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Attitudes toward smoking and smoking behaviors of patients with crohn’s disease
THE AMERICAN JOURNAL OF GASTROENTEROLOGY © 2001 by Am. Coll. of Gastroenterology Published by Elsevier Science Inc.
Vol. 96, No. 6, 2001 ISSN 0002-9270/01/$20.00 PII S0002-9270(01)02445-5
Attitudes Toward Smoking and Smoking Behaviors of Patients With Crohn’s Disease Robert J. Hilsden, M.D., M.Sc., F.R.C.P.C., David Hodgins, Ph.D., Diana Czechowsky, Marja J. Verhoef, Ph.D., and Lloyd R. Sutherland, M.D.C.M., M.Sc., F.R.C.P.C. Departments of Medicine, Psychiatry, and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada
OBJECTIVE: To examine the smoking behaviors of people with Crohn’s disease. In active smokers, we measured their willingness to quit, their degree of nicotine dependence, and the proportion that made a quit attempt within 6 months to determine if they were refractory to smoking cessation in comparison to the general population. We also examined factors that were important in their decision to smoke. METHODS: We conducted a cross-sectional survey of outpatients, supplemented by telephone interviews and a 6-month follow-up questionnaire of active smokers. Measures included disease activity, current smoking behaviors, intentions (stage of change), Fagerstrom Test for Nicotine Dependence, and factors related to their decision to smoke (decisional balance). RESULTS: The questionnaire was completed by 115 patients (78% response rate). Forty percent were active smokers. Of active smokers, 59% were considering quitting within the next 6 months, and of these, 15% were planning on quitting within the next 30 days. Those with moderate disease activity were more likely to be considering quitting than those with mild or severe activity. Nicotine dependence was rated as high in 33% and as moderate in 43%. Factors unrelated to Crohn’s disease were more important in their decision to smoke than were Crohn’s disease-related factors. After 6 months, 23% had made an attempt to quit and this attempt was strongly associated with their stated intentions at the baseline questionnaire. Two of three patients who had recently quit at baseline had resumed smoking. CONCLUSION: When compared to similar data for the general population, patients with Crohn’s disease are no more refractory to smoking cessation. (Am J Gastroenterol 2001; 96:1849 –1853. © 2001 by Am. Coll. of Gastroenterology)
pressive therapy, and development of fistulas (2–5). Furthermore, there is evidence that patients who successfully quit smoking have an improved disease course compared with those who continue to smoke. Cosnes et al. (6) found patients who quit smoking were less likely to suffer a flare-up of the disease, require corticosteroids, start immunosuppressive therapy, or require an increased dose of immunosuppressives. However, only 53 of 474 smokers (11%) in the study abstained from smoking 1 yr after receiving cessation counseling. Despite the evidence that smoking adversely affects the course of Crohn’s disease, standard gastroenterology and inflammatory bowel disease texts place little emphasis on smoking cessation as a potential therapy for Crohn’s disease. Furthermore, Shields and Low-Beer (7) reported that many patients were unaware of the risks of smoking on their Crohn’s disease and could not recall their physician ever telling them about these risks. Why don’t gastroenterologists put more effort into getting their patients to quit? One explanation may be that gastroenterologists view their patients as being refractory to quitting. As Cosnes et al. (6) stated, “CD patients are poorly receptive to smoking cessation advice.” However, is this true and are these patients any more refractory than average smokers? To explore this, we conducted a study with a group of Crohn’s disease patients attending gastroenterology outpatient clinics to determine whether they are refractory to smoking cessation. We determined (1) their willingness to quit (stage of change) (2), their degree of nicotine dependence (3), and the proportion of smokers who made a quit attempt within the subsequent 6 months. We also examined which factors are important in their decision to smoke, their beliefs about how smoking affects their disease, and their perceived barriers to smoking cessation.
INTRODUCTION There is a clear link between smoking tobacco and Crohn’s disease (CD). Smoking has been consistently shown to be a risk factor for the development of the disease (1). There is also a growing body of evidence that smoking also adversely affects the course of Crohn’s disease, in terms of the risk for recurrence or reoperation, the need for immunosup-
MATERIALS AND METHODS Study Design There were three components to this study. First, we conducted a cross-sectional survey of patients with Crohn’s disease using a mailed, structured questionnaire. Second, a subset of patients who were current smokers underwent a
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Table 1. Stages of Change Stage
Intention or Behavior
Precontemplation Contemplation
No intention to quit in next 6 mo Intends to quit in next 6 mo but not in next 30 days Intends to quit in next 30 days and has made quit attempt in past year Quit smoking within past 6 mo Quit smoking for more than 6 mo
Preparation Action Maintenance
telephone interview using structured and open-ended questions to further assess their beliefs about how smoking influences their disease and to find out what are their perceived barriers to smoking cessation. Third, all patients, who at the time of the survey indicated they were currently a smoker or who had quit within the previous 6 months, were sent a second questionnaire 6 months later to establish whether they had made an attempt to quit since receiving the first questionnaire. For both mailings, patients who did not respond within 3 wk of the date of mailing of the first questionnaire were sent a second questionnaire. The study was approved by the University of Calgary Conjoint Health Research Ethics Board (Calgary, Alberta, Canada). Patients Patients were recruited from the outpatient clinics of 10 gastroenterologists practicing in an academic or private practice setting in Calgary, Alberta, Canada from May to July 1998. Consecutive patients with documented Crohn’s disease were mailed a questionnaire within 10 days of their clinic visit. Instruments For the baseline assessment a structured questionnaire was created and pretested in a small group of patients. The questionnaire included items on basic demographic, disease, and treatment characteristics. Patient-rated disease activity was determined using a 7-point Likert scale ranging from one (inactive) to seven (terrible, bad as it ever gets). The questionnaire also included the following validated measures: stage of change, decisional balance, and Fagerstrom Test for Nicotine Dependence. Stage of change and decisional balance measures were obtained from the website of the creators’ institution, Cancer Prevention Research Center at the University of Rhode Island (http://www.uri.edu/research/cprc/). In addition, several questions were developed addressing attitudes toward and experiences with smoking cessation, and beliefs about the effects of smoking on Crohn’s disease. STAGE OF CHANGE. Smoking cessation is a process that occurs over a period of time. The Transtheoretical Model of Behavior Change describes how individuals changing addictive behaviors proceed through a series of stages (Table 1) (8). A respondent’s stage of change was ascertained by a discrete categorical measure, which assesses stage of change from a series of mutually exclusive questions.
