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Stage of change and motivation to healthier lifestyle in non-alcoholic fatty liver disease
Research Article
Stage of change and motivation to healthier lifestyle in non-alcoholic fatty liver disease Elena Centis1, Simona Moscatiello1, Elisabetta Bugianesi2, Stefano Bellentani3, Anna Ludovica Fracanzani4, Simona Calugi5, Salvatore Petta6, Riccardo Dalle Grave5 Giulio Marchesini1,⇑ 1
Unit of Metabolic Diseases and Clinical Dietetics, ‘‘Alma Mater Studiorum’’ University, Bologna, Italy; 2Gastroenterology Unit, University of Turin, Italy; 3Gastroenterology, ‘‘Ramazzini’’ Hospital, Carpi (MO), Italy; 4University Department of Internal Medicine, Maggiore Hospital, IRCCS Ca’ Granda Foundation, Milan, Italy; 5Unit of Eating and Weight Disorders, Villa Garda Hospital, Garda (VR), Italy; 6Gastroenterology Section, Di.Bi.M.I.S., University of Palermo, Italy
Backgrounds & Aims: Healthy diet and physical activity are the treatment cornerstones of non-alcoholic fatty liver disease (NAFLD); their effectiveness is however limited by difficulties in implementing lifestyle changes. We aimed at determining the stage of change and associated psychological factors as a prerequisite to refine strategies to implement behavior changes. Methods: We studied 138 consecutive NAFLD patients (73% male, age 19–73 years). The diagnosis was confirmed by liver biopsy in 64 cases (steatohepatitis, 47%). All cases completed the validated EMME-3 questionnaire, consisting of two parallel sets of instruments (for diet and physical activity, respectively) and providing stages of change according to transtheoretical model. Logistic regression analysis was used to identify factors associated with stages making behavioral changes more demanding. Results: The individual profiles were variable; for diet, no cases had precontemplation as prevalent stage of change (highest score in individual profiles); 36% had contemplation. For physical activity, 50% were classified in either precontemplation or contemplation. Minor differences were recorded in relation to associated metabolic complications or steatohepatitis. Logistic regression identified male sex (odds ratio, 4.51; 95% confidence interval, 1.69–12.08) and age (1.70; 1.20–2.43 per decade) as the independent parameters predicting precontemplation or contemplation for diet. No predictors were identified for physical activity. Conclusions: NAFLD cases have scarce readiness to lifestyle changes, particularly with regard to physical activity. Defining stages of change and motivation offers the opportunity to improve clinical care of NAFLD people through individual programs exploiting the powerful potential of behavioral counseling, an issue to be tested in longitudinal studies. Ó 2012 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved. Keywords: Lifestyle; Psychological factors; Physical activity; Healthy diet. Received 17 September 2012; received in revised form 27 October 2012; accepted 20 November 2012; available online 29 November 2012 ⇑ Corresponding author. Address: Unit of Metabolic Diseases & Clinical Dietetics, ‘‘Alma Mater’’ University of Bologna, Policlinico S. Orsola, Via Massarenti, 9, I-40138 Bologna, Italy. Tel.: + 39 051 6364889; fax: +39 051 6364502. E-mail address: [email protected] (G. Marchesini).
