.org 1 November 2014 | Volume 9 | Issue 11 | e112289
Materials and Methods
Study Population
The current analysis uses data from a population-based
longitudinal study designed to investigate the lifestyle risk factors
of CVD among Japanese adults. The methods are described in
detail elsewhere [19,20].
There were 1,208 subjects who had received a health
examination including blood examinations in 2011. Of these,
1,163 subjects agreed to participate and provided informed
consent for their data to be analyzed. Subjects were excluded if
they did not provide any dietary information (n = 21) or did not
answer the Rome III Modular Questionnaire (n = 46). Owing to
these exclusions, the final cross-sectional study population
comprised 1,096 subjects (mean [standard deviation, SD] age:
46.2 [11.2] years; male, 77.5%). The Institutional Review Board of
the Tohoku University Graduate School of Medicine approved the
study protocol.
Assessment of IBS
The Japanese version of the Rome III Questionnaire was used
to screen for IBS [21]. All subjects were asked to complete self-
reported ROME III diagnostic questionnaires. Screening for IBS
requires that subjects have abdominal discomfort or pain lasting at
least 3 days per month, not necessarily consecutive, during the
previous 3 months which is associated with 2 or more of the
following: relief by defecation; onset associated with a change in
frequency of stool; onset associated with a change in form
(appearance) of stool.
Assessment of MS and Other
Waist circumference was measured at the umbilical level with
participants standing and breathing normally. Blood pressure (BP)
was measured twice from the upper left arm using a YA-
MASU605P automatic device (Kenzmedico, Saitama, Japan) after
5 min of rest in the seated position. The mean of these 2
measurements was taken as the BP value. Blood samples were
collected in siliconized vacuum glass tubes containing sodium
fluoride, for the analysis of fasting blood glucose (FBG), or
containing no additives, for the analysis of lipids. Fasting blood
glucose was measured by using enzymatic methods (Eerotec,
Tokyo, Japan). The concentrations of triglycerides (TG), low-
density lipoprotein cholesterol (LDL), and high-density lipoprotein
cholesterol (HDL) were measured by enzymatic methods using
appropriate kits (Sekisui Medical, Tokyo, Japan). Serum high-
sensitive C-reactive protein (hsCRP) levels were determined using
N-latex CRP-2 (Siemens Healthcare Japan, Tokyo, Japan). The
measurement limit of hsCRP was 0.02 mg/L and an hsCRP value
less than the measurement limit was considered to be 0.01 mg/L.
Metabolic syndrome was defined in accordance with the criteria
of the American Heart Association scientific statements of 2009
[22]. Participants were considered to have MS when they
presented three or more of the following components: 1) elevated
waist circumference for Asian individuals ($90 cm and $80 cm in
male and female, respectively), 2) elevated TG ($150 mg/dL), or
drug treatment for elevated TG, 3) reduced HDL (,40 mg/dL in
male; ,50 mg/dL in female) or drug treatment for reduced HDL,
4) elevated blood pressure (SBP $130 mm Hg and/or DBP $
85 mm Hg) or antihypertensive drug treatment, 5) elevated fasting
glucose ($100 mg/dL) or drug treatment of elevated glucose.
Assessment of Dietary Intake
The subjects were instructed to complete a brief, self-adminis-
tered diet history questionnaire (BDHQ) that included questions
on 75 food items along with their specified serving sizes, described
in terms of natural portions or standard weights and volume
measures of the servings, commonly consumed by the study
population. For each food item, the subjects indicated their mean
frequency of consumption of the food over the past month in terms
of the specified serving size by checking 1 of the 7 frequency
categories, ranging from ‘‘almost never’’ to ‘‘2 or more times/
day’’. The mean daily consumption of nutrients was calculated
using an ad hoc computer program developed to analyze the
questionnaire. The Japanese food composition tables, 5
th
edition,
[23] and other [24] were used as the nutrient database. The
reproducibility and validity of the BDHQ have already been
described in detail elsewhere [25]. Foods from the BDHQ were
categorized into 39 food subgroups, which were used to derive
dietary patterns via principal-components analysis.