DECISIONAL BALANCE. The decisional balance scale measures the importance of various factors in the decisionmaking process about smoking cessation and has been shown to predict subsequent smoking status (9). For this study, the short-form version of the scale was used. Each of the six items is responded to on a 5-point Likert scale. It incorporates two subscales identified as the pros of smoking and the cons of smoking. The pros include: smoking relieves tension, helps concentration, and relaxes (1–3). The cons include: smoking embarrasses, bothers other people, and makes people think the smoker is foolish for ignoring the warnings about cigarettes (1–3). The scores for each of the three items in the subscale are summed resulting in a total score from 3 to 15. The higher the subscale score, the greater the importance of that subscale in the patient’s decisionmaking process. DECISIONAL BALANCE—CROHN’S DISEASE. We created five additional items reflecting unique Crohn’s disease-related factors that we believed could potentially influence a patients decision to smoke. The structure of these items was similar to the general decisional balance scale. The new items included four “pros” and one “con.” The four pros were that smoking (1) helps the patient deal with abdominal pain (2), decreases appetite and helps the patient avoid eating when sick (3), reduces nausea (4), and is one of the few things that the patient can enjoy when sick. The con was that smoking makes the patient’s Crohn’s disease worse. The four pros items were summed to give a “Pros –CD” score from 4 to 20. FAGERSTROM TEST FOR NICOTINE DEPENDENCE (FTND). This six-item scale measures nicotine dependence on a range of scores from 0 to 10. Scores of 3–5 are indicative of moderate dependence and scores of ⬎5 of high dependence (10, 11). Reasonable test-retest reliability has been established over a 2-wk interval (Crohnbach’s alpha 0.64) (12). Validity has been demonstrated through multiple means, including correlation with biochemical measures of heaviness of smoking (10, 12). TELEPHONE INTERVIEW. Respondents who indicated in their returned questionnaire that they were willing to undergo a telephone interview were mailed a copy of the questionnaire to complete and were then interviewed by a trained research assistant. All those interviewed provided verbal consent at the time of the interview. The questionnaire focused on how patients believed smoking affected their Crohn’s disease, factors that they believed had prevented them from successfully quitting smoking in the past, and what kind of help they would like from their gastroenterologist to aid them to successfully quit in the future. All items were answered using a Likert scale. FOLLOW-UP QUESTIONNAIRE. The 6-month questionnaire included items on changes in disease and treatment
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Smoking and Crohn’s Disease
Table 2. Patient Characteristics Age, mean (range) Gender (F/M) Duration of disease, n (%) ⬍1 yr 1–5 yr ⬎5 yr Disease activity, n (%) Inactive/mild Moderate Very Education, n (%)* High school Post-secondary
38yr (19–77) 80/35 23 (20%) 23 (20%) 69 (60%) 44 (39%) 37 (32%) 33 (29%) 35 (31%) 79 (69%)
* One patient did not respond to this item.
characteristics, and whether the patient had attempted to quit smoking in the 6 months after the previous questionnaire. Data Analysis All questionnaires were coded into a computer database. Disease activity was divided into three categories: inactive/ mildly active, moderately active, and very active. Standard summary statistics were calculated. Associations between two variables were tested using a Fisher’s Exact Test. To determine whether the number of smokers in the study sample was greater than what would be expected in the general population, indirect standardization using age and sex-specific smoking prevalence rates for the Alberta general population were used with the calculation of a standard prevalence ratio of observed to expected cases along with a 95% CI.