Introduction Healthy diet and physical activity are the cornerstones in the treatment of non-alcoholic fatty liver disease (NAFLD). A series of epidemiological and observational studies have consistently linked NAFLD to excess body weight [1], unhealthy diet [2] and sedentary behaviors [3]. Of note, disease progression from fatty liver to necroinflammation and fibrosis (non-alcoholic steatohepatitis – NASH) is also largely dictated by obesity, diabetes, and the other features of the metabolic syndrome associated with unhealthy behaviors [1]. Diet and physical activity promote weight loss, reduce liver fat and tend to normalize liver enzymes [4–6]. These benefits have been supported by a randomized, controlled trial of behavior therapy in subjects with NASH [7], mimicking the procedures and main targets of the US Diabetes Prevention Program (7% weight loss; 150-min/week physical activity) [8]. Achieving the target of 7% weight loss significantly reduced liver steatosis and several histological indices of necroinflammation. Fibrosis did not improve significantly, but the trend was nonetheless favorable [7]. Notably, the effects of physical activity on liver fat seem to be independent of weight loss [9] and any effort should be made to combine a healthy diet with aerobic and resistance training [10]. Physical activity is also expected to improve cardiorespiratory fitness [11], thus reducing the high cardiovascular risk associated with NAFLD [12]. However, it is not easy to make patients change their unhealthy lifestyle [13]. Behavior therapy may only be successful in motivated patients, and motivation to dieting and exercising may be different according to age and sex. Personal motivation for change plays a pivotal role in behavior changes. According to the transtheoretical model proposed by Prochaska and DiClemente [14], behavioral changes occur through a defined sequence of the following qualitatively distinct five stages: (a) precontemplation (not thinking about changing the problem behavior within the next 6 months); (b) contemplation (intending to change in the next 6 months, but unwilling to start); (c) determination (planning to change in the next month, mostly having already tried unsuccessfully to change at least once in the past year); (d) action (making health-relevant changes in
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Research Article the behavior for as little as one day or as long as 6 months); (e) maintenance (having made behavioral changes for longer than 6 months) [15]. The different stages of change have been theorized to predict treatment participation to programs and dropout, as well as efficacy and long-term maintenance of improvement [15,16]. In addition, the transtheoretical model recommends that approaches need to be matched to the individual’s specific stage of change in order to be effective [15,17]. Accordingly, the proposed interventions may be less effective than programs that match patients’ readiness to change. Finally, the model has also been associated with the development of an effective approach to overcome resistance to change, namely, the motivational interview [18]. The aim of the study was to determine the stage of change and a series of psychological factors associated with motivation to change dietary habits and physical activity in NAFLD patients, as a prerequisite to refine strategies to implement behavior
changes in the population [19]. As far as we know, no study has evaluated the stage of change towards lifestyle modification in patients referred to tertiary centers for the assessment and treatment of their NAFLD.
Patients and methods Patients The study involved 138 consecutive NAFLD patients attending the centers of Bologna, Carpi (MO), Milan, Palermo and Turin, Italy, as part of a cooperative study within the European Union FP7 Health Program. They had been specifically referred to the institutions as 2nd level Centers for the assessment and treatment of NAFLD. Their anthropometric, clinical and biochemical characteristics are reported in Table 1. In all cases, the diagnosis was based on ‘‘bright liver’’ at ultrasonography, with/without elevated liver enzymes (alanine aminotransferase – ALT or g-glutamyl transpeptidase – GGT), negative hepatitis B and C virus tests,
Table 1. Characteristics of the NAFLD population. Data are presented as means ± SD or as number of cases (%).
Characteristics Age (yr) Education (%) Primary/secondary/commercial or vocational/degree Occupation (%) Employee/self-employed/housewife/retired Anthropometric data Body Mass Index (kg/m2) Waist circumference (cm) Clinical data Diabetes Hypertension Dyslipidemia Overweight (BMI, 25-29.9 kg/m2) Obesity (BMI, ≥30 kg/m2) Systolic pressure (mmHg) Diastolic pressure (mmHg) Biochemical tests Blood glucose (mg/dl) Fasting insulin (µU/ml) HOMA (%) Total cholesterol (mg/dl) HDL-cholesterol (mg/dl) Triglycerides (mg/dl) Aspartate aminostransferase (U/L) Alanine aminotransferase (U/L) γ-glutamyl-transpeptidase (U/L) Histology^ Steatosis (grade 1-3) Ballooning (score 0-2) Lobular inflammation (score 0-2) NASH Activity Score (1-7) Fibrosis (stage 0-4)
Males (n = 101) 44.0 ± 11.5
Females (n = 37) 57.5 ± 10.9*
1/9/54/36
3/18/64/15
63/32/0/5
17/22/41/20*
30.0 ± 5.3 104.8 ± 11.9
32.2 ± 5.0 103.2 ± 9.1
14 (14%) 34 (34%) 50 (50%) 50 (50%) 50 (50%) 128.1 ± 11.9 82.8 ± 9.0
11 (30%) 17 (46%) 20 (54%) 13 (35%) 23 (62%) 132.9 ± 12.7 85.1 ± 8.3
94.6 ± 19.5 15.9 ± 10.2 3.64 ± 2.37 199.2 ± 42.0 45.6 ± 10.4 171.1 ± 130.5 34.2 ± 18.1 55.4 ± 31.7 71.3 ± 81.6
103.6 ± 22.4 15.8 ± 6.0 4.11 ± 2.03 207.3 ± 39.5 51.8 ± 13.2* 171.6 ± 172.8 29.9 ± 15.6 40.5 ± 25.3* 58.9 ± 44.5
1.98 ± 0.63 1.25 ± 0.69 1.22 ± 0.71 4.45 ± 1.46 1.39 ± 1.02
1.93 ± 0.70 1.13 ± 0.52 1.13 ± 0.74 4.20 ± 1.42 1.07 ± 1.10
^n = 49 in men and n = 15 in women. ⁄ Significantly different from the corresponding value of males (p <0.025).
