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Disease-related knowledge and smoking behavior of patients with Crohn's disease

Digestive and Liver Disease, In Press, Corrected Proof, Available online 26 May 2016, Available online 26 May 2016

Abstract

Background

Patients’ knowledge poses effects on quality of life, treatment adherence and coping skills in the management of Crohn's disease. Smoking is the most established risk factor and associated with a more severe course.

Aims

We aimed to investigate the status of patients’ knowledge on Crohn's disease in China, and explore the relationship between patients’ knowledge and smoking behavior.

Methods

Web-based questionnaires were created including a validated Crohn's and Colitis Knowledge Score applied to all participants and the Fagerström Test for Nicotine Dependence to smokers. The sociodemographic data, disease characteristics and smoking status were recorded. Patients were enrolled through invitation emails and Internet advertising. Current and ex-smokers were re-visited 6 months after enrollment.

Results

923 patients completed valid questionnaires with the knowledge score of 12.18 ± 4.61. Disease duration and educational status were independent predictors of the knowledge score by multiple linear regression analysis. The smoking rate was 8.2%. Low knowledge score was related with smoking behavior but not nicotine dependence, and smoking relapse during 6 months after enrollment.

Conclusions

Patients’ education should be a priority considering its impacts on many factors including smoking. Extra attention should be given to those from countryside area or having low family income and educational achievement.

Keywords: Disease knowledge, Patients education, Smoking.

1. Introduction

Crohn's disease (CD), a subtype of inflammatory bowel disease (IBD), is defined as a chronic inflammatory disorder affecting any part of the digestive tract with an unknown etiology. This disease can lead to many physical symptoms including abdominal pain and diarrhea as well as extra-intestinal manifestations, and create excessive financial and psychological burdens due to its incurability and chronicity. Disease information support and patients’ education have been gaining attention and proposed in the guidelines of IBD [1], suggesting an important role of disease-related knowledge in the patients’ self-management. Increasing evidence shows that a higher level of disease-related knowledge is associated with a better quality of life in IBD [2] and [3]. Patients with high levels of knowledge also have few disease-related worries and concerns [4], and use more adaptive coping strategies [5]. A latest study further demonstrated a favorable effect on the health care costs of patients’ knowledge [6].

Smoking has been well proven to be an independent risk factor for developing CD, and exert many detrimental effects on the disease course [7], [8], and [9]. CD patients who smoke suffer increased rates of relapse and postoperative recurrence, and are more frequently treated by steroids, immunosuppressants and anti-TNF drugs. Smoking also influences disease behaviour resulting in more cases of stricturing phenotype and is associated with higher risk of hospitalization and surgery. In line with this point, smoking cessation brings favorable results. Cosnes et al. conducted an intervention study and demonstrated that patients who quit smoking had a decreased risk of flare-up as well as less need for steroids and for introduction or reinforcement of immunosuppressive medications when compared with continuing smokers [10].

The incidence and prevalence of IBD continue to rise in Asia and much of the developing world [11]. However to our knowledge there are few data reporting the levels of patients’ knowledge from the developing countries. Rezailashkajani et al. evaluated one hundred patients with IBD from an outpatient clinic in Tehran with only 9 CD patients enrolled [12]. Another single-center study in Sri Lanka also recruited relatively few patients with CD [13]. The study by Leong et al. was conducted more than one decade ago using a self-devised knowledge questionnaire instead of the most common assessment tool [14]. Considering more severe and refractory disease course and negative effects of smoking in CD, we performed this large-scale study to specially investigate the levels of disease-related knowledge and its potential predictors among patients with CD in China, and for the first time to identify the association of patients’ knowledge and smoking.

2. Materials and methods

2.1. Patient enrollment

This is a cross-sectional study with CD patients recruited via targeted email through the interest groups based on the QQ chat software and advertising on the Chinese IBD Forum (www.ibdlife.info). Free consulting service was promised as a nominal incentive for completing the survey. Informed consent was obtained via mails from the final participants as well as the electronic medical records if needed. The questionnaire used was web-based and designed by the secure third-party survey provider WenJuanXing (www.sojump.com). The answer time was monitored automatically and several trap questions were set without telling the patients in order to ensure the validity and reliability of the results. A trap question was the one describing the same meaning as the original question in a different way with the options rearranged.

