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doi: 10.1111/nmo.12556
& F. ROESCH-DIETLEN *
*Digestive Physiology and Gastrointestinal Motility Laboratory, Instituto de Investigaciones Medico Biol
ogicas, Universidad
Veracruzana, Veracruz, Mexico
Department of Internal Medicine, Hospital Regional de Alta Especialidad de Veracruz, Veracruz, Mexico
Key Messages
Situations with a high emotional burden, such as sexual abuse and posttraumatic stress disorders have been
associated with IBS, and have even been regarded as triggering factors.
Recent studies have shown that providing long-term care for the chronically ill patient can have a negative
impact, both mentally and physically, on caregivers.
This is the first study showing that caregivers of chronically ill patients have a high prevalence (49%) of IBS,
and a greater probability of presenting with depression, anxiety, and a worse quality of life.
Caregiving that involves chronically ill patients should be regarded as another condition associated with IBS.
Abstract
Background Caregivers are an at-risk population for
psychic and physical diseases such as irritable bowel
syndrome (IBS). However, it is not known whether
providing care for the chronically ill patient can be
considered a risk factor for developing IBS. In this
study, our aim was to evaluate the prevalence of IBS
according to the Rome II criteria in a group of
caregivers. Methods A cross-sectional study was conducted through an evaluation of caregivers of chronically ill patients. Subjects completed questionnaires
including the Rome II Modular Questionnaire, the
Hospital Anxiety and Depression Scale, the Zarit
Caregiver Burden Interview (ZCBI) (an instrument
for evaluating the burden experienced by caregivers),
and the irritable bowel syndrome quality of life (IBSQoL) questionnaire. Key Results Ninety-six primary
INTRODUCTION
J. M. Remes-Troche et al.
METHODS
Population
A cross-sectional study was conducted through an evaluation of
caregivers of chronically ill patients, carried out at the Department of Internal Medicine of the Hospital Regional de Alta
Especialidad de Veracruz and the Institute of Medical and
Biological Research of the Universidad Veracruzana in the Mexican city of Veracruz and the state of the same name, within the
time frame of 1 April 2009 and 31 May 2010.
Consecutive caregivers were invited to voluntarily participate
in the study. The primary caregivers of patients with chronic
degenerative diseases that lived in the patients home and did not
receive remuneration for their activity of providing care were
included. Temporary caregivers were excluded, as were those that
presented with any type of degenerative disease, such as diabetes
mellitus, chronic kidney disease, primary neurologic diseases, and
rheumatologic diseases.
After receiving an explanation of the study protocol and signing
statements of informed consent, all the subjects underwent:
1. An analysis of sociodemographic characteristics: the information pertaining to age, civil status, and occupation of the
subjects, together with the characteristics of the patients they
were caring for, was gathered through a data collection tool.
2. Application of the validated Spanish version of the Rome II
Modular Questionnaire25: this instrument was applied to all
the subjects through direct interview to determine the presence of IBS and its subtypes (IBS with constipation [IBS-C], IBS
with diarrhea [IBS-D], and mixed IBS [IBS-M]). All subjects were
specifically investigated if they had presented with symptoms
consistent with IBS before providing care for their chronically
ill patient.
3. Evaluation of anxiety and depression: all the subjects answered
the self-rating version of the Hospital Anxiety and Depression
Scale questionnaire, an instrument used in the evaluation of
anxiety and depression in situations of stress, which has been
validated in the Mexican population.26 This questionnaire
consists of 14 questions, divided into two subscales of seven
questions each; one subscale measures anxiety in accordance
with the Hamilton scale and the other evaluates depression
based on anhedonia and lack of pleasure. The intensity or
frequency of each answer is evaluated through a Likert scale
(03), with each total subscale score ranging from a possible 0
to 21; a score of 07 is considered normal, 810 inconclusive,
and more than 10 is indicative of significant anxiety and
depression.