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JOURNAL OF HEPATOLOGY negative history of alcohol intake (<40 g/day in men and <20 g/day in women), autoimmune disease or use of hepatotoxic drugs. The diagnosis was confirmed by liver biopsy in 64 cases and 47% of them were classified as definite NASH [20]. All subjects received a comprehensive evaluation of their metabolic and clinical status, and completed the motivation questionnaires during the first visit or at entry into a web-based educational protocol for healthy nutrition and regular physical activity, also intended to favor weight loss (7–10% of initial weight), by creating a daily calorie deficit of approximately 500 kcal. No data on habitual diet and physical activity were systematically collected at entry.
Table 2. Stages of change towards healthy diet and habitual physical activity in the NAFLD population.
Healthy diet
Questionnaire Motivation to change was tested by the EMME-3 questionnaire for healthy diet and habitual physical activity [21], derived from a previously validated tool for individuals with alcohol problems [22]. The questionnaire consists of two parallel sets of instruments (for diet and physical activity, respectively): (a) an 18-item questionnaire (MAC 2) on a Likert scale from 0 (totally false) to 6 (totally true); (b) a set of 6 visual analog scales (VAS) from 0 to 100. A third part of the test, containing 9 brief descriptions (PORTRAITS) of imaginary people, confirmatory of the same motivational components of the MAC 2 questionnaire, was not used in this setting. The answers to the different questions are summed up to evaluate motivation to change according to the transtheoretical model of stages of change [23] (precontemplation, contemplation, determination, action, maintenance) using 10 statements, two for each stage. The scores of the five stages provide a graphic summary of the stage-of-change profile. The area with the highest score was considered as the prevalent stage of change. The remaining eight questions of MAC 2R, combined with the VAS responses, provide scores on discrepancy, self-efficacy, importance, temptation, readinessto-change and stabilization-of-change. Discrepancy refers to the contradiction between what one is or behaves like and what one aims to be or behave like, related to personal ‘‘image of self’’, values, goals and expectations [24]. When habitual diet and low physical activity are considered as threats to health, individuals perceive a need for change, but they may be unable to make the desired changes [25]. Discrepancy (also named internal fracture) reflects concern and dissatisfaction with the present situation (need for change) and the perceived importance of change (desire for change). Self-efficacy, as defined by Bandura [26], is the perceived confidence in attaining and maintaining the predefined goals of change. It has been extensively evaluated in the area of alcohol abstinence as a key factor in dealing with highrisk situations and reaching the desired targets [27,28]. Importance and temptation are defined as the importance attributed to the new lifestyle and the attractive value of the old lifestyle; finally readiness-tochange and stabilization-of-change offer a summary assessment of the stage of change. The questionnaires demonstrated good internal consistency with theoretical assumptions, reliability and concurrent validity in a large study of 431 subjects, most of whom were overweight or obese [21]. Clinical, anthropometric and biochemical measurements The presence of associated diseases (diabetes, dyslipidemia, hypertension) was recorded on the basis of patients’ history and associated drug treatment. Height and weight were measured on a standard scale at half centimeter and kilogram. Waist circumference was measured with a tape at the midpoint between the lower rib limit and the superior iliac spine. Obesity was diagnosed in the presence of body mass index (BMI, weight (in kg)/height2 (in m)) P30 kg/m2. A score (from 0 to 5) of ‘‘metabolic’’ severity was calculated as the sum of five features (diabetes, dyslipidemia, hypertension, obesity and alanine aminotransferase (ALT)>40 U/L), each being assigned one point. Glucose and lipid levels were measured in