2.2. Data collection

The sociodemographic data, disease characteristics and smoking status were recorded, and all patients were asked to complete a well-validated 24-item Crohn's and Colitis Knowledge (CCKNOW) questionnaire that covers four areas of disease management including general knowledge, medication, diet and complications [15]. The Chinese version of CCKNOW was developed by translation and back translation, and has been validated in the Chinese population [16]. One point was awarded for each correct answer with no negative marks for incorrect answers. For those current smokers, the Fagerström Test for Nicotine Dependence (FTND) was used to evaluate the dependency on tobacco [17]. Moreover, patients that were current smokers or ex-smokers at enrollment were re-visited after 6 months to inquire about the present smoking status, through previously registered phone number and/or email address.

2.3. Statistical analysis

Differences for continuous variables between two groups were tested by independent t test. One-way ANOVA was used for multi-group comparisons and Bonferroni post hoc method to analyze the intergroup differences. Chi-square test was conducted for group comparisons with respect to categorical variables. Associations between CCKNOW score and disease duration as well as FTND score were assessed with Pearson correlation analysis. Multiple linear regression was adopted to identify the influencing factors of CCKNOW score. All variables were simultaneously included in the multivariable analysis. All P values were two-sided, and P < 0.05 was considered statistically significant. All statistical analysis was performed using IBM SPSS for Windows version 19.0.

2.4. Ethical considerations

All study material and data were kept confidential. This study was approved by the Ethics Committee of Jinling Hospital.

3. Results

3.1. Patient characteristics

A total of 976 patients participated the survey from March 2015 to June 2015, 923 (94.57%) of whom finished valid questionnaires. Demographic and clinical characteristics are presented in Table 1. Patients consisted of 645 males and 278 females, with an average age of 31.25 ± 9.34 and 30.65 ± 9.24 respectively. The disease duration was 6.02 ± 4.59 years in men and 6.57 ± 4.69 in women. 485 (52.6%) lived in the city while 254 (27.5%) in the town and 184 (19.9%) in the countryside area. Educational status was basic in 121 (13.1%), secondary in 382 (41.4%) and higher in 420 (45.5%) of enrolled patients. No significant differences were found between male and female patients for age, region, educational status and disease characteristics including disease duration, surgery and medical treatment. Noteworthily, a significantly higher proportion of men were in employment compared with women (67.8% vs. 55.4%, P < 0.001), which may be the reason for a greater family income in the male patients (P = 0.004).

Table 1 Patients characteristics.

Male (n = 645) Female (n = 278) Total (n = 923) P-value
Age (mean ± SD) 31.25 ± 9.34 30.65 ± 9.24 31.07 ± 9.31 0.370
Region 0.627
 Countryside 125 (19.4) 59 (21.2) 184 (19.9)
 Town 183 (28.4) 71 (25.5) 254 (27.5)
 City 337 (52.2) 148 (53.2) 485 (52.6)
Educational statusa 0.073
 Basic education 76 (11.8) 45 (16.2) 121 (13.1)
 Secondary education 262 (40.6) 120 (43.2) 382 (41.4)
 Higher education 307 (47.6) 113 (40.6) 420 (45.5)
Family income (CNY/month) 0.004
 <5000 357 (55.3) 178 (64.0) 535 (58.0)
 5000–10,000 178 (27.6) 75 (27.0) 253 (27.4)
 >10,000 110 (17.1) 25 (9.0) 135 (14.6)
Employment 437 (67.8) 154 (55.4) 591 (64.0) <0.001
Disease duration (years) 6.02 ± 4.59 6.57 ± 4.69 6.19 ± 4.63 0.097
Surgery for CD 241 (37.4) 101 (36.3) 342 (37.1) 0.824
Medical treatmentsb
 5-ASA 302 (46.8) 142 (51.1) 444 (48.1) 0.251
 Azathioprine 260 (40.3) 102 (36.7) 362 (39.2) 0.305
 Corticosteroids 78 (12.1) 40 (14.4) 118 (12.8) 0.336
 Enteral nutrition 215 (33.3) 96 (34.5) 311 (33.7) 0.762
 Infliximab 99 (15.3) 37 (13.3) 136 (14.7) 0.479

a Education status was categorized as ≤primary school, junior middle school (basic education), ≥a senior high school (including vocational/technical secondary school and junior college), (secondary education) and ≥senior college and university (higher education).

b As a patient may receive a combination of several treatments, the sum is more than 100%.

