High smoking cessation rate in Crohn`s disease patients after

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High smoking cessation rate in Crohn`s disease patients after
Journal of Crohn's and Colitis (2013) 7, 202–207
Available online at www.sciencedirect.com
High smoking cessation rate in Crohn's disease
patients after physician advice – The
TABACROHN Study☆
Tiago Nunes a,1,2 , Maria Josefina Etchevers a,1,2 , Olga Merino b ,
Sonia Gallego c , Valle García-Sánchez d , Ignacio Marín-Jiménez e ,
Luis Menchén e , Manuel Barreiro-de Acosta f , Guillermo Bastida g,2 ,
Sara García h , Elena Gento h , Daniel Ginard i , Eva Martí i ,
Fernando Gomollón j , Maite Arroyo j , David Monfort k ,
Esther García-Planella l , Benito Gonzalez m , Carme Loras n , Carles Agustí a,2 ,
Carolina Figueroa a,2 , Miquel Sans a,⁎,2
for the TABACROHN Study Group of GETECCU 3
a
Hospital Clinic/IDIBAPS, Barcelona, Spain
Hospital de Cruces, Barakaldo, Spain
c
Hospital Miguel Servet, Zaragoza, Spain
d
Hospital Reina Sofia, Córdoba, Spain
e
Hospital Gregorio Marañón, Madrid, Spain
f
Hospital Clinico Universitario, Santiago de Compostela, Spain
g
Hospital La Fe, Valencia, Spain
h
Hospital General Yague, Burgos, Spain
i
Hospital Universitario Son Espases, Palma de Mallorca, Spain
j
Hospital Clinico, Zaragoza, Spain
k
Consorci Sanitari de Terrassa, Terrassa, Spain
l
Hospital Sant Pau, Barcelona, Spain
m
Hospital Juan Canalejo, A Coruña, Spain
n
Hospital Mutua de Terrassa, Terrassa, Spain
b
Abbreviations: CD, Crohn's disease; UC, Ulcerative colitis; IBD, Inflammatory bowel disease.
Specific author contributions: Tiago Nunes, Maria Josefina Etchevers and Miquel Sans wrote the original manuscript. Tiago Nunes and
Miquel Sans performed all statistical analysis. Olga Merino, Sonia Gallego, Valle García-Sánchez, Ignacio Marín-Jiménez, Luis Menchén, Manuel
Barreiro-de Acosta, Guillermo Bastida, Sara García, Elena Gento, Daniel Ginard, Fernando Gomollón, Maite Arroyo, David Monfort, Eva Martí,
Esther García, Benito Gonzalez, Carme Loras, Carles Agustí and Carolina Figueroa contributed to patient inclusion, data collection, literature
review and original manuscript correction. All authors have approved the final draft.
⁎ Corresponding author at: Department of Gastroenterology, Hospital Clínic i Provincial / IDIBAPS, 170 Villarroel, 08036 Barcelona, Spain.
Tel.: +34 649189146; fax: +34 93 2279387.
E-mail address: [email protected] (M. Sans).
1
Both authors have equally contributed to this work.
2
CIBEREHD: Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas.
3
Spanish Working Group in Crohn's Disease and Ulcerative Colitis.
☆
1873-9946/$ - see front matter © 2012 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.crohns.2012.04.011
High smoking cessation rate in Crohn's disease patients after intensive counseling
203
Received 10 February 2012; received in revised form 24 April 2012; accepted 24 April 2012
KEYWORD
Inflammatory bowel
disease;
Crohn's disease;
Environmental factors;
Smoking;
Tobacco;
Smoking cessation
Abstract
Introduction: Tobacco smoking has a significant impact on the development of Crohn's disease
(CD) and its clinical course, making smoking cessation one of the main goals in CD therapeutic
strategy.
Aims: To evaluate the effectiveness of an advice-based smoking cessation strategy among CD
patients.
Methods: We have performed a prospective multicenter study which enrolled 408 CD smokers.
At inclusion all patients were instructed about the risks of smoking and subsequently followed
every 3 months. Each center used additional smoking cessation strategies based on available
resources. Urinary cotinine and exhaled carbon monoxide levels were evaluated in a subgroup of
patients.