4. The Zarit Caregiver Burden Interview (ZCBI)2123 is an instrument for evaluating the burden experienced by caregivers. It
consists of a total of 22 questions that are graded on a Likert
scale (04). The score range is from 0 to 88, and a higher score
indicates a greater burden. A score of 021 is considered null or
minimum burden, 2140 is regarded as moderate burden, 4160
is moderate to severe burden, and a score above 61 represents
severe burden. The questions evaluate three domains: (i)
consequences of care, (ii) interpersonal relation, and (iii) selfefficacy expectations. Caregiver stress syndrome was defined if
subjects had a ZCBI score >21.
5. Quality of life was evaluated through the Spanish version of
the IBS-QoL questionnaire27; it includes a global evaluation
Statistical analysis
The nominal variables were described through absolute and
relative frequencies. The continuous variables were analyzed
using means and standard deviation or medians and ranges,
depending on their distribution. A comparative analysis was
carried out between the caregivers that presented with IBS and
those that did not. The Students t-test or MannWhitney U-test
was used for the comparison of two continuous variables, when
appropriate, and the chi-squared test or Fisher exact test was used
for comparing the proportions between two groups, when appropriate. A logistic regression analysis was also performed to look at
the relative effects of the independent variables (age, gender,
occupation, civil status, home setting, length of time taking care
of the patient, level of burden, and Zarit score) on IBS (dependent
variable, yes/no) in the population. Statistical significance was set
at a p < 0.05. The statistical analysis was performed using the
SPSS version 10.0 (SPSS, Inc., Chicago, IL, USA) program. This
study and its protocol and the statements of informed consent
were reviewed by the institutional Research and Ethics Committee, following the bioethical principles of good clinical practice.
RESULTS
Demographic characteristics
Ninety-six primary caregivers with a mean age of
43.6 13.7 years were evaluated; 87% (n = 84) of
them were women. The mean length of time providing
care was 37.6 months (range: 3288 months). Table 1
shows the caregivers relation to their patients, occupation, and civil status.
Caregivers
with IBS
(n = 47)
Caregivers
without IBS
(n = 49)
44 (92%)
42 14
32 63
40 (81%)
44 13
37 17
47 12
28 8
0.0001*
25.3 9.6
18.4 9.1
0.004*
4.6 1
4.1 2.3
0.02*
8.2 2.8
6.1 2
0.003*
78 18
87 17
0.01*
11.2 4.6
7.5 4.4
0.0001*
9.5 4.5
7.2 3.8
0.008*
30
22
21
10
10
03
(31.2)
(22.9)
(21.0)
(10.0)
(10.0)
(03.1)
72
15
06
03
(75.0)
(15.6)
(06.2)
(03.1)
Gender
Female (n, %)
Age, years (mean SD)
Length of time taking
care of the patient,
months (mean SD)
Global Zarit Score
(mean SD)
Consequences of
care domain
Interpersonal
relation domain
Self-efficacy
expectation domain
Global IBS-QoL
Score (mean SD)
Anxiety Score
(mean SD)
Depression Score
(mean SD)
59 (61.4)
21 (20.8)
15 (05.2)
62 (64.5)
34 (35.4)
p-value
n (%)