the fasting state by standard techniques. Insulin was measured by an immuno-enzymometric assay (AIA-PACK IRI, AIA-1200 system, Tosoh Co., Tokyo, Japan) with intra- and interassay CVs for quality control <7%. Insulin resistance (homeostasis model assessment – HOMA) was calculated as the product of blood glucose (mg/dL) and fasting insulin (lU/ mL), divided by 405 [29]. Statistical analysis A descriptive analysis of the database was carried out by means of parametric or non-parametric tests, as appropriate. The very few missing answers in the questionnaires (less than 1%) were replaced by intermediate values. The results were also split by gender, age (<45 vs. P45 years) and severity of liver disease (for
⁄
Physical activity
Males
Females
Males
Pre-contemplation
28 ± 18
34 ± 22
20 ± 18
Females 18 ± 23
Contemplation
65 ± 22
67 ± 27
68 ± 19
68 ± 17
Determination
73 ± 22
73 ± 20
67 ± 27
72 ± 23
Action
68 ± 21
56 ± 22*
47 ± 29
29 ± 25*
Maintenance
58 ± 28
53 ± 26
38 ± 28
42 ± 29
Discrepancy
48 ± 28
61 ± 22*
57 ± 26
67 ± 17*
Importance
86 ± 11
86 ± 17
75 ± 22
84 ± 15*
Self-effectiveness
74 ± 15
66 ± 24
71 ± 17
67 ± 21
Temptation
58 ± 23
58 ± 26.7
37 ± 24
31 ± 21
Readiness-to-change
73 ± 23
67 ± 28
69 ± 22
70 ± 28
Stabilization-of-change
66 ± 20
60 ± 22
57 ± 26.5
50 ± 29
Significantly different from the corresponding value of males, p <0.025.
cases where a liver biopsy was available, NASH vs. non-NASH, either fatty liver or ‘‘borderline’’ [20]) and metabolic involvement (0–2 features vs. 3–5). Comparison between motivational profiles for nutrition and physical activity was performed by Student t test for paired data. Logistic regression analyses were also carried out to determine factors associated with the probability of having precontemplation or contemplation as the prevalent stages of change vs. determination, action or maintenance. For this purpose, age (continuous), gender, education and job status (nominal) were considered as independent variables and either prevalent precontemplation or contemplation as dependent variable. Although several scales were considered, they belong to only two questionnaires for diet and physical activity; for this reason, the significance limit was set at p <0.025.
Results Clinical data The population under study was in a wide age range (19– 73 years) and was characterized by male prevalence and a high level of education, overweight or obesity and associated metabolic diseases (Table 1). The HOMA index was suggestive of insulin resistance (>2.7) in 64% of cases. At the time of analyses, liver enzymes (either ALT or GGT) were elevated in 58% of cases. At histology, the NAS score indicated the presence of NASH in 30/ 64 cases (47%). Fibrosis was severe (stage 2–4) in 26/64 cases (41%). Stages of change The stages of change towards healthy diet and habitual physical activity and the associated psychological factors are reported in Table 2 and Fig. 1. In both males and females, the individual profiles were extremely variable, with significantly lower scores of action and higher scores of discrepancy for both healthy diet and physical activity in females. Notably, the score of importance was significantly lower in males. The prevalent stage of change (highest scores in individual profile) is represented in Fig. 2. As to healthy diet, no cases scored the highest point in the precontemplation stage, 36% were in the contemplation stage, the rest being engaged in either determination or action or maintenance. The distribution was considerably different for habitual physical activity, with over 50% of cases (69/ 138) in either the precontemplation or contemplation stage.
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50 40 n po cy rta Se nc lfef e fi Te cac y m pt at R i ea on d St ine ab s iliz s at io n
Im
D
50 40 30 20 10 0
Habitual physical activity Prevalent stage of change (No. of cases)
Prevalent stage of change (No. of cases)
Healthy diet
60
70 60 50 40 30 20 10 0
Fig. 2. Prevalent stage of change towards healthy diet and habitual physical activity in NAFLD. Note that a much higher number of cases are in the precontemplation or contemplation stages for physical activity (and a much lower number in action or maintenance), compared to stages for healthy diet.