Factor analysis (principal-components analysis) was used to
derive dietary patterns and to determine factor loadings for each of
the 39 food subgroups (in g/d) [26]. Factors were rotated with
varimax rotation to maintain uncorrelated factors and enhance
interpretability [27]. A combined evaluation of the eigenvalues,
scree plot test, and factor interpretability was used in determining
the number of retained factors. The distinctive dietary patterns of
the study population were well described by the 3 factors. Factors
were named descriptively according to the food items showing
high loading (absolute value) with respect to each dietary pattern
as follows: ‘‘Japanese’’ dietary pattern (factor 1), ‘‘sweets-fruits’’
pattern (factor 2), and ‘‘Izakaya (Japanese Pub)’’ pattern (factor 3)
(see Table S1). For each dietary pattern and each subject, we
calculated a factor score by summing the consumption from each
food item weighted by its factor loading as follows [27]:
Xfood groupiservings=dðÞ|food groupifactor loadingðÞ½Þ
where i= food groups 1–39. A higher factor score indicates
greater conformity to the dietary pattern. Variables unrelated to a
given dietary pattern are weighted close to zero. For further
analyses, factor scores were categorized into 3 equal groups by
using tertiles cutoffs.
Assessment of Other Variables
Sociodemographic variables, including age, gender, and edu-
cational levels were also assessed. The educational level was
assessed by determining the last grade level and was divided into 2
categories: ,college or $college. Body mass index (BMI) was
calculated as weight in kilograms divided by squared height in
meters (kg/m2). History of physical illness and current medication
were noted from ‘‘yes’’ or ‘‘no’’ responses to relevant questions.
Information on smoking status, and drinking status were obtained
from a questionnaire survey. Levels of daily physical activity (PA)
were estimated using the International Physical Activity Ques-
tionnaire (IPAQ) (Japanese version) [28]. Total daily PA
(metabolic equivalents [METs]6hours/week) were calculated as
follows: (daily hours of walking 6days per week with
walking63.3)+(daily hours of moderate-intensity activity6days
per week with moderate-intensity activity64.0)+(daily hours of
vigorous activity6days per week with vigorous activity68.0). The
METs values were derived from the IPAQ validity and reliability
study [28]. Physical activity was categorized into three groups: no
PA, low PA (0,PA,23 METs 6hours/week), and high PA ($23
METs6hours/week) [29]. Depressive symptoms were assessed
according to the Japanese version of the Self-Rating Depression
Scale (SDS) [30]. An SDS score $45 was taken as the cutoff point
indicating depressive symptoms [31].
Irritable Bowel Syndrome & Metabolic Syndrome
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Statistical Analysis
All statistical analyses were performed using the Statistical
Analysis System 9.1 edition for Windows (SAS Institute Inc., Cary,
NC, USA). The age- and sex-adjusted variable differences
according to IBS status were examined by analysis of covariance
(ANCOVA) for continuous variables or by the multiple logistic
regression analysis for variables of proportion. For main analysis,
the MS or its components were used as a dependent variable and
IBS status as independent variables. The odds ratio (OR) and 95%
confidence interval (CI) of MS and its components compared with
IBS status were calculated using multiple logistic regression
analysis. We used age, sex, BMI, smoking and drinking status,
educational level, PA levels, dietary patterns, total energy intake,
depressive symptoms and mutual metabolic syndrome components
as covariates for multiple adjustments. Model fit was evaluated
using the Hosmer-Lemeshow goodness-of-fit statistic. For all
models, the test was not significant (P$0.31). Interactions between
IBS status and confounders of MS or its components were tested
by the addition of cross-product terms to the regression model. All
tests were two-tailed and P,0.05 was defined as statistically
significant.
Results
Among 1,096 subjects who were available to be analyzed, 213
(19.4%) had self-reported IBS, and 160 (14.6%) had MS.
Age- and sex-adjusted characteristics of study subjects with and
without IBS are presented in Table 1. Subjects with IBS were
significantly younger than the non-IBS subjects (P,0.01) with a
mean (95% CI) 43.4 (41.9–45.0) y compared to 46.1 (45.3–47.0) y.
Subjects with IBS contained a lower proportion of males, and a
higher proportion of ex-smokers and depressive symptoms (P,
0.05 for all comparisons). Compared to subjects with IBS, the non-
IBS subjects had lower total energy intake, and serum TG levels
(P,0.05 for all comparisons).