RESULTS Subjects A questionnaire was sent to 147 patients and 115 (78%) responded. The characteristics of the study sample are shown in Table 2. Smoking Status Seventy-six respondents (66%) had smoked at some time and 46 (40%) were current smokers. The number of current smokers observed in the sample was 1.6 ⫻ what would have been expected based on the age- and sex-specific rates for the Alberta population (95% CI for observed/expected, 1.2– 2.1). Of those who had quit smoking, the majority (90%) had quit more than 6 months previously. Forty-five percent of women and 29% of men were current smokers (p ⫽ NS). Patients with at least some postsecondary education were less likely to be smokers than those whose highest level of education was a high school degree (33 vs 57%, p ⫽ 0. 022). Stage of Change Of the 46 current smokers, 19 (41%) were in the precontemplation stage, indicating they were not considering quitting smoking within the next 6 months (Table 3). Of the 27
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Table 3. Stage of Change and Nicotine Dependence of Current Smokers Stage of change Precontemplation Contemplation Preparation Nicotine dependence Low Moderate High
19 (41%) 20 (44%) 7 (15%) 11 (24%) 20 (43%) 15 (33%)
patients who were considering quitting in the next 6 months 20 (44% of all current smokers) were in the contemplation stage and seven (15%) were in the preparation stage. When stage of change was examined for each of the three disease activity levels, there was evidence that the proportion of patients in the precontemplation stage was not the same across categories of disease activity (p ⫽ 0.027). Ten patients (67%) who rated their disease as very active were in the precontemplation phase as compared with two (15%) and seven (39%) of those with moderately active and inactive/mildly active disease, respectively. Nicotine Dependence Twenty patients (43%) were rated as moderately dependent on nicotine and 15 patients (33%) were rated as highly dependent (Table 3). Seventeen of 19 patients (90%) in the precontemplation stage were at least moderately addicted to nicotine compared with 18 of 27 patients (67%) in the contemplation or preparation stages (p ⫽ 0.07). The majority of patients (70%) smoked 20 or fewer cigarettes per day. Fifty-five percent of current smokers had made at least one quit attempt that lasted more than 24 h in the previous year. Ten patients (21% of current smokers) had previously quit smoking for more than 6 months. Decisional Balance The median scores for the two subscales that examined the general pros and cons to smoking were both eight out of a maximum score of 15. Only one patient (2%) rated all three of the general pros to smoking as unimportant in their decision to smoke. In contrast, 13 patients (30%) rated all four of the Crohn’s disease-related pros to smoking as unimportant. Eighteen patients (40%) indicated the effect of smoking on their Crohn’s disease was not important in their decision to smoke. There was a trend for patients in the precontemplation stage to have higher scores on the general and Crohn’s disease-related pros to smoking and lower scores on the cons to smoking than those in the contemplation/preparation stages, but these did not reach statistical significance. The most important general pro to smoking was that smoking relieves tension, rated as at least very important by 48% of smokers. The most important general con to smoking was that smoking bothers others (37%).
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Telephone Interviews Thirty-three of the 46 (72%) current smokers completed a telephone interview. Fifteen respondents (45%) indicated smoking had no affect on diarrhea, fatigue, hunger, nausea, or pain from Crohn’s disease. Patients who believed smoking affected these symptoms were split between whether they believed they improved them or worsened them. For example, six patients believed smoking made their pain better, whereas three patients thought it made their pain worse. In contrast, eight patients thought it made their nausea worse and seven thought it made their diarrhea worse. Only three patients thought it improved their nausea and none thought it improved their diarrhea. Twenty-four patients (72%) had made an attempt to quit from the time when they were diagnosed with Crohn’s disease. Patients reported a variety of factors that they believed contributed to their lack of success. The most common one was the concern about gaining weight, reported by seven patients (21%). Six patients (18%) said increased Crohn’s disease symptoms while they were trying to quit were a factor. In an open-ended question that asked about barriers to successfully quitting, many patients mentioned the affects of smoking on stress or the increased stress while trying to quit. Only two patients (6%) mentioned lack of support from their family doctor or gastroenterologist as an important factor. Six Month Follow-Up Thirty-eight of the 49 patients (78%) who were current smokers or had recently quit smoking (⬍6 months) at the time of the first questionnaire completed a second questionnaire 6 months later. Eight of the current smokers (23%) had made an attempt to quit since the first questionnaire. Making an attempt to quit was strongly associated with stage of change at baseline. Only one of 16 (6%) of patients in the precontemplation stage had made a quit attempt compared with seven of 19 (37%) who were in the contemplation or preparation stage (p ⫽ 0.047). Two of the three recent patients who had recently quit at the time of the baseline questionnaire had resumed smoking.