Results: Median study follow up was 18 months. 31% of the patients achieved complete smoking
cessation and 23% were smoking-free at the end of their follow up with 8% of smoking relapse.
Most patients not achieving smoking cessation did not change their smoking habit with only 5%
presenting a decrease in tobacco load. 63% of patients willing to quit smoking received help from
another specialist, most frequently the pulmonologist (47%). Surprisingly, most patients (88%)
tried to quit smoking with no pharmacological therapy and bupropion, varenicline and nicotine
replacement treatment were used in few patients. Urinary cotinine and exhaled CO levels tested
in a subgroup of patients proved to have a good correlation with the self-reported smoking habit.
No predictors of successful smoking cessation were identified.
Conclusion: Our results underline that an anti-tobacco strategy mostly based on CD patients´s
education and counseling is feasible and effective in helping patients reach complete abstinence.
© 2012 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.
1. Introduction
Crohn's disease (CD) is a complex polygenic immune-mediated
intestinal illness that develops in genetically susceptible
individuals exposed to a number of environmental factors. 1–3
Tobacco smoking is the most studied and better characterized
of these factors, increasing CD predisposition and impacting
negatively on its clinical behavior. 4–9 In this regard, most of
the available data supports that smoking results in a higher
prevalence of stenosing and penetrating phonotype, perianal
disease, need for surgery and post-surgical recurrence in
smokers. 7–21 In addition, an increased need for steroids and
immunosuppressive treatment has been also linked to active
smoking. 7
Given the importance of tobacco smoking in CD pathogenesis, it is remarkable the low number of studies evaluating the
usefulness of smoking cessation strategies in this specific
scenario. Hilsden and coworkers in a cross-sectional questionnaire based study found that CD patients seem to be no
more refractory to smoking cessation when compared to the
general population. 22 Nevertheless, it has also been shown
that smoking cessation rates at and after diagnosis are
identical between CD and ulcerative colitis (UC) patients,
suggesting that many patients are still not aware of the
relationship between tobacco and their condition. 23
In the only available prospective study evaluating the
impact of smoking cessation on CD clinical course, Cosnes
and coworkers managed to achieve a smoking cessation rate
(patients who stopped smoking for more than 15 days) of 25%
with only 12% remaining abstinent for more than 1 year. 24
Additional studies specifically designed to evaluate smoking
cessation in CD patients are needed to provide evidencebased cessation strategies. The aim of this study was to
prospectively evaluate the effectiveness of a multicenter
anti-tobacco strategy based mostly on physician advice and
counseling in CD patients attending referral inflammatory
bowel disease units in Spain.
2. Materials and methods
2.1. Study design and inclusion criteria
Detailed information on the different anti-tobacco strategies
and response to smoking cessation was collected from the
ongoing multicenter prospective interventional study Tabacrohn. The Tabacrohn Study was designed and is supported by
the Spanish Working Group in Crohn's Disease and Ulcerative
Colitis (GETECCU) and primarily aims at evaluating the longterm impact of smoking cessation on CD clinical activity and
complications. This study currently takes place in 14 Spanish IBD
units and presents a current median follow-up of 18 months.
During a six-month inclusion period, 1217 consecutive
patients with established diagnosis of CD presenting varied
smoking exposure status (non, active and former smokers)
were evaluated and 420 active smokers were enrolled in the
anti-tobacco strategy. Smoking habits were determined
using the classification previously established by Cosnes. 8
204
Patients were classified as active smokers if they were
smoking at inclusion and had smoked more than seven
cigarettes per week for at least 6 months.
2.2. Smoking cessation and follow-up
At inclusion, all active smokers were instructed by their
gastroenterologist about the known relationship between
tobacco consumption and CD clinical course with detailed
information on the deleterious effects of smoking and the
potential benefits of smoking cessation. A specifically designed
graphic material summarizing that information was given to all
individuals. Patients were subsequently invited to try to quit
smoking and were followed every 3 months, regardless of
initial smoking cessation acceptance. In the following visits,
the smoking habit was checked by patients' self-report and the
smoking cessation strategy was individualized at each center
according to their current clinical practice and resource
availability. In that regard, each participating center determined the need for referral to smoking cessation units,
participation of other professionals (psychologists, pulmonologists, otorrynologists or general practitioners) and the use of
pharmacological therapy. Urinary cotinine and exhaled carbon
monoxide were assessed to evaluate the correlation between
these cessation biomarkers and the self-reported smoking
status at the coordinating center (Hospital Clinic Barcelona).