Because IBS may affect the dietary pattern [32], as an initial
step, we evaluated the relationships between dietary patterns and
IBS. Three major dietary patterns were identified by factor
analysis (Table S1). Factor 1, identified as a traditional
‘‘Japanese’’ dietary pattern was characterized by a high consump-
tion of vegetables, seaweeds, soybean products, fish, fruits, miso
soup, and green tea. Factor 2 was typified by a greater
consumption of cake, ice cream, fruits, bread, dairy products,
mayonnaise and lower consumption of alcohol (named the
‘‘sweets-fruits’’ pattern). Factor 3 was typified by a greater
consumption of noodles, Squid, octopus, lobster, shellfish, meat,
fish, cola, alcohol, coffee, mayonnaise, chicken egg, and bread
(named the ‘‘Izakaya (Japanese Pub)’’ pattern). These 3 patterns
explained 32.1% of the variance in dietary consumption (18.6%
for factor 1, 7.5% for factor 2, and 6.0% for factor 3). Increasing
the number of patterns did not materially increase the total
proportion of variance in dietary consumption explained by the
model. Daily food and nutrient consumption are presented
according to tertiles of dietary pattern factor score in Table S2.
Compared to subjects with factor scores in the lowest tertile for the
‘‘Japanese’’ dietary pattern, those in the highest tertile had a
higher consumption of total meats, total fish, seaweeds, total
vegetables, soybean products, total fruits, dairy products, green
tea, black or oolong tea, total energy intake, animal protein,
vegetable protein, animal fat, vegetable fat, carbohydrate, total
fiber, calcium, and eicosapentaenoic acid (EPA) +docosahexae-
noic acid (DHA), and lower consumptions of cola (Pfor trend ,
0.05). Compared to those in the middle ‘‘sweets-fruits’’ pattern
tertile, subjects in the highest tertile had significant higher
consumptions of total fish, total seaweeds, total vegetables, total
fruit, dairy products, green tea, cola, total energy intake, animal
protein, vegetable protein, animal fat, vegetable fat, carbohydrate,
total fiber, calcium, EPA+DHA, and a lower consumption of
alcohol (P,0.05). Compared to those in the lowest ‘‘Izakaya
(Japanese Pub)’’ pattern tertile, subjects in the highest tertile had a
higher consumption of total meats, total fish, seaweeds, coffee,
cola, total energy intake, animal protein, vegetable protein, animal
fat, vegetable fat, carbohydrate, total fiber, calcium, EPA+DHA,
alcohol, lower consumption of total fruits, and dairy products (P
for trend ,0.01). The age- and sex-adjusted relationships between
tertiles of dietary pattern factor score and IBS status are indicated
in Table 1. No significant relationships between the tertiles of
each dietary pattern and IBS status were observed. These results
were unchanged when we adjusted for multiple confounding
factors (see Table 2 model 5) (P.0.15 for all comparisons).
We next investigated whether IBS status is related to MS and its
components. Table 2 shows the adjusted relationships between
IBS status and MS and its components. In the final multivariate
models, the adjusted ORs (95% CI) of MS related to IBS group as
compared with the non-IBS group is 2.01 (1.13–3.55). In MS
components analysis, IBS status was only positively related to
elevated TG in the final model (OR [95% CI]: 1.50 [1.03–2.18]).
Although the difference was not statistically significant, the
proportion of subjects with elevated waist circumference was
higher in IBS group (OR [95% CI]: 1.60 [0.85–2.96]) in the final
multivariate models. No significant relationships were observed
between IBS status and other MS components in the final
multivariate models. The tests for interactions between IBS status
and other potential confounders in the final models were also not
statistically significant (interaction P values.0.22).
Discussion
In this cross-sectional study, we investigated the relationships
between IBS and MS in an adult population. This study is the first
to show that IBS is independently related to a higher prevalence of
MS and elevated TG. Further, no significant relationships between
IBS and dietary patterns were observed.
In this study, we adjusted for various potential confounders
related to IBS and/or MS. First, we considered that age, sex (see
Table 1), and body mass index [33] were potential confounders.
Second, the effect of lifestyle factors, such as smoking [33] and
drinking status [34], physical activity [35], and educational level
[36], were adjusted. Moreover, IBS can affect dietary intake and
thus affect the dietary pattern. Furthermore, dietary factors are
also important for incidence of MS [35]. Accordingly, we made
adjustments for total energy intake, and dietary pattern. Third,
depressive symptoms are also closely related to IBS (see Table 1)
and MS [37]. However, adjustments for these confounding factors
did not change the significant positive relationship between IBS
and MS. That is, the positive relationship between IBS and MS
was independent of these factors.