DISCUSSION Given the growing evidence of the role that tobacco smoking plays in the course of Crohn’s disease, it is surprising that more attention has not been given to promoting smoking cessation in these patients. Rates of tobacco use are higher among patients with Crohn’s disease than among the general population (1), and the pattern was again present in our study sample. Forty percent of our sample were active smokers, which was 1.6 ⫻ what would have been expected based on age-sex specific smoking rates in the Alberta general population (13). The primary objective of this study was to determine whether patients with Crohn’s disease are refractory to smoking cessation. This has been suggested by other inves-
AJG – Vol. 96, No. 6, 2001
tigators (6) and could represent one reason why more effort has not been made to get these patients to quit. However, our results consistently failed to provide any evidence that patients with Crohn’s disease are any more refractory to smoking cessation than smokers in the general population. First, only 41% of patients were in the precontemplation stage (not considering quitting in the next 6 months). The distribution of the Crohn’s disease patients by stage of change was very similar to the distribution reported in several different groups of smokers in the general population (14). Second, most (67%) of the Crohn’s disease patients were not highly dependent on nicotine as measured with a validated instrument. The majority of patients smoked 20 or fewer cigarettes per day. Although there are no sound Canadian population norms for nicotine dependence, the patients in this study had similar levels of nicotine dependence as a representative sample of adults from the USA (15), and were less dependent than subjects in a smoking cessation trial (16) and hospitalized smokers (17). Third, approximately 25% of patients who were active smokers at the time of the first questionnaire made an attempt to quit in the subsequent 6 months. As expected, the likelihood of making an attempt to quit was associated with the patient’s stage of change at baseline, with those in the precontemplation stage being much less likely to make a quit attempt than those in a more advanced stage. Therefore, based on the distribution of patients within the stages of change, their measured nicotine dependence, and their actions over the subsequent 6 months, there is no evidence that this group was any more refractory to smoking cessation than smokers in the general population. Furthermore, nearly 40% of all patients who had ever regularly smoked tobacco had previously quit. Although we did not determine whether these patients had quit before or after the onset of their disease, the very fact that such a large proportion had quit and the majority had maintained long-term abstinence provides further evidence that patients with Crohn’s disease are not refractory to smoking cessation. Therefore, efforts to promote and assist in smoking cessation should be an important and consistent component of the management of patients with Crohn’s disease who smoke. However, similar to smokers in the general population, remaining abstinent is difficult for people with Crohn’s disease. Two of the three patients who had quit within 6 months of the baseline questionnaire had resumed smoking within the next 6 months. This study also addressed what factors were important in a patient’s decision to smoke and what factors patients perceived as preventing them from successfully remaining abstinent. Smoking cessation programs and education often address risks of smoking and the benefits of quitting. Within our sample, nondisease specific pros and cons of smoking appeared to be more important than ones related to Crohn’s disease. Concerns about weight gain and increased stress appeared to be the most important barriers to quitting. Some patients indicated that increased Crohn’s disease symptoms
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while attempting to quit led to a smoking relapse. However, there was no consistent pattern in the patients’ perceptions of how smoking affected their Crohn’s disease. This would suggest that a cessation program designed for smokers in the general population would not necessarily have to be significantly altered to accommodate those with Crohn’s disease. We had predicted that stage of change might be associated with Crohn’s disease activity, with less willingness to change in those with higher disease activity. We did find evidence that the distribution of patients by stage of change was not the same in each strata of disease activity, but a linear trend was not seen. The proportion of patients in the precontemplation stage was lowest in patients with moderate disease activity and higher in those whose disease was inactive or very active. We do not have a ready explanation for this finding. The possibility of a type 1 error must be considered. This finding remains to be confirmed and explained through further research on a large group of patients. We failed to find any evidence that people with Crohn’s disease are overly refractory to smoking cessation. Further research is required to develop and refine smoking cessation strategies appropriate for this patient group. However, given that Crohn’s disease-related factors were not found to be that important in patients’ decisions to smoke, it would seem that available strategies would be appropriate for use in this group. Given the widespread availability of pharmacological treatments and self-help information (18), all patients with Crohn’s disease who smoke should be offered help to quit.
ACKNOWLEDGMENTS Financial support has provided by Crohn’s and Colitis Foundation Canada Summer Studentship (D. C.) and Medical Research Council of Canada Fellowship (R. J. H.). R. J. H. is an Alberta Heritage Foundation for Medical Research Population Health investigator. Reprint requests and correspondence: Robert Hilsden, M.D., M.Sc., F.R.C.P.C., Department of Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta T2N 4N1, Canada. Received Nov. 21, 2000; accepted Jan. 25, 2001.
REFERENCES 1. Calkins BM. A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci 1989;34:1841–54.