In relation to the severity of metabolic involvement, no differences between subjects with 0–2 metabolic complications (n = 118) vs. 3–5 (n = 18) were observed in the different scores of questionnaires (not reported in detail), with the notable exception of determination for physical activity, which was much higher (81 ± 14 vs. 66 ± 2; p = 0.023) in subjects with more complicated diseases. In relation to age, the score of contemplation in the healthy diet questionnaire differed between subjects aged less than 45 years (70.8 ± 19.5), compared to subjects aged 45 or more (61.6 ± 26.2; p = 0.024). In addition, older people with NAFLD had higher scores of determination in the physical activity area (74.7 ± 19.6 vs. 60.1 ± 30.2; p = 0.008) but lower scores of action (37.3 ± 28.1 vs. 49.0 ± 29.2; p = 0.018), as well as higher discrepancy (64.0 ± 20.9 vs. 54.2 ± 27.4; p = 0.019). 774
Ac tio M ai n nt en an ce
D
C
is
ep a cr is D
Fig. 1. Mean scores of stage of change and other psychological variables related to healthy diet (light blue circles) and habitual physical activity (black circles) in subjects with NAFLD. Data are presented as means ± 95% confidence intervals.
Pre-contemplation Contemplation Determination Action Maintenance
pl at et io n er m in at io n
pl at io n
60
30 25 20 15 10 5 0 -5 -10 -15
cr ep Im anc po y r Se tan c lfef e fic a Te m cy pt at R i ea on di ne St ab s iliz s at io n
70
on
nt em Pr eco Score difference (%)
80
30
70
30 25 20 15 10 5 0 -5 -10
te m
n Ac tio M ai n nt en an ce
n
at io in
et er
m
n
at io pl
at io C
on
te m
pl te m -c on Pr e
90 Mean score (%)
Score difference (%)
Healthy diet Habitual physical activity
80 70 60 50 40 30 20 10
D
Mean score (%)
Research Article
Fig. 3. Differences in mean score of stage of change and other psychological variables related to healthy diet and physical activity. Positive values indicate higher scores in the healthy diet questionnaire; negative values indicate higher scores in habitual physical activity. All scores not crossing the zero line stand for a statistically significant difference between a healthy diet and habitual physical activity.
Finally, in relation to the histological severity of liver disease, no significant differences were observed between subjects with fibrosis stage 0–1 vs. subjects with fibrosis 2–4 or in subjects with NASH vs. non-NASH, either fatty liver or borderline (not reported in detail). Logistic regression analysis identified male gender (Odds ratio (OR), 4.51; 95% confidence interval (CI), 1.69–12.08) and age (OR, 1.70; 1.20–2.43 per decade) as the sole independent parameters predicting a prevalent score in the precontemplation or contemplation area for healthy diet. No predictors were identified in the area of physical activity. Paired comparison between healthy diet and physical activity questionnaires Fig. 3 In individual NAFLD patients, precontemplation was significantly higher (by 10 points) in the area of healthy diet, but also the gaps in action and maintenance were positive (by 20 and 15 points, respectively). The difference in discrepancy was significantly negative, but patients reported a more intense temptation towards the original unhealthy behavior in the diet area (temptation), although the new nutritional lifestyle was regarded as more stable (stability), compared to changes attained in the area of physical activity. These differences were not remarkably different in relation to gender, with the exception of importance (only significant in males, 11.3 ± 21.3; p <0.001). Significant differences were observed in relation to age. The gap in determination (12.8 ± 36.9 vs. 1.8 ± 23.9; p = 0.006) was significantly different from zero, and much higher, only in patients aged <45 years, whereas the gap in discrepancy was only significant and much more negative in older people (12.4 ± 25.0 vs. 2.0 ± 28.2; p = 0.021).