It is hypothesized that IBS has a potentially adverse effect on
MS and its components possibly due to effect on dietary pattern,
food digestion, or nutrient absorption. However, no significant
relationships between IBS and dietary patterns were observed.
The result was similar to a previous study, suggesting that IBS is
not related to dietary habits and/or nutritional intake [38].
Furthermore, although several studies have demonstrated self-
reported food intolerances in most patients with IBS [3–8], two
other studies have indicated that those with IBS appear to have
adequate and balanced food and macronutrient intake, with no
evidence of inadequate micronutrient intake [39,40]. Therefore,
Irritable Bowel Syndrome & Metabolic Syndrome
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we consider that while IBS symptoms affect the choice of certain
specific food items, it has no essential impact on dietary pattern or
the intake of nutrients. In the modern world, especially in
developed countries, a variety of different foods are available in
daily life. The availability of these choices may well make up for
IBS symptoms-bringing harmful effects from certain food items.
Further study is needed to confirm this hypothesis.
Despite underlying causes of pathophysiologic changes still not
being completely understood, low grade mucosal inflammation,
increased intestinal mucosal permeability, and abnormal intestinal
motility are accepted mechanisms which alter gut function and
Table 1. Age- and sex-adjusted characteristics of the subjects in relation to irritable bowel syndrome (n = 1,096)
{
Irritable bowel syndrome
P
value
`
No (n = 883) Yes (n = 213)
Age (y) 46.1 (45.3–47.0)
1
43.4 (41.9–45.0) ,0.01
Sex (male, %) 79.2 70.4 0.02
BMI (kg/m2) 22.8 (22.5–23.0) 22.6 (22.1–23.1) 0.54
Smoking status (%)
Current smoking 40.8 36.6 0.46
Ex-smoking 12.5 17.4 0.049
Never-smoking 46.6 46.0 0.53
Drinking status (%)
Daily 28.3 25.4 0.77
Sometimes 48.5 50.2 0.93
Never-drinking 23.2 24.4 0.89
Educational level ($college, %) 33.8 28.2 0.14
PA (%)
0 METs hours/week 25.4 23.5 0.50
0–23 METs hours/week 39.9 44.6 0.37
$23 METs hours/week 34.8 31.9 0.76
Total energy intake (kcal/d) 1733.0 (1686.7–1779.4) 1836.6 (1754.4–1918.7) 0.02
‘‘Japanese’’ dietary pattern
The lowest tertile of factor score 32.7 35.7 0.85
The middle tertile of factor score 33.9 31.5 0.41
The highest tertile of factor score 33.4 32.9 0.48
‘‘sweets-fruits’’ dietary pattern
The lowest tertile of factor score 34.4 28.6 0.37
The middle tertile of factor score 33.6 32.4 0.44
The highest tertile of factor score 31.9 39.0 0.09
‘‘Izakaya (Japanese Pub)’’ dietary pattern
The lowest tertile of factor score 33.8 31.5 0.24
The middle tertile of factor score 33.9 31.5 0.55
The highest tertile of factor score 32.4 37.1 0.08
Depressive symptoms (SDS $45, %) 30.9 42.7 ,0.01
Waist (cm) 80.2 (79.5–81.0) 80.6 (79.3–81.9) 0.61
SBP (mmHg) 122.1 (120.9–123.2) 121.6 (119.6–123.6) 0.67
DBP (mmHg) 75.7 (74.8–76.5) 75.1 (73.6–76.6) 0.49
Log translated TG (mg/dl)
"
86.5 (82.7–90.5) 98.4 (90.9–106.5) ,0.01
FBG (mg/dl) 96.7 (94.8–98.6) 96.4 (93.0–99.7) 0.85
HDL (mg/dl) 62.6 (61.5–63.7) 61.5 (59.6–63.4) 0.31
LDL (mg/dl) 114.1 (111.7–116.4) 114.5 (110.2–118.7) 0.87
Log translated hsCRP (mg/L)
"
0.32 (0.29–0.35) 0.30 (0.26–0.36) 0.64
{
BMI, body mass index; PA, physical activity; METs, metabolic equivalents; SDS, Self-rating Depression Scale; SBP, systolic blood pressure; DBP, diastolic blood pressure;
TG, triglyceride; FBG, fasting blood glucose; HDL, high-density lipoprotein-cholesterol; LDL, low-density lipoprotein; hsCRP, high-sensitivity C-reactive protein.