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2. Lindberg E, Ja¨rnerot G, Huitfeltdt B. Smoking in Crohn’s disease. Effect on localisation and clinical course. Gut 1992; 33:779 – 82. 3. Cottone M, Rosselli M, Orlando A, et al. Smoking habits and recurrence in Crohn’s disease. Gastroenterology 1994;106: 643– 8. 4. Timmer A, Sutherland LR, Martin F, et al. Oral contraceptive use and smoking are risk factors for relapse in Crohn’s disease. Gastroenterology 1998;114:1143–50. 5. Russel MG, Nieman FH, Bergers JM, et al. Cigarette smoking and quality of life in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 1996;8:1075– 81. 6. Cosnes J, Beaugerie L, Carbonnel F, et al. Decreased severity of Crohn’s disease after smoking cessation. Preliminary results of a prospective intervention study. Gastroenterology 2000;118:A870. 7. Shields PL, Low-Beer TS. Patients’ awareness of adverse relation between Crohn’s disease and their smoking: Questionnaire survey. BMJ 1996;313:265– 6. 8. Prochaska JO, Velicer WF. The transtheoretical model of health behavior change. Am J Health Promot 1997;12:38 – 48. 9. Velicer WF, DiClemente CC, Prochaska JO, et al. Decisional balance measure for assessing and predicting smoking status. J Pers Soc Psychol 1985;48:1279 – 89. 10. Heatherton TF, Kozlowski LT, Frecker RC, et al. The Fagerstrom Test for Nicotine Dependence. A revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 1991;91:1119 – 27. 11. Leed-Kelly A, Russell KS, Bobo JK, et al. Feasibility of smoking cessation counseling by phone with alcohol treatment center graduates. J Subst Abuse Treat 1996;13:203–10. 12. Pomerleau CS, Carton SM, Lutzke ML, et al. Reliability of the Fagerstrom Tolerance Questionnaire and the Fagerstrom Test for Nicotine Dependence. Addict Behav 1994;19:33–9. 13. Statistics Canada. Health Statistics at a Glance. Ottawa: Industry, Science and Technology Canada, 1999. 14. Velicer WF, Fava JL, Prochaska JO, et al. Distribution of smokers by stage in three representative samples. Prev Med 1995;24:401–11. 15. Fagerstrom KO, Kunze M, Schoberberger R, et al. Nicotine dependence versus smoking prevalence: Comparisons among countries and categories of smokers. Tob Control 1996;5: 52– 6. 16. Hurt RD, Dale LC, Fredrickson PA, et al. Nicotine patch therapy for smoking cessation combined with physician advice and nurse follow-up. One-year outcome and percentage of nicotine replacement. JAMA 1994;271:595– 600. 17. Vernon JD, Crane LA, Prochazka AV, et al. Smokers hospitalized in an urban, public hospital: Addiction, stages of change, and self-efficacy. Prev Med 1999;28:488 –95. 18. Hilsden RJ, Hodgins DC, Timmer A, et al. Helping patients with Crohn’s disease quit smoking. Am J Gastroenterol 2000; 95:352– 8.
Vol. 96, No. 6, 2001 ISSN 0002-9270/01/$20.00 PII S0002-9270(01)02445-5
Attitudes Toward Smoking and Smoking Behaviors of Patients With Crohn’s Disease Robert J. Hilsden, M.D., M.Sc., F.R.C.P.C., David Hodgins, Ph.D., Diana Czechowsky, Marja J. Verhoef, Ph.D., and Lloyd R. Sutherland, M.D.C.M., M.Sc., F.R.C.P.C. Departments of Medicine, Psychiatry, and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada
OBJECTIVE: To examine the smoking behaviors of people with Crohn’s disease. In active smokers, we measured their willingness to quit, their degree of nicotine dependence, and the proportion that made a quit attempt within 6 months to determine if they were refractory to smoking cessation in comparison to the general population. We also examined factors that were important in their decision to smoke. METHODS: We conducted a cross-sectional survey of outpatients, supplemented by telephone interviews and a 6-month follow-up questionnaire of active smokers. Measures included disease activity, current smoking behaviors, intentions (stage of change), Fagerstrom Test for Nicotine Dependence, and factors related to their decision to smoke (decisional balance). RESULTS: The questionnaire was completed by 115 patients (78% response rate). Forty percent were active smokers. Of active smokers, 59% were considering quitting within the next 6 months, and of these, 15% were planning on quitting within the next 30 days. Those with moderate disease activity were more likely to be considering quitting than those with mild or severe activity. Nicotine dependence was rated as high in 33% and as moderate in 43%. Factors unrelated to Crohn’s disease were more important in their decision to smoke than were Crohn’s disease-related factors. After 6 months, 23% had made an attempt to quit and this attempt was strongly associated with their stated intentions at the baseline questionnaire. Two of three patients who had recently quit at baseline had resumed smoking. CONCLUSION: When compared to similar data for the general population, patients with Crohn’s disease are no more refractory to smoking cessation. (Am J Gastroenterol 2001; 96:1849 –1853. © 2001 by Am. Coll. of Gastroenterology)
pressive therapy, and development of fistulas (2–5). Furthermore, there is evidence that patients who successfully quit smoking have an improved disease course compared with those who continue to smoke. Cosnes et al. (6) found patients who quit smoking were less likely to suffer a flare-up of the disease, require corticosteroids, start immunosuppressive therapy, or require an increased dose of immunosuppressives. However, only 53 of 474 smokers (11%) in the study abstained from smoking 1 yr after receiving cessation counseling. Despite the evidence that smoking adversely affects the course of Crohn’s disease, standard gastroenterology and inflammatory bowel disease texts place little emphasis on smoking cessation as a potential therapy for Crohn’s disease. Furthermore, Shields and Low-Beer (7) reported that many patients were unaware of the risks of smoking on their Crohn’s disease and could not recall their physician ever telling them about these risks. Why don’t gastroenterologists put more effort into getting their patients to quit? One explanation may be that gastroenterologists view their patients as being refractory to quitting. As Cosnes et al. (6) stated, “CD patients are poorly receptive to smoking cessation advice.” However, is this true and are these patients any more refractory than average smokers? To explore this, we conducted a study with a group of Crohn’s disease patients attending gastroenterology outpatient clinics to determine whether they are refractory to smoking cessation. We determined (1) their willingness to quit (stage of change) (2), their degree of nicotine dependence (3), and the proportion of smokers who made a quit attempt within the subsequent 6 months. We also examined which factors are important in their decision to smoke, their beliefs about how smoking affects their disease, and their perceived barriers to smoking cessation.