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JOURNAL OF HEPATOLOGY Discussion This is the first study where a comprehensive analysis of motivation to change was carried out in a relatively large cohort of NAFLD patients attending tertiary centers for the evaluation of their metabolic liver disease, before entering specific behaviorchange programs. The results indicate that motivational profiles are variable in the NAFLD population and a large number of cases have scarce readiness to change, particularly in the area of physical activity. The low level of readiness for change and motivation highlights the importance of using individually tailored evidencebased techniques to implement behavior changes in these groups. Behavior-change theories were developed to explain the reasons why individuals change their behavioral patterns. They include the learning theory [30], the social cognitive theory [31], theories of reasoned action and planned behavior [32], the transtheoretical model [33] and the health action process approach [34]. The interest in behavioral change theories, particularly in the transtheoretical model, has increased in the last decade due to their possible application to medical problems requiring a behavioral change, such as adherence to treatments [35,36], weight management [37], and smoking cessation [38] The solidity of the transtheoretical model in the area of eating disorders and weight control has been criticized [39], but the model offers the theoretical basis to develop stage-matched approaches during the initial consultation, in order to improve the outcome of treatment of patients with unhealthy behaviors. The questionnaires we used produce a stage-of-change profile for both diet and physical activity. They do not fix patients into a single stage and make it possible to score and to classify individuals in multiple, frequently adjacent stages, in relation to specific circumstances. This is sometimes perceived as a limit of the model [40], but might become a strength allowing for a more comprehensive assessment of the whole process, where the prevalent stage may be identified [41]. The questionnaire also evaluates the components of readiness to change indicated by motivational interviewing described by Miller and Rollnick [18], in particular discrepancy and self-efficacy. The concept of discrepancy is based on the perception of a fracture between present behavior and what a person would like to be or to behave like, i.e., the difference between the present situation and the goals to be pursued [42]. This fracture may act as a stimulus to change, unless it becomes so large that changing is considered a threat for the person, bigger than that due to the present unhealthy situation. The Bandura’s concept of self-efficacy relates to the personal feeling of being able to pursue the desired goals, largely based on previous personal experience [26,43]. The importance of self-efficacy in the process of change has been extensively investigated and is considered one of the most important drives to success [27]. Whereas questionnaires testing self-efficacy are largely available, no questionnaire is available for measuring discrepancy in the area of metabolic diseases. The tool should provide an assessment of concerns, stress and dissatisfaction with the present status compared with expected goals, beyond a mere analysis of positive and negative consequences or a cost-benefit balance [44]. The results indicate important differences in the stage of change towards a healthy diet and habitual physical activity in NAFLD, similar to what observed in type 2 diabetes [45]. The positive finding is that nearly no cases have precontemplation
as the prevalent stage in both lifestyle areas, a result indicative of patients’ awareness of the importance of lifestyle in the pathogenesis of disease and of its change for a successful treatment. Notably, the score of precontemplation was 10 points lower in the physical activity area, but also the scores of action or maintenance were lower by 20–25 points. Apparently, almost all patients were aware of the importance of physical activity, but many felt unable to start or maintain an exercise program. This is also reflected in the 10-point higher discrepancy score. Discrepancy is expected to have a powerful effect in the initial phase of the process of change, being the drive to determination also at low discrepancy values, with high levels not necessarily associated to higher readiness-to-change. Specific activity programs have been developed [46] or suggested in metabolic disorders [47], but the barriers and difficulties to implement physical activity also in the area of NAFLD are well known [48]. They might be further increased by the presence of fatigue [49], a common symptom of NAFLD unrelated to disease severity. This difficulty is well expressed by the comparison between young and old patients, with older patients having higher scores of determination (i.e., willingness to start exercising) but lower scores of action (i.e., active practice of physical activity), resulting in higher levels of discrepancy. The very low levels of temptation measured in the area of physical activity might reflect the scarce participation in exercise programs, limiting the attraction towards old, unhealthy sedentary behaviors. This conclusion carries out important therapeutic considerations: therapists should help patients find reasonable and attainable programs and levels of physical activity, to avoid frustration and the attrition generated by high discrepancy levels. The severity of liver disease, measured either by the presence of multiple metabolic disorders or by the histological severity, had a very scarce impact on motivation to change. Notably, also the presence of elevated liver enzymes did not systematically drive motivation to change. Thirty years after the recognition that NAFLD may be a threat for health, leading to cirrhosis [50] and even hepatocellular carcinoma [51], its impact on the community remains modest and not sufficient to activate the process of change. This is also the case for most disorders related to unhealthy lifestyles, whose clinical awareness is largely underestimated in the community. Specific programs devoted to general practitioners to increase their role in counseling and treatment are welcome [52], as well as are multidisciplinary interventions delivered by dedicated teams [53]. A limitation of the study is the lack of systematic data on habitual diet and physical activity in our cohort. A recent overview of data collected in different countries confirmed that, independently of obesity, unbalanced nutrition and sedentary behaviors are associated with NAFLD [54]. In both males and females of our cohort, the average BMI was in the obesity range, indicating that, whatever the present lifestyle, it was insufficient to maintain body frame in a healthy range and making counseling for diet and physical activity a priority. Longitudinal studies are expected to verify whether the stage of change really predicts adherence to behavior programs and lifestyle changes. In conclusion, the study provides evidence that NAFLD patients have a large variability in their readiness to change both their diet and physical activity, and a large subgroup is not ready to enter parallel modification programs on both sides. Behavior is fluid and people can move between stages. Defining stages of change and motivation offers the opportunity to improve clinical
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Research Article care of people with NAFLD through individual programs and specific treatment strategies, exploiting the powerful potential of targeted behavioral counseling. Behavioral counseling provides people with the knowledge, self-efficacy, beliefs and tools to achieve and sustain a better lifestyle, both diet and physical activity, possibly improving the ultimate outcome of NAFLD patients.