Values in parentheses are percentages (%).

The CCKNOW total score as well as the scores for each knowledge area are shown in Table 2. In all, the CCKNOW total score in our study population was 12.18 ± 4.61 and the scores regarding general knowledge, diet, treatment and complication were 5.83 ± 2.23, 1.19 ± 0.72, 2.32 ± 1.36 and 2.83 ± 1.43, respectively. There was no difference in the total and subscale scores between the genders. A significant, albeit weak, association was observed between CCKNOW total score and disease duration (ρ = 0.103, P = 0.002) (Fig. 1A). Patients living in the countryside had a lower CCKNOW score compared to those in town and city (Fig. 2A). Poorer disease-related knowledge was also demonstrated in those having low family income (Fig. 2B) and basic education (Fig. 2C). The influence of many possible factors on CCKNOW total score was calculated with multiple linear regression in the overall population (Table 3). Disease duration ≥5 years and educational status were found to independently predict the knowledge score. The percentage of patients who answered correctly to each question in four disease-related knowledge areas is indicated in Supplementary Table 1. Of all the 24 items, only 5.0% of the patients answered the question related to the ileorectal anastomosis operation correctly. The pregnancy-related question also had a low rate of correct answers (7.7%).

Table 2 Knowledge scores (total score and scores of subscales).

Male (n = 645) Female (n = 278) Total (n = 923) P-value
CCKNOW total score 12.23 ± 4.64 12.06 ± 4.56 12.18 ± 4.61 0.625
CCKNOW subscales
 General knowledge 5.89 ± 2.22 5.69 ± 2.26 5.83 ± 2.23 0.203
 Diet 1.19 ± 0.72 1.19 ± 0.74 1.19 ± 0.72 0.952
 Treatment 2.32 ± 1.37 2.32 ± 1.35 2.32 ± 1.36 0.968
 Complications 2.82 ± 1.45 2.86 ± 1.40 2.83 ± 1.43 0.686
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Fig. 1 Correlation between CCKNOW total score and disease duration. A positive weak correlation was observed between CCKNOW total score and disease duration (ρ = 0.103, P = 0.002) (A). Correlation between CCKNOW total score and FTND score. There was a negative but insignificant association between CCKNOW total score and nicotine dependence (ρ = −0.087, P = 0.455) (B).

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Fig. 2 Comparison of CCKNOW total score among different groups of patients divided by region (A), family income (B) and educational background (C). *P < 0.05; **P < 0.01; ****P < 0.0001.

Table 3 Multiple linear regression analysis of CCKNOW total score.

Variables Estimated coefficient (95% CI) P-value
Gender (male) −0.06 (−0.68 to 0.56) 0.847
Age ≥29 years −0.08 (−0.71 to 0.55) 0.807
Disease duration ≥5 years 0.90 (0.31 to 1.48) 0.003
Employment −0.10 (−0.75 to 0.55) 0.762
Region
 Countryside Reference
 Town 0.60 (−0.25 to 1.45) 0.167
 City 0.50 (−0.32 to 1.32) 0.231
Educational status
 Basic education Reference
 Secondary education 1.85 (0.91 to 2.78) <0.001
 Higher education 3.78 (2.80 to 4.77) <0.0001
Family income (CNY/month)
 <5000 Reference
 5000–10,000 0.66 (−0.03 to 1.35) 0.062
 >10,000 0.20 (−0.68 to 1.08) 0.655

Continuous variables were categorized by their medians.