INTRODUCTION There is a clear link between smoking tobacco and Crohn’s disease (CD). Smoking has been consistently shown to be a risk factor for the development of the disease (1). There is also a growing body of evidence that smoking also adversely affects the course of Crohn’s disease, in terms of the risk for recurrence or reoperation, the need for immunosup-
MATERIALS AND METHODS Study Design There were three components to this study. First, we conducted a cross-sectional survey of patients with Crohn’s disease using a mailed, structured questionnaire. Second, a subset of patients who were current smokers underwent a
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AJG – Vol. 96, No. 6, 2001
Table 1. Stages of Change Stage
Intention or Behavior
Precontemplation Contemplation
No intention to quit in next 6 mo Intends to quit in next 6 mo but not in next 30 days Intends to quit in next 30 days and has made quit attempt in past year Quit smoking within past 6 mo Quit smoking for more than 6 mo
Preparation Action Maintenance
telephone interview using structured and open-ended questions to further assess their beliefs about how smoking influences their disease and to find out what are their perceived barriers to smoking cessation. Third, all patients, who at the time of the survey indicated they were currently a smoker or who had quit within the previous 6 months, were sent a second questionnaire 6 months later to establish whether they had made an attempt to quit since receiving the first questionnaire. For both mailings, patients who did not respond within 3 wk of the date of mailing of the first questionnaire were sent a second questionnaire. The study was approved by the University of Calgary Conjoint Health Research Ethics Board (Calgary, Alberta, Canada). Patients Patients were recruited from the outpatient clinics of 10 gastroenterologists practicing in an academic or private practice setting in Calgary, Alberta, Canada from May to July 1998. Consecutive patients with documented Crohn’s disease were mailed a questionnaire within 10 days of their clinic visit. Instruments For the baseline assessment a structured questionnaire was created and pretested in a small group of patients. The questionnaire included items on basic demographic, disease, and treatment characteristics. Patient-rated disease activity was determined using a 7-point Likert scale ranging from one (inactive) to seven (terrible, bad as it ever gets). The questionnaire also included the following validated measures: stage of change, decisional balance, and Fagerstrom Test for Nicotine Dependence. Stage of change and decisional balance measures were obtained from the website of the creators’ institution, Cancer Prevention Research Center at the University of Rhode Island (http://www.uri.edu/research/cprc/). In addition, several questions were developed addressing attitudes toward and experiences with smoking cessation, and beliefs about the effects of smoking on Crohn’s disease. STAGE OF CHANGE. Smoking cessation is a process that occurs over a period of time. The Transtheoretical Model of Behavior Change describes how individuals changing addictive behaviors proceed through a series of stages (Table 1) (8). A respondent’s stage of change was ascertained by a discrete categorical measure, which assesses stage of change from a series of mutually exclusive questions.
DECISIONAL BALANCE. The decisional balance scale measures the importance of various factors in the decisionmaking process about smoking cessation and has been shown to predict subsequent smoking status (9). For this study, the short-form version of the scale was used. Each of the six items is responded to on a 5-point Likert scale. It incorporates two subscales identified as the pros of smoking and the cons of smoking. The pros include: smoking relieves tension, helps concentration, and relaxes (1–3). The cons include: smoking embarrasses, bothers other people, and makes people think the smoker is foolish for ignoring the warnings about cigarettes (1–3). The scores for each of the three items in the subscale are summed resulting in a total score from 3 to 15. The higher the subscale score, the greater the importance of that subscale in the patient’s decisionmaking process. DECISIONAL BALANCE—CROHN’S DISEASE. We created five additional items reflecting unique Crohn’s disease-related factors that we believed could potentially influence a patients decision to smoke. The structure of these items was similar to the general decisional balance scale. The new items included four “pros” and one “con.” The four pros were that smoking (1) helps the patient deal with abdominal pain (2), decreases appetite and helps the patient avoid eating when sick (3), reduces nausea (4), and is one of the few things that the patient can enjoy when sick. The con was that smoking makes the patient’s Crohn’s disease worse. The four pros items were summed to give a “Pros –CD” score from 4 to 20. FAGERSTROM TEST FOR NICOTINE DEPENDENCE (FTND). This six-item scale measures nicotine dependence on a range of scores from 0 to 10. Scores of 3–5 are indicative of moderate dependence and scores of ⬎5 of high dependence (10, 11). Reasonable test-retest reliability has been established over a 2-wk interval (Crohnbach’s alpha 0.64) (12). Validity has been demonstrated through multiple means, including correlation with biochemical measures of heaviness of smoking (10, 12). TELEPHONE INTERVIEW. Respondents who indicated in their returned questionnaire that they were willing to undergo a telephone interview were mailed a copy of the questionnaire to complete and were then interviewed by a trained research assistant. All those interviewed provided verbal consent at the time of the interview. The questionnaire focused on how patients believed smoking affected their Crohn’s disease, factors that they believed had prevented them from successfully quitting smoking in the past, and what kind of help they would like from their gastroenterologist to aid them to successfully quit in the future. All items were answered using a Likert scale. FOLLOW-UP QUESTIONNAIRE. The 6-month questionnaire included items on changes in disease and treatment
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Smoking and Crohn’s Disease
Table 2. Patient Characteristics Age, mean (range) Gender (F/M) Duration of disease, n (%) ⬍1 yr 1–5 yr ⬎5 yr Disease activity, n (%) Inactive/mild Moderate Very Education, n (%)* High school Post-secondary
38yr (19–77) 80/35 23 (20%) 23 (20%) 69 (60%) 44 (39%) 37 (32%) 33 (29%) 35 (31%) 79 (69%)
* One patient did not respond to this item.