[12]
[13]
[14] [15]
Financial support The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. HEALTH-F2– 2009-241762 for the project FLIP. EC and SM are supported by a specific research contract within the same program.
[16] [17] [18] [19]
[20]
Conflict of interest The authors who have taken part in this study declared that they do not have anything to disclose regarding funding or conflict of interest with respect to this manuscript. Acknowledgements
[21]
[22]
[23]
The authors are indebted to Arianna Mazzotti (Bologna), Marianna Porzio (Milan), Alessia Procaccini (Modena), Maria Rosa Barcellona (Palermo) and Chiara Rosso (Turin) for systematic collection of data.
[24] [25]
[26]
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JOURNAL OF HEPATOLOGY [39] Wilson GT, Schlam TR. The transtheoretical model and motivational interviewing in the treatment of eating and weight disorders. Clin Psychol Rev 2004;24:361–378. [40] Littell JH, Girvin H. Stages of change. A critique. Behav Modif 2002;26:223–273. [41] Dunn EC, Neighbors C, Larimer M. Assessing readiness to change binge eating and compensatory behaviors. Eat Behav 2003;4:305–314. [42] Festinger L. A theory of cognitive dissonance. Evanston (IL): Row & Peterson; 1957. [43] Bandura A. Self-efficacy in changing societies. Cambridge (UK): Cambridge University Press; 1995. [44] Spiller V, Zavan V, Guelfi GP. Motivation and change: a three dimensional continuum. In: Tober G, Raistrick D, editors. Motivational dialogue. London: Routledge; 2007. [45] Centis E, for Gruppo di lavoro interassociativo SID-AMD. Diabete tipo 2 e stile di vita: analisi ad interim della motivazione al cambiamento. Il Diabete 2012;24:26 [PD10]. [46] Di Loreto C, Fanelli C, Lucidi P, Murdolo G, De Cicco A, Parlanti N, et al. Validation of a counseling strategy to promote the adoption and the maintenance of physical activity by type 2 diabetic subjects. Diabetes Care 2003;26:404–408. [47] Dalle Grave R, Calugi S, Centis E, Marzocchi R, El Ghoch M, Marchesini G. Lifestyle modification in the management of metabolic syndrome: achievements and challenges. Diabetes Metab Syndr Obes 2010;3:1–13.
[48] Centis E, Marzocchi R, Suppini A. Dalle Grave R, Villanova N, Hickman IJ, et al. The role of lifestyle change in the prevention and treatment of NAFLD. Curr Pharma Des 2013. [49] Newton JL, Jones DE, Henderson E, Kane L, Wilton K, Burt AD, et al. Fatigue in non-alcoholic fatty liver disease (NAFLD) is significant and associates with inactivity and excessive daytime sleepiness but not with liver disease severity or insulin resistance. Gut 2008;57:807–813. [50] Ludwig J, Viggiano TR, McGill DB, Oh BJ. Non-alcoholic steatohepatitis: Mayo Clinic experience with an hitherto unnamed disease. Mayo Clin Proc 1980;55:434–438. [51] Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, et al. Expanding the natural history of non-alcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 2002;123:134–140. [52] Ahmed MH, Abu EO, Byrne CD. Non-Alcoholic Fatty Liver Disease (NAFLD): new challenge for general practitioners and important burden for health authorities? Prim Care Diabetes 2010;4:129–137. [53] Cobbold JFL, Peake CM, Anstee QM, Yee MS, Thursz MR. Measuring the effectiveness of a multidisciplinary non-alcoholic fatty liver disease clinic. J Hepatol 2012;56:S506. [54] Zelber-Sagi S, Ratziu V, Oren R. Nutrition and physical activity in NAFLD: an overview of the epidemiological evidence. World J Gastroenterol 2011;17:3377–3389.