Patients were divided into two groups according to cessation outcome: quitters and non-quitters. The non-quitter group
included patients who failed to achieve complete tobacco
abstinence including those who decreased their tobacco
consumption without quitting and those who did not change
their smoking habit at all. Quitters were considered patients
who self-reported being completely smoking-free for at least
1 week. This group was further subdivided into continuing
quitters (the ones who were still smoking-free at the last
follow-up visit) and the relapse group (patients who resumed
smoking). Patients that did not accept to try to quit smoking
were considered as non-quitters with no change in smoking
habit.
2.3. Data collection
Data including demographics, disease characteristics, current treatment and previous and present smoking habits was
collected at outpatient visits and from clinical records.
Disease location and behavior were categorized according to
the Montreal Classification.
T. Nunes et al.
deviation. Fisher and Chi-square tests were used to compare
qualitative variables. The Student's t was used to compare
quantitative variables. All tests were two-tailed with a significance level set at b 0.05. To determine predictors for a
successful smoking cessation in CD patients, a logistic regression model was constructed. Multiplicative interaction between
possible predictors and the outcome (complete abstinence)
was assessed. Age, gender, tobacco load in pack year, disease
duration, location, complicated phenotype (structuring or
penetrating), perianal disease, surgery and disease activity
were analyzed separately for complete abstinence. For discrete
variables, results were calculated and compared by χ 2 or exact
tests. Odds ratios, tests of significance, and 95% confidence
intervals (CIs) were calculated. The Student's t-test (for normal
data) or the Wilcoxon rank-sum test were used for continuous
variables. Variables achieving a p value of less than 0.1 were
selected and subsequently included in the multivariate analysis. Following adjustment for all confounding variables, a
p b 0.05 was considered significant.
3. Results
3.1. Tabacrohn study population
420 current smokers were included in the Tabacrohn study.
Twelve patients were subsequently excluded due to lack of data
regarding their smoking status, leaving 408 eligible patients for
further analysis. At inclusion, patients presented a median
tobacco load of 13 pack year. The median study follow-up was
18 months. Additional information regarding gender, age,
disease duration, CD phenotype and medical treatment is
summarized in Table 1.
3.2. Cessation acceptance and outcome
Within the median 18-month follow-up, 62% of the studied
population accepted to attempt to quit smoking with most of
them (56% of all patients) accepting it at inclusion. The
remaining 38% did not accept to attempt to quit at any time
during the current follow-up. The overall smoking cessation
rate (patients who managed to quit smoking) was 31% (128 of
408 patients) with 23% (95 of 408 patients) remaining
smoking-free until the end of the follow-up and 8% of
relapse rate (33 of 408 patients). In the other hand, 69% (280
of 408 patients) failed to quit smoking and most non-quitters
did not change their smoking habit with only 5% (19 of 408
patients) presenting decrease in tobacco load (Fig. 1).
2.4. Ethics and support
The Tabacrohn Study was designed and supported by the
Spanish Working Group in Crohn's Disease and Ulcerative Colitis
(GETECCU). The study was approved by the Ethics Committee
of Hospital Clinic i Provincial of Barcelona, Spain. All data was
anonymously analyzed to preserve patient's confidentiality.
2.5. Statistical analysis
Qualitative variables were expressed using frequencies. Continuous variables were expressed using mean and standard
3.3. Population characteristics with respect to
smoking habit and smoking cessation predictors
Non-quitters presented longer disease duration when compared to quitters. Quitters presented the lowest surgery rate
between both groups. No other detectable differences were
found between quitters and non-quitters, including disease
activity and phenotype (Table 1). Only disease duration, surgery and tobacco load in pack year reached the cut-off p-value
of ≤0.1 to enter the logistic regression model evaluating
possible independent predictive factors of complete
High smoking cessation rate in Crohn's disease patients after intensive counseling
Table 1 Population characteristics according to the smoking
habit including median with its related interquatile range in
case of numerical variables and absolute number with
percentage in case of categorical outcomes. Variables
presenting statistical significant differences (p-value b 0.05)
between non-quitters and quitters are marked with (*).