`
Analysis of covariance or logistic regression analysis adjusted for age and sex where appropriate.
1
Adjusted least squares mean (95% confidence interval) (all such values).
"
Adjusted geometric mean (95% confidence interval).
doi:10.1371/journal.pone.0112289.t001
Irritable Bowel Syndrome & Metabolic Syndrome
PLOS ONE | www.plosone.org 4 November 2014 | Volume 9 | Issue 11 | e112289
generate symptoms of IBS [41]. The response of the gastrointes-
tinal tract to ingestion of food is a complex and closely controlled
process, which allows optimization of propulsion, digestion,
absorption of nutrients, and removal of indigestible remnants.
Therefore, it is believed that IBS is an important risk factor in the
digestion of food and in nutrient absorption. Many studies have
investigated the effects of IBS on the digestion of food or nutrient
absorption [9–11]. These studies have consistently demonstrated
that increased and discordant absorption of some nutrients, such
as mannitol and sorbitol occurs in subjects with IBS compared to
healthy controls [9–11]. In the present study, we found that IBS is
mainly related to elevated TG, suggesting that IBS may affect the
digestion and absorption of fats in the gastrointestinal tract. In fact,
several studies have evaluated the relationships between IBS and
the digestion and absorption of fats [8,42]. Simren et al. have
reported IBS to be related to increased colonic sensitivity and an
altered viscerosomatic referral pattern after duodenal lipids
infusion [42]. Another study also indicated that gastrointestinal
symptoms were frequently reported after intake of fried and fatty
foods in IBS patients [8]. Therefore, we consider the relationship
between IBS and MS and its components to be possibly due to the
disorder of food digestion and nutrient absorption, especially in the
fat components. This study, which was designed to investigate the
relationships between IBS and MS, is very limited and we
therefore cannot determine an exact mechanism to explain our
observations. Further studies are needed to make certain the
causality and exact mechanisms of IBS in MS.
On the other hand, gut microbiota alterations could also be
considered a potential link between IBS and MS and its
components. The accumulated evidence has indicated that IBS
is related to quantitative and qualitative changes in gut microbiota
[43]. Because the gut microbiota is becoming known as a more
and more important risk factor for the treatment and prevention of
MS [44,45], there is conjecture that IBS may be a potential risk
factor for MS due to the effect of IBS on the quantitative and
qualitative changes of gut microbiota. Further studies are needed
to clarify this hypothesis.
A small-scale case-control study has shown that IBS was
significantly related to a higher FBS and higher prevalence of
prediabetes than in the control group [46]. In contrast, the present
study did not find significant relationships between IBS and FBG
or elevated FBG. Although the reason remains unclear, differences
in age (mean age is 46.2 y in our study vs 33.0 y in their study),
adjustment factors (all lifestyle factors were adjusted in their study)
and population size may partly explain the discrepancy. Further
study is needed to investigate this issue.
To the best of our knowledge, no previous study has examined
the relationships between dietary pattern and IBS among the
general population. The present study first investigated the
relationships between dietary patterns and IBS in apparently
healthy adults. The results suggest that dietary patterns were not
related to the prevalence of IBS. Furthermore, the traditional
Japanese diet is a well-known healthy diet pattern [26,47]. Thus,
we also evaluated whether the traditional Japanese dietary pattern
was significantly related to a lower prevalence of IBS. The results
indicated that no significant relationships between traditional
Japanese dietary patterns and IBS were observed. Further study is
needed to make certain of our observations.
This study had several limitations. First, the Rome III
questionnaire is designed for the measurement and screening of
IBS, not for making a clinical diagnosis. Therefore, a population
study that uses a standardized comprehensive structured diagnos-
tic interview should be undertaken to confirm the influence of IBS
on MS. Second, because this study was a cross-sectional study, we
could not conclude that IBS increases the occurrence of MS or
that MS leads to episodes of IBS in adult populations. Therefore, a
prospective study or trial should be undertaken to confirm the
existence of a relationship between IBS, and MS and elevated TG.
In the present study, IBS was significantly related to a higher
prevalence of MS and elevated TG among an adult population.
The differences in dietary patterns are not likely to explain our
findings. The findings suggest that the treatment of IBS may be a
potentially beneficial factor for the development and prevention of
MS. Further study is required to clarify this causality.
Supporting Information
Table S1 Principal components analysis varimax-rotated 39
food groups factor loading scores (n = 1,096).