3.3. Smoking status

76 (8.2%) of patients were current smokers, 178 (19.3%) were former smokers and 669 (72.5%) were never smokers. 183 (19.8%) were current smokers at diagnosis. Interestingly, the patients who never smoked presented a significantly higher CCKNOW total score in contrast to those with current smoking (12.49 ± 4.57 vs. 10.58 ± 5.01, P = 0.002) (Fig. 3A). The patients with CCKNOW total score less than or equal to 10 had the highest smoking rate going up to 11.6%, implying that a negative correlation existed between CCKNOW total score and smoking behavior (P = 0.034) (Fig. 3B). We further selected those who were currently smoking for calculation of FTND score. The patients more addicted to smoking seemed to have a lower level of knowledge, however this association did not reach significance (ρ = −0.087, P = 0.455) (Fig. 1B). At 6 months, 14/76 (18.4%) current smokers and 37/178 (20.8%) ex-smokers were lost to follow-up. The patients who lost follow-up (51/254, 20.1%) had similar disease knowledge (10.61 ± 3.91) compared with those who did not (11.54 ± 4.79) (P = 0.201). Of note, the majority of patients (54/62) with current smoking continued to be smokers, irrespective of the levels of CCKNOW score (Fig. 3C), and those who quit smoking at 6 months had a low baseline FTND score (≤2). But for the ex-smokers, those with the lowest CCKNOW score had the significantly highest rates of having smoked during 6 months after baseline (Fig. 3D).

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Fig. 3 Comparison of CCKNOW total score among never-smokers, ex-smokers and smokers (A). Smoking behavior in different groups of patients divided by CCKNOW total score. The percentages presented are the current smoking rates (B). Percentages of patients who quit smoking at 6 months in current smokers at baseline divided by CCKNOW total score (C). Percentages of patients who smoked during 6 months in ex-smokers at baseline divided by CCKNOW total score (D). The percentages presented are the corresponding rates. **P < 0.01.

4. Discussion

To our knowledge this is so far the first large-scale study to assess the levels of disease-related knowledge among CD patients in China, and is also the first to demonstrate a correlation between knowledge scores and smoking behavior. We found that patients represented knowledge deficit of disease if they lived in the countryside area, had low educational attainment, or earned little family income. Multiple linear regression analysis identified disease duration and educational background to be independent factors influencing levels of knowledge. The population of current smokers showed a poor understanding of disease which may be the reason for persistent smoking. Besides, defective knowledge of CD may also result in an increased likelihood of smoking relapse. These results further reinforced the need and advantages of patients’ education, in consideration of detrimental effects brought by smoking on disease outcomes.

The CCKNOW score in Chinese population was 12.18 ± 4.61 with no gender difference. The severe deficit of knowledge was evident in surgery- and pregnancy-related issues. In fact, there was substantial variation across different studies [6], [12], [13], [15], and [18], almost all of which collected data based on a single center about one decade ago from a small amount of patients. There was only one recent study by Colombara et al. that was fairly small and presented a median CCKNOW score of 7.50 (range 5.25–9.75) in 33 CD patients who were in older age with a median of 43 years and had a relatively lower level of education [6].

Living in the countryside, having low family income and educational achievement were associated with a lack of disease knowledge. Educational background turned out to be an independent factor by multiple linear regression analysis. Our observation is in line with the findings from previous studies [12] and [13]. Highly educated patients may be more conscious and more capable to utilize a number of approaches to gain insight into the disease and the principle of management. Disease duration was another influencing factor that we found. Opinions were divided on this point. Some previous studies have shown that duration of disease bore no correlation with the CCKNOW score [12] and [15]. There was also evidence from recent researches that supported their relationship [13] and [19]. In the present large-scale study, multiple linear analysis indicated that patients with disease duration ≥5 years only gained a slightly higher score by 0.90 point (95% CI: 0.31–1.48) compared with those <5 years. Pearson analysis further confirmed a positive but weak correlation between disease duration and CCKNOW score (ρ = 0.103, P = 0.002). A more reasonable conclusion may be that knowledge of disease would not evidently increase as disease duration extended if no intervention was done.