characteristics, and whether the patient had attempted to quit smoking in the 6 months after the previous questionnaire. Data Analysis All questionnaires were coded into a computer database. Disease activity was divided into three categories: inactive/ mildly active, moderately active, and very active. Standard summary statistics were calculated. Associations between two variables were tested using a Fisher’s Exact Test. To determine whether the number of smokers in the study sample was greater than what would be expected in the general population, indirect standardization using age and sex-specific smoking prevalence rates for the Alberta general population were used with the calculation of a standard prevalence ratio of observed to expected cases along with a 95% CI.
RESULTS Subjects A questionnaire was sent to 147 patients and 115 (78%) responded. The characteristics of the study sample are shown in Table 2. Smoking Status Seventy-six respondents (66%) had smoked at some time and 46 (40%) were current smokers. The number of current smokers observed in the sample was 1.6 ⫻ what would have been expected based on the age- and sex-specific rates for the Alberta population (95% CI for observed/expected, 1.2– 2.1). Of those who had quit smoking, the majority (90%) had quit more than 6 months previously. Forty-five percent of women and 29% of men were current smokers (p ⫽ NS). Patients with at least some postsecondary education were less likely to be smokers than those whose highest level of education was a high school degree (33 vs 57%, p ⫽ 0. 022). Stage of Change Of the 46 current smokers, 19 (41%) were in the precontemplation stage, indicating they were not considering quitting smoking within the next 6 months (Table 3). Of the 27
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Table 3. Stage of Change and Nicotine Dependence of Current Smokers Stage of change Precontemplation Contemplation Preparation Nicotine dependence Low Moderate High
19 (41%) 20 (44%) 7 (15%) 11 (24%) 20 (43%) 15 (33%)
patients who were considering quitting in the next 6 months 20 (44% of all current smokers) were in the contemplation stage and seven (15%) were in the preparation stage. When stage of change was examined for each of the three disease activity levels, there was evidence that the proportion of patients in the precontemplation stage was not the same across categories of disease activity (p ⫽ 0.027). Ten patients (67%) who rated their disease as very active were in the precontemplation phase as compared with two (15%) and seven (39%) of those with moderately active and inactive/mildly active disease, respectively. Nicotine Dependence Twenty patients (43%) were rated as moderately dependent on nicotine and 15 patients (33%) were rated as highly dependent (Table 3). Seventeen of 19 patients (90%) in the precontemplation stage were at least moderately addicted to nicotine compared with 18 of 27 patients (67%) in the contemplation or preparation stages (p ⫽ 0.07). The majority of patients (70%) smoked 20 or fewer cigarettes per day. Fifty-five percent of current smokers had made at least one quit attempt that lasted more than 24 h in the previous year. Ten patients (21% of current smokers) had previously quit smoking for more than 6 months. Decisional Balance The median scores for the two subscales that examined the general pros and cons to smoking were both eight out of a maximum score of 15. Only one patient (2%) rated all three of the general pros to smoking as unimportant in their decision to smoke. In contrast, 13 patients (30%) rated all four of the Crohn’s disease-related pros to smoking as unimportant. Eighteen patients (40%) indicated the effect of smoking on their Crohn’s disease was not important in their decision to smoke. There was a trend for patients in the precontemplation stage to have higher scores on the general and Crohn’s disease-related pros to smoking and lower scores on the cons to smoking than those in the contemplation/preparation stages, but these did not reach statistical significance. The most important general pro to smoking was that smoking relieves tension, rated as at least very important by 48% of smokers. The most important general con to smoking was that smoking bothers others (37%).
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Telephone Interviews Thirty-three of the 46 (72%) current smokers completed a telephone interview. Fifteen respondents (45%) indicated smoking had no affect on diarrhea, fatigue, hunger, nausea, or pain from Crohn’s disease. Patients who believed smoking affected these symptoms were split between whether they believed they improved them or worsened them. For example, six patients believed smoking made their pain better, whereas three patients thought it made their pain worse. In contrast, eight patients thought it made their nausea worse and seven thought it made their diarrhea worse. Only three patients thought it improved their nausea and none thought it improved their diarrhea. Twenty-four patients (72%) had made an attempt to quit from the time when they were diagnosed with Crohn’s disease. Patients reported a variety of factors that they believed contributed to their lack of success. The most common one was the concern about gaining weight, reported by seven patients (21%). Six patients (18%) said increased Crohn’s disease symptoms while they were trying to quit were a factor. In an open-ended question that asked about barriers to successfully quitting, many patients mentioned the affects of smoking on stress or the increased stress while trying to quit. Only two patients (6%) mentioned lack of support from their family doctor or gastroenterologist as an important factor. Six Month Follow-Up Thirty-eight of the 49 patients (78%) who were current smokers or had recently quit smoking (⬍6 months) at the time of the first questionnaire completed a second questionnaire 6 months later. Eight of the current smokers (23%) had made an attempt to quit since the first questionnaire. Making an attempt to quit was strongly associated with stage of change at baseline. Only one of 16 (6%) of patients in the precontemplation stage had made a quit attempt compared with seven of 19 (37%) who were in the contemplation or preparation stage (p ⫽ 0.047). Two of the three recent patients who had recently quit at the time of the baseline questionnaire had resumed smoking.