(DOC)
Table 2. Adjusted odds ratios and 95% confidence interval for the relationship between MS and IBS (n = 1,096)
{
IBS vs non IBS
Model 1
`
Model 2
1
Model 3
"
Model 4 Model 5
|
MS 1.85 (1.05–3.20) 1.94 (1.10–3.37) 2.01 (1.13–3.52) 2.01 (1.13–3.55) -
MS components
Waist circumference $90 cm for male
or $80 cm for female
1.61 (0.89–2.92) 1.68 (0.91–3.06) 1.64 (0.88–3.03) 1.60 (0.86–2.97) 1.60 (0.85–2.96)
Triglycerides $150 mg/dL 1.52 (1.05–2.18) 1.53 (1.06–2.20) 1.52 (1.04–2.19) 1.51 (1.04–2.19) 1.50 (1.03–2.18)
HDL-cholesterol ,40 mg/dL 1.04 (0.56–1.85) 0.99 (0.51–1.80) 1.00 (0.52–1.83) 1.04 (0.53–1.92) 1.00 (0.51–1.85)
SBP $130 mmHg or DBP $85 mmHg 1.04 (0.74–1.48) 1.03 (0.72–1.47) 1.05 (0.73–1.51) 1.06 (0.74–1.53) 1.04 (0.72–1.50)
High fasting glucose $100 mg/dL 1.27 (0.74–2.11) 1.24 (0.72–2.07) 1.26 (0.73–2.12) 1.25 (0.72–2.11) 1.19 (0.68–2.03)
{
MS, metabolic syndrome; IBS, irritable bowel syndrome; HDL, high-density lipoprotein cholesterol; SBP, systolic blood pressure; DBP, diastolic blood pressure.
`
Adjusted for age, sex and body mass index.
1
Additionally adjusted for smoking and drinking status, educational level, and physical activity.
"
Additionally adjusted for dietary patterns, and total energy intake.
Additionally adjusted for depressive symptoms.
|
Additionally adjusted for mutual metabolic syndrome components.
doi:10.1371/journal.pone.0112289.t002
Irritable Bowel Syndrome & Metabolic Syndrome
PLOS ONE | www.plosone.org 5 November 2014 | Volume 9 | Issue 11 | e112289
Table S2 Daily food and nutrient consumption of the partici-
pants according to the tertiles of dietary pattern factor score
(n = 1,096).
(DOC)
Acknowledgments
We gratefully acknowledge all the men and women who participated in the
study and Sendai Oroshisho Center for the possibility to perform the study.
Author Contributions
Conceived and designed the experiments: KN SF RN. Performed the
experiments: YG KN HM YK MC AO. Analyzed the data: YG KN.
Contributed reagents/materials/analysis tools: YG KN. Wrote the paper:
YG KN. Critical revision of the manuscript for important intellectual
content: YG KN SF RN.
References
1. Camilleri M (2001) Management of the irritable bowel syndrome. Gastroenter-
ology 120: 652–668.
2. Chang L (2004) Review article: epidemiology and quality of life in functional
gastrointestinal disorders. Aliment Pharmacol Ther 20 Suppl 7: 31–39.
3. Hayes P, Corish C, O’Mahony E, Quigley EM (2013) A dietary survey of
patients with irritable bowel syndrome. J Hum Nutr Diet: (in press. doi:
10.1111/jhn.12114).
4. Feinle-Bisset C, Azpiroz F (2013) Dietary lipids and functional gastrointestinal
disorders. Am J Gastroenterol 108: 737–747.
5. Simren M, Mansson A, Langkilde AM, Sved lund J, Abrahamsson H, et al.
(2001) Food-related gastrointestinal symptoms in the irritable bowel syndrome.
Digestion 63: 108–115.
6. Park HJ, Jarrett M, Heitkemper M (2010) Quality of life and sugar and fiber
intake in women with irritable bowel syndrome. West J Nurs Res 32: 218–232.
7. Aller R, de Luis DA, Izaola O, La Calle F, del Olmo L, et al. (2004) [Dietary
intake of a group of patients with irritable bowel syndrome; relation between
dietary fiber and symptoms]. An Med Interna 21: 577–580.
8. Bohn L, Storsrud S, Tornblom H, Bengtsson U, Simren M (2013) Self-reported
food-related gastrointestinal symptoms in IBS are common and associated with
more severe symptoms and redu ced quality of life. Am J Gastroenterol 108:
634–641.