Sufficient disease-related knowledge of patients and self-management education programs have been shown to be pivotal in disease control and improvement of clinical outcomes in various chronic conditions [20], [21], and [22]. Although conflicting data existed regarding the effects of IBD-related knowledge on quality of life [2], [3], [4], [19], [23], and [24] and patients’ anxiety [25], [26], [27], and [28], more amount of solid evidence came up supporting its beneficial role by implying that patients with higher knowledge of IBD had fewer worries [4], better relationship with physicians [3], improved coping skills and treatment adherence [26], [29], and [30], and reduced cost [6]. Defective disease-related knowledge appeared to be associated with the behavior of current smoking and smoking relapse in our patients with CD, stressing the importance and feasibility of patients’ education in prompting patients to quit smoking or remain smoke-free condition. Physicians offering detailed information on the deleterious effects of smoking and the potential benefits of quitting smoking helped effectively patients achieve tobacco cessation [31].

The etiology of CD involves environmental factors, among which tobacco smoking is the most studied and established factor that is associated with CD predisposition and deleteriously affects natural history of disease [7], [8], and [9]. The current smoking rate in our overall population was 8.2%, which was in line with the previously reported data in Asia [32] and [33], suggesting that smoking may be not a risk factor for disease onset in Asia [33]. Besides, few patients in our study achieved smoking cessation at the 6-month follow up. In line with our results, Leung et al. analyzed variables associated with smoking cessation in 300 CD patients with a median of disease duration of 12 years, and found that if no intervention current smokers had low levels of motivation to quit smoking and very few quit 6 months after the baseline assessment [34]. Therefore, clinicians should consciously take the initiative to inquire about the smoking behavior even for those patients with longer duration of disease, and intervene if needed. Reward-based financial-incentive programs may be commonly accepted and helpful for smoking cessation [35].

There are limitations in the present study. Since our study is web-based, those less-educated patients with less access to Internet may be unfully and difficultly assessed. However, according to a recently published report by China Internet Network Information Center (http://www.ce.cn/xwzx/gnsz/gdxw/201507/23/t20150723_6022843.shtml), Chinese Internet users have topped 668 million in number and Internet penetration rate reaches 48.8% up to June 2015. We believed the web-based research design, in contrast to the multi-center setting based on tertiary general hospitals, assessed patient cohorts closer to the full cross section, as can be reflected by the enrollment of one fifth of participants living in the countryside area. In fact, it is more accurate to say that difficulty lies in the diagnosis rather than in the assessment of those from economically backward countryside area. Secondly, this is simply an observational cross-sectional study. Therefore to further confirm causality and evaluate the effects of disease-related knowledge on smoking behavior of patients, an intervention study will be warranted.

Clinicians are always more concerned about what treatment modalities or regimes may obtain maximal benefits in clinical practice thereby neglecting the pivotal role of patients’ self-management in controlling disease and improving outcomes. However the fact is that patients’ knowledge and information support greatly impact on the disease course and prognosis by influencing coping skills, treatment adherence, smoking behavior and so on. Patients’ education should be a priority especially considering the increasing incidence of CD in China, and the knowledge assessment in our study may have some helps in guiding the development of education programmes. Extra special attention should be given to those from countryside area or having low family income and educational achievement, who are always presenting the most defective disease-related knowledge. More researches are required to investigate the relationship between various forms of education programmes and clinical outcomes in patients with CD.

Conflict of interest

None declared.

Funding

This study was supported by grants from National Natural Science Foundation of China (81270478 and 81571881).

Acknowledgement

We thank Zhu Liang, administrator of the Chinese IBD Forum (www.ibdlife.info), for his support for recruiting patients.

Appendix A. Supplementary data

The following are the supplementary data to this article:

Download file

Supplementary Table 1. The percentage of correct answers for each question in the 24-item CCKNOW questionnaire in 923 patients with CD.

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Footnotes

a Department of Surgery, Jinling Hospital, Medical School of Nanjing University, Nanjing, China

b Medical School of Southeast University, Nanjing, China

Corresponding author at: Department of General Surgery, Jinling Hospital, 305 East Zhongshan Road, Nanjing 210002, China. Tel.: +86 13605169808; fax: +86 2584803956.