0.02
0.46
0.23
J. M. Remes-Troche et al.
22
19
6
2
(45%)
(39%)
(12%)
(4%)
5
17
23
2
(11%)
(36%)
(49%)
(4%)
100
80
40
p-value
0.0001*
20
No burden
Mild burden
Moderate burden
Severe burden
IBS (n = 47)
60
r = 0.60, p = 0.001
30
40
50
60
70
Zarit score
80
90
10
Gender
Men (n, %)
Women (n, %)
Age (mean SD)
IBS (n, %)
Civil status (n, %)
Single
Married
Divorced
Widowed
Occupation (n, %)
Homemaker
Employee
Unemployed
Cared-for patient
pathologies (n, %)
Chronic kidney
disease
Cancer
Chronic kidney
disease and diabetes
Neurologic diseases
End-stage AIDS
Anxiety
15
20
r = 0.67, p = 0.001
30
40
50
60
70
Zarit score
80
90
20
r = 0.58 p = 0.01
Subjects with
caregiver stress
syndrome
(n = 69)
Subjects without
caregiver stress
syndrome
(n = 27)
10 (14%)
59 (86%)
43.02 11
42 (61%)
2 (7%)
25 (93%)
44.07 13.2
5 (18%)
11
52
3
3
p-value
0.34
0.73
0.001*
(16%)
(76%)
(4%)
(4%)
4 (15%)
20 (74%)
0
3 (11%)
0.89
0.89
0.27
0.21
41 (59%)
16 (23%)
12 (18%)
18 (66%)
5 (18%)
4 (14%)
0.51
0.61
0.76
32 (46%)
12 (44%)
0.86
12 (17%)
7 (10%)
7 (26%)
4 (15%)
0.34
0.51
15 (22%)
3 (4%)
3 (11%)
1 (4%)
0.23
0.88
10
DISCUSSION
This study is the first to report the prevalence of IBS in
caregivers of patients with a chronic disease. Caregiving is an activity that causes stress (physical and
psychological) in a population that is highly susceptible to the development of psychosocial disorders.
According to Zarit et al.,28 caregiving burden is defined
as: The extent to which caregivers perceive that
caregiving has had an adverse effect on their emotional,
social, financial, physical, and spiritual functioning.
This definition emphasizes the multidimensional toll
caregiving may exact on care providers and also the fact
that caregiving is an individualized experience.29 Risk
factors for caregiver burden include female gender, low
educational attainment, residing with the care recipient, depression, social isolation, financial stress, higher
number of hours spent caregiving, and lack of choice in
being a caregiver.30
In accordance with the Rome II criteria, in our study,
close to 50% of the subjects taking care of a chronically
Depression
15
10
20
30
40
50
60
70
Zarit score
Figure 4 Positive correlation between the Zarit (burden) and
depression (HAD) scores.
J. M. Remes-Troche et al.
ACKNOWLEDGMENT
control group, prevalence of other functional GI disorders, chronic pain disorders, and psychological disorders in the group with IBS before starting their
caregiving duties, and afterwards. In addition, it is
not known if the IBS symptoms of the caregivers could
be representative of another condition, such as celiac
disease or food intolerances. The study subjects were
recruited at referral centers from different localities,
and from diverse socioeconomic strata, making it
difficult to include an adequate control group. Even
though it appears that the majority of the caregivers
developed symptoms starting from the time they began
to take care of the chronically ill patient, there was an
obvious recall bias that was difficult to eliminate. It is
also important to mention that IBS QoL is a diseasespecific questionnaire, thus non-IBS subjects would be
expected to have lower scores. Finally, despite the fact
that we did not employ a scale for evaluating IBS
severity, we used anxiety and depression scales as
subrogates of more severe disease.
In conclusion, this is the first study showing that
caregivers of chronically ill patients have a high
prevalence (49%) of IBS, which is associated with
depression, anxiety, and poor quality of life. This
association is novel and should be regarded as another
psychological condition associated with IBS.
REFERENCES
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FUNDING
This study was funded by an internal grant from the Medical
Biological Research Institute, Universidad Veracruzana, Veracruz,
Mexico.
CONFLICTS OF INTEREST
Jos
e Mara Remes-Troche is a member of the Advisory Counsel
for Takeda Pharmaceuticals, Alfa-Wassermann, Almirall, and
Janssen. He has been a speaker for Nycomed- Takeda, Advance
Medical, Endomedica, Astra-Zeneca, and Bristol-Myers-Squibb.
He has received research funding from Sanofi-Pasteur, Asofarma,
and Astra Zeneca. M Torres- Aguilera, V Montes-Martnez, VA
Jimen
ez-Garca, and F Roesch-Dietlen do not have any conflict of
interest.
AUTHOR CONTRIBUTION
JMR-T contributed to the planning and/or the conducting of the
study, interpreting data, and drafting the manuscript; MT-A, VMM, and VAJ-G contributed to the conducting of the study and to
interpreting data; FR-D contributed to the conducting and drafting
of the manuscript. All authors have approved the final draft
submitted.
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