Characteristics
Male
Age (years)
Cigarettes (units)
Tobacco load
(pack year)
Disease duration⁎
Median (interquartile range) / N (%)
Non-quitters Quitters
Total
134 (48%)
41 (33–49)
15 (10–20)
13 (7–26)
198 (49%)
41 (48–32)
15 (10–20)
13 (6–25)
96 (48–144)
(months)
Familial IBD
30 (11%)
Ileal disease
95 (34%)
Colonic disease
52 (19%)
Ileocolonic disease 121 (43%)
Upper GI disease
18 (6%)
Complicated
116 (41%)
phenotype
Perianal disease
82 (29%)
Surgery⁎
118 (42%)
Disease activity
81 (29%)
during follow-up
Immunosuppressant 166 (59%)
Biologic
111 (40%)
64
40
10
11
(50%)
(32–47)
(10–20)
(5–22)
61 (24–132)
10
53
21
48
9
57
84 (36–136)
(8%)
(41%)
(16%)
(38%)
(7%)
(45%)
40 (10%)
148 (36%)
73 (18%)
169 (41%)
27 (7%)
173 (42%)
29 (23%)
37 (29%)
32 (25%)
111 (27%)
155 (38%)
113 (28%)
69 (54%)
42 (33%)
235 (58%)
153 (38%)
abstinence; however none of them reached statistical significance in the multivariate analysis.
3.4. Quitters: Time to quit, time without smoking
and time to relapse
Most patients quit in the first 6 months (70%) with a overall
median time of 6 months to achieve complete cessation
(3–9 months of interquatile range). The median smokingfree time was 9 months of complete abstinence (1.5–
15 months of interquatile range) with 33% of the patients in
cessation spending more than 1 year without smoking. Most
patients who fail to continue smoking cessation resume
205
smoking after a few months of quitting with median of
6 months to relapse (3–11 of interquatile range).
3.5. The cessation strategy
63% of the patients willing to quit smoking received help
from a non-gastroenterologist expert, most frequently, the
pulmonologist (Fig. 2). Of note, most patients tried to quit
smoking without receiving pharmacological therapy. As the
smoking cessation strategy was individualized taking into
consideration each center's clinical practice and resource
availability, patients under pharmacological treatment were
only found in 6 IBD units. Bupropion, varenicline and nicotine
replacement treatment were used in few patients (Fig. 2).
Urinary cotinine and exhaled CO levels were assessed in a
subgroup of patient at the study coordinator center. Both
parameters had a good correlation with the self-reported
smoking habit, as shown in Table 2.
4. Discussion
Tobacco smoking is the most established environmental
factor associated not only with CD development 25–28 but
also with a poor clinical outcome. 7–21 Nevertheless, very
few studies have assessed the effectiveness of a smoking
cessation strategy in this specific population. In fact, more
than ten years after the pivotal study performed by Cosnes
and coworkers, 24 no other prospective study assessing
smoking cessation in CD has been performed.
Conversely to the notion that CD patients are especially
refractory to smoking cessation, 31% of the patients were
able to quit smoking and 23% remained smoking-free for a
median follow-up period of 9 months. Our results are slightly
superior to the 25% of overall cessation and 12% of 1-year
sustained abstinence reported in the previous single-center
study. 24 In any case, both studies have found fine cessation
rates which underlines that CD patients are at least as
responsive to smoking cessation as the general population.
These results suggest that most CD smokers are willing to
attempt to quit smoking after being invited to do so by their
physician. In this regard, many patients permanently quit
after they experience the consequences of smoking which
underlines the function of smoking-related diseases as an
important trigger for smoking cessation. 29–31 In the specific
context of CD, the role of the gastroenterologist is very
Figure 1 Chart flow indicating the population classification according to smoking cessation outcome with number of patients (n)
and percentages [%] related to the total population.