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Stage of change and motivation to healthier lifestyle in non-alcoholic fatty liver disease Elena Centis1, Simona Moscatiello1, Elisabetta Bugianesi2, Stefano Bellentani3, Anna Ludovica Fracanzani4, Simona Calugi5, Salvatore Petta6, Riccardo Dalle Grave5 Giulio Marchesini1,⇑ 1
Unit of Metabolic Diseases and Clinical Dietetics, ‘‘Alma Mater Studiorum’’ University, Bologna, Italy; 2Gastroenterology Unit, University of Turin, Italy; 3Gastroenterology, ‘‘Ramazzini’’ Hospital, Carpi (MO), Italy; 4University Department of Internal Medicine, Maggiore Hospital, IRCCS Ca’ Granda Foundation, Milan, Italy; 5Unit of Eating and Weight Disorders, Villa Garda Hospital, Garda (VR), Italy; 6Gastroenterology Section, Di.Bi.M.I.S., University of Palermo, Italy
Backgrounds & Aims: Healthy diet and physical activity are the treatment cornerstones of non-alcoholic fatty liver disease (NAFLD); their effectiveness is however limited by difficulties in implementing lifestyle changes. We aimed at determining the stage of change and associated psychological factors as a prerequisite to refine strategies to implement behavior changes. Methods: We studied 138 consecutive NAFLD patients (73% male, age 19–73 years). The diagnosis was confirmed by liver biopsy in 64 cases (steatohepatitis, 47%). All cases completed the validated EMME-3 questionnaire, consisting of two parallel sets of instruments (for diet and physical activity, respectively) and providing stages of change according to transtheoretical model. Logistic regression analysis was used to identify factors associated with stages making behavioral changes more demanding. Results: The individual profiles were variable; for diet, no cases had precontemplation as prevalent stage of change (highest score in individual profiles); 36% had contemplation. For physical activity, 50% were classified in either precontemplation or contemplation. Minor differences were recorded in relation to associated metabolic complications or steatohepatitis. Logistic regression identified male sex (odds ratio, 4.51; 95% confidence interval, 1.69–12.08) and age (1.70; 1.20–2.43 per decade) as the independent parameters predicting precontemplation or contemplation for diet. No predictors were identified for physical activity. Conclusions: NAFLD cases have scarce readiness to lifestyle changes, particularly with regard to physical activity. Defining stages of change and motivation offers the opportunity to improve clinical care of NAFLD people through individual programs exploiting the powerful potential of behavioral counseling, an issue to be tested in longitudinal studies. Ó 2012 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved. Keywords: Lifestyle; Psychological factors; Physical activity; Healthy diet. Received 17 September 2012; received in revised form 27 October 2012; accepted 20 November 2012; available online 29 November 2012 ⇑ Corresponding author. Address: Unit of Metabolic Diseases & Clinical Dietetics, ‘‘Alma Mater’’ University of Bologna, Policlinico S. Orsola, Via Massarenti, 9, I-40138 Bologna, Italy. Tel.: + 39 051 6364889; fax: +39 051 6364502. E-mail address: [email protected] (G. Marchesini).
Introduction Healthy diet and physical activity are the cornerstones in the treatment of non-alcoholic fatty liver disease (NAFLD). A series of epidemiological and observational studies have consistently linked NAFLD to excess body weight [1], unhealthy diet [2] and sedentary behaviors [3]. Of note, disease progression from fatty liver to necroinflammation and fibrosis (non-alcoholic steatohepatitis – NASH) is also largely dictated by obesity, diabetes, and the other features of the metabolic syndrome associated with unhealthy behaviors [1]. Diet and physical activity promote weight loss, reduce liver fat and tend to normalize liver enzymes [4–6]. These benefits have been supported by a randomized, controlled trial of behavior therapy in subjects with NASH [7], mimicking the procedures and main targets of the US Diabetes Prevention Program (7% weight loss; 150-min/week physical activity) [8]. Achieving the target of 7% weight loss significantly reduced liver steatosis and several histological indices of necroinflammation. Fibrosis did not improve significantly, but the trend was nonetheless favorable [7]. Notably, the effects of physical activity on liver fat seem to be independent of weight loss [9] and any effort should be made to combine a healthy diet with aerobic and resistance training [10]. Physical activity is also expected to improve cardiorespiratory fitness [11], thus reducing the high cardiovascular risk associated with NAFLD [12]. However, it is not