9. Marciani L, Cox EF, Hoad CL, Pritchard S, Totman JJ, et al. (2010)
Postprandial changes in small bowel water content in healthy subjects and
patients with irritable bowel syndrome. Gastroenterology 138: 469–477, 477
e461.
10. Keller J, Layer P (2009) Intestinal and anorectal motility and functional
disorders. Best Pract Res Clin Gastroenterol 23: 407–423.
11. Yao CK, Tan HL, van Langenberg DR, Barrett JS, Rose R, et al. (2013) Dietary
sorbitol and mannitol: food content and distinct absorption patterns between
healthy individuals and patients with irritable bowel syndrome. J Hum Nutr
Diet.
12. Nikolopoulou A, Kadoglou NP (2012) Obesity and metabolic syndrome as
related to cardiovascular disease. Expert Rev Cardiovasc Ther 10: 933–939.
13. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, et al. (2012) Global and
regional mortality from 235 causes of death for 20 age groups in 1990 and 2010:
a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:
2095–2128.
14. Nestel P (2004) Nutritional aspects in the causation and management of the
metabolic syndrome. Endocrinol Metab Clin North Am 33: 483–492, v.
15. Josse AR, Jenkins DJ, Kendall CW (2008) Nutritional determinants of the
metabolic syndrome. J Nutrigenet Nutrigenomics 1: 109–117.
16. Leao LS, de Moraes MM, de Carvalho GX, Koifman RJ (2011) Nutritional
interventions in metabolic syndrome: a systematic review. Arq Bras Cardiol 97:
260–265.
17. Willett WC, McCullough ML (2008) Dietary pattern analysis for the evaluation
of dietary guidelines. Asia Pac J Clin Nutr 17 Suppl 1: 75–78.
18. Hu FB (2002) Dietary pattern analysis: a new direction in nutritional
epidemiology. Curr Opin Lipidol 13: 3–9.
19. Niu K, Kobayashi Y, Guan L, Monma H, Guo H, et al. (2013) Low-fat dairy,
but not whole-/high-fat dairy, consumption is related with higher serum
adiponectin levels in apparently healthy adults. Eur J Nutr 52: 771–778.
20. Niu K, Kobayashi Y, Guan L, Momma H, Guo H, et al. (2013) Longitudinal
changes in the relationship between serum adiponectin concentration and
cardiovascular risk factors among apparently healthy middle-aged adults.
Int J Cardiol: (http://dx.doi.org/10.1016/j.bbr.2011.1003.1031).
21. Fukudo S, Hongo M, Matsueda K, Drossman DA (2008) The Japanese Version
of Rome III: the Functional Gastrointestinal Disorders, 3rd edn. Tokyo:
KYOWA KIKAKU Ltd,.
22. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, et al. (2009)
Harmonizing the metabolic syndrome: a joint interim statement of the
International Diabetes Federation Task Force on Epidemiology and Prevention;
National Heart, Lung, and Blood Institute; American Heart Association; World
Heart Federation; International Atherosclerosis Society; and International
Association for the Study of Obesity. Circulation 120: 1640–1645.
23. Science and Technology Agency: Standard Tables of Food Composition in
Japan (Fifth revised edition). Printing Buteau, Ministry of Finance, Tokyo, 2000
(in Japanese).
24. Sakai K, Nakajima M, Watanabe S, Kobayashi T (1995) Available data on
assessments of dietary fatty acid intake. J Lipid Nutr 4: 97–103 (in Japanese).
25. Sasaki S (2005) Serum Biomarker-based Validation of a Brief-type Self-
administered Diet History Questionnaire for Japanese Subjects, The Study
Group of Ministry of Health, Labor and Welfare of Japan, Tanaka H, chairman,
‘‘A research for assessment of nutrition and dietary habit in ‘‘Kenko Nippon 21’’.
Tokyo: 10–42 (in Japanese).
26. Guo H, Niu K, Monma H, Kobayashi Y, Guan L, et al. (2012) Association of
Japanese dietary pattern with serum adiponectin concentration in Japanese adult
men. Nutr Metab Cardiovasc Dis 22: 277–284.
27. Kim J, Mueller C (1978) Factor Analysis: Statistical Methods and Practical
Issues. Beverly Hills, Calif: Sage Publications;.
28. Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, et al. (2003)
International physical activity questionnaire: 12-country reliability and validity.
Med Sci Sports Exerc 35: 1381–1395.