206
T. Nunes et al.
Figure 2 A) Professionals involved in smoking cessation and
B) Pharmacological treatment. GP: general practitioner; ORL:
otorhinolaryngologist; GI: gastroenterologist.
important to clearly establish the link between smoking and
poorer clinical outcomes since the negative impact of
smoking on CD is less well known than in lung or heart
diseases.
Table 2 Correlation between self-reported smoking habit
and the biomarkers urinary cotinine and exhaled carbon
monoxide. Sensitivity, specificity, the positive and negative
predictive values and accuracy of self-reported smoking
status in comparison to either exhaled carbon monoxide
or urinary cotinine. PPV: positive predictive value; NPV:
negative predictive value; Se: sensitivity; Sp: specificity; A:
accuracy.
Status
Positive Negative PPV NPV Se
CO level CO level
Smokers
19
Non-smokers 2
Total
21
4
73
77
6
23
29
A
83% 97% 90% 95% 94%
Positive Negative PPV NPV Se
cotinine cotinine
level
level
Smokers
76
Non-smokers 3
Total
79
Sp
Sp
A
93% 88% 96% 79% 91%
Our cessation results might suggest that many patients
were unaware of the detrimental effects of tobacco, even
though prior knowledge about this important environmental
factor was not measured at inclusion. As previous studies
have shown, there is still an important lack of knowledge
among CD patients about the consequences of smoking. 23 In
this regard, in one large population-based study, patients
presenting tobacco-related diseases were no more likely
to have been advised to quit smoking than smokers in
general. 32 In addition, most smokers did not perceive
physicians to be involved in their efforts to quit smoking.
Considering the deleterious influence of tobacco on CD
natural history, physicians should increase their efforts in
properly advising smokers to quit, especially in the case of
patients with complicated phenotype or poor response to CD
therapy.
Biochemical validation has been used in some studies to
determine if participants have been smoking. 24 However,
urinary cotinine and exhaled carbon monoxide levels are not
used in most centers in clinical practice. In keeping with
previous reports, measurement of urinary cotinine and
exhaled carbon monoxide in a subgroup of patients demonstrated that both parameters have an excellent correlation
with self-reported smoking habit. 24 These results suggest that
self-reported smoking status is reliable to define tobacco
consumption in CD clinical setting.
In smoking cessation, it is well established that a longer
follow-up with multiple visits are preferred to a short-time
follow-up, with 3 and 6 months emerging as a recommended
standard to use in study interventions. 33 In the latest Cochrane
review evaluating the role of physician advice in smoking
cessation, all included trials assessed smoking status six
months after the intervention with almost 70% of the studies
presenting a longer follow-up period, typically around one
year. 33 Currently, our patients are far beyond the 6-month
mark, presenting a median follow-up of 18 months since
study inclusion and a median of 9 months of smoking-free
follow-up.
Two thirds of the patients willing to quit smoking received
help from another professional, however, no differences with
respect to smoking cessation outcome were observed when
these professionals were compared. Surprisingly, bupropion,
varenicline and nicotine replacement treatment were used in
very few patients indicating that most patients tried to quit
smoking with no pharmacological therapy. The fact that, in
Spain, anti-tobacco therapies are expensive and not currently
covered by the public health system could partly account for
the low rate of drug use in this population. Our cessation
results in the light of this lack of pharmacological therapy
underlines the importance of the anti-tobacco counseling and
the patient–physician relationship in CD smoking cessation.
In conclusion, smokers followed at IBD units undergoing
smoking cessation present impressive acceptance and good
quitting rates. In our clinical practice, several different
professionals participate in the smoking cessation process
but most patients do not use pharmacological therapy. Our
results underline that an anti-tobacco strategy mostly based
on patients' education and counseling is feasible and effective
in helping patients reach complete abstinence. All active CD
smokers should be offered detailed information and assistance
to decrease their tobacco consumption and, ideally, achieve
full smoking cessation.
High smoking cessation rate in Crohn's disease patients after intensive counseling
Conflict of interest statement
No conflicts of interest.
Acknowledgement
This worh has been partially funded by Fundació Miarnau.
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