DISCUSSION Given the growing evidence of the role that tobacco smoking plays in the course of Crohn’s disease, it is surprising that more attention has not been given to promoting smoking cessation in these patients. Rates of tobacco use are higher among patients with Crohn’s disease than among the general population (1), and the pattern was again present in our study sample. Forty percent of our sample were active smokers, which was 1.6 ⫻ what would have been expected based on age-sex specific smoking rates in the Alberta general population (13). The primary objective of this study was to determine whether patients with Crohn’s disease are refractory to smoking cessation. This has been suggested by other inves-
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tigators (6) and could represent one reason why more effort has not been made to get these patients to quit. However, our results consistently failed to provide any evidence that patients with Crohn’s disease are any more refractory to smoking cessation than smokers in the general population. First, only 41% of patients were in the precontemplation stage (not considering quitting in the next 6 months). The distribution of the Crohn’s disease patients by stage of change was very similar to the distribution reported in several different groups of smokers in the general population (14). Second, most (67%) of the Crohn’s disease patients were not highly dependent on nicotine as measured with a validated instrument. The majority of patients smoked 20 or fewer cigarettes per day. Although there are no sound Canadian population norms for nicotine dependence, the patients in this study had similar levels of nicotine dependence as a representative sample of adults from the USA (15), and were less dependent than subjects in a smoking cessation trial (16) and hospitalized smokers (17). Third, approximately 25% of patients who were active smokers at the time of the first questionnaire made an attempt to quit in the subsequent 6 months. As expected, the likelihood of making an attempt to quit was associated with the patient’s stage of change at baseline, with those in the precontemplation stage being much less likely to make a quit attempt than those in a more advanced stage. Therefore, based on the distribution of patients within the stages of change, their measured nicotine dependence, and their actions over the subsequent 6 months, there is no evidence that this group was any more refractory to smoking cessation than smokers in the general population. Furthermore, nearly 40% of all patients who had ever regularly smoked tobacco had previously quit. Although we did not determine whether these patients had quit before or after the onset of their disease, the very fact that such a large proportion had quit and the majority had maintained long-term abstinence provides further evidence that patients with Crohn’s disease are not refractory to smoking cessation. Therefore, efforts to promote and assist in smoking cessation should be an important and consistent component of the management of patients with Crohn’s disease who smoke. However, similar to smokers in the general population, remaining abstinent is difficult for people with Crohn’s disease. Two of the three patients who had quit within 6 months of the baseline questionnaire had resumed smoking within the next 6 months. This study also addressed what factors were important in a patient’s decision to smoke and what factors patients perceived as preventing them from successfully remaining abstinent. Smoking cessation programs and education often address risks of smoking and the benefits of quitting. Within our sample, nondisease specific pros and cons of smoking appeared to be more important than ones related to Crohn’s disease. Concerns about weight gain and increased stress appeared to be the most important barriers to quitting. Some patients indicated that increased Crohn’s disease symptoms
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while attempting to quit led to a smoking relapse. However, there was no consistent pattern in the patients’ perceptions of how smoking affected their Crohn’s disease. This would suggest that a cessation program designed for smokers in the general population would not necessarily have to be significantly altered to accommodate those with Crohn’s disease. We had predicted that stage of change might be associated with Crohn’s disease activity, with less willingness to change in those with higher disease activity. We did find evidence that the distribution of patients by stage of change was not the same in each strata of disease activity, but a linear trend was not seen. The proportion of patients in the precontemplation stage was lowest in patients with moderate disease activity and higher in those whose disease was inactive or very active. We do not have a ready explanation for this finding. The possibility of a type 1 error must be considered. This finding remains to be confirmed and explained through further research on a large group of patients. We failed to find any evidence that people with Crohn’s disease are overly refractory to smoking cessation. Further research is required to develop and refine smoking cessation strategies appropriate for this patient group. However, given that Crohn’s disease-related factors were not found to be that important in patients’ decisions to smoke, it would seem that available strategies would be appropriate for use in this group. Given the widespread availability of pharmacological treatments and self-help information (18), all patients with Crohn’s disease who smoke should be offered help to quit.
ACKNOWLEDGMENTS Financial support has provided by Crohn’s and Colitis Foundation Canada Summer Studentship (D. C.) and Medical Research Council of Canada Fellowship (R. J. H.). R. J. H. is an Alberta Heritage Foundation for Medical Research Population Health investigator. Reprint requests and correspondence: Robert Hilsden, M.D., M.Sc., F.R.C.P.C., Department of Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta T2N 4N1, Canada. Received Nov. 21, 2000; accepted Jan. 25, 2001.
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