29. Ishikawa-Takata K, Tabata I (2007) Exercise and Physical Activity Reference
for Health Promotion 2006 (EPAR2006). J Epidemiol 17: 177.
30. Fukuda K, Kobayashi S (1973) A study on a self-rating depression scale.
Psychiatria et Neurologia Japonica 75: 673–679 (in Japanese).
31. Barrett J, Hurst MW, DiScala C, Rose RM (1978) Prevalence of depression over
a 12-month period in a nonpatient population. Arch Gen Psychiatry 35: 741–
744.
32. Morcos A, Dinan T, Quigley EM (2009) Irritable bowel syndrome: role of food
in pathogenesis and management. J Dig Dis 10: 237–246.
33. Cena H, Fonte ML, Turconi G (2011) Relationship between smoking and
metabolic syndrome. Nutr Rev 69: 745–753.
34. Alkerwi A, Boutsen M, Vaillant M, Barre J, Lair ML, et al. (2009) Alcohol
consumption and the prevalence of metabolic syndrome: a meta-analysis of
observational studies. Atherosclerosis 204: 624–635.
35. Yamaoka K, Tango T (2012) Effects of lifestyle modification on metabolic
syndrome: a systematic review and meta-analysis. BMC Med 10: 138.
36. Li YQ, Zhao LQ, Liu XY, Wang HL, Wang XH, et al. (2013) Prevalence and
distribution of metabolic syndrome in a southern Chinese population. Relation
to exercise, smoking, and educational level. Saudi Med J 34: 929–936.
37. Pan A, Keum N, Okereke OI, Sun Q, Kivimaki M, et al. (2012) Bidirectional
association between depression and metabolic syndrome: a systematic review
and meta-analysis of epidemiological studies. Diabetes Care 35: 1171–1180.
38. Jung HJ, Park MI, Moon W, Park SJ, Kim HH, et al. (2011) Are Food
Constituents Relevant to the Irritable Bowel Syndrome in Young Adults? - A
Rome III Based Prevalence Study of the Korean Medical Students.
J Neurogastroenterol Motil 17: 294–299.
39. Williams EA, Nai X, Corfe BM (2011) Dietary intakes in people with irritable
bowel syndrome. BMC Gastroenterol 11: 9.
40. Saito YA, Locke GR 3rd, Weaver AL, Zinsmeister AR, Talley NJ (2005) Diet
and functional gastrointestinal disorders: a population-based case-control study.
Am J Gastroenterol 100: 2743–2748.
41. Camilleri M, Lasch K, Zhou W (2012) Irritable bowel syndrome: methods,
mechanisms, and pathophysiology. The confluence of increased permeability,
inflammation, and pain in irritable bowel syndrome. Am J Physiol Gastrointest
Liver Physiol 303: G775–785.
42. Simren M, Abrahamsson H, Bjornsson ES (2007) Lipid-induced colonic
hypersensitivity in the irritable bowel syndrome: the role of bowel habit, sex,
and psychologic factors. Clin Gastroenterol Hepatol 5: 201–208.
43. Ghoshal UC, Shukla R, Ghoshal U, Gwee KA, Ng SC, et al. (2012) The gut
microbiota and irritable bowel syndrome: friend or foe? Int J Inflam 2012:
151085.
44. Xiao S, Fei N, Pang X, Shen J, Wang L, et al. (2013) A gut microbiota-targeted
dietary intervention for amelioration of chronic inflammation underlying
metabolic syndrome. FEMS Microbiol Ecol: (in press. doi: 10.1111/1574–
6941.12228).
45. D’Aversa F, Tortora A, Ianiro G, Ponziani FR, Annicchiarico BE, et al. (2013)
Gut microbiota and metabolic syndrome. Intern Emerg Med 8 Suppl 1: S11–15.
46. Gulcan E, Taser F, Toker A, Korkmaz U, Alcelik A (2009) Increased frequency
of prediabetes in patients with irritable bowel syndrome. Am J Med Sci 338:
116–119.
47. Shimazu T, Kuriyama S, Hozaw a A, Ohmori K, Sato Y, et al. (2007) Dietary
patterns and cardiovascular disease mortality in Japan: a prospective cohort
study. Int J Epidemiol 36: 600–609.
Irritable Bowel Syndrome & Metabolic Syndrome
PLOS ONE | www.plosone.org 6 November 2014 | Volume 9 | Issue 11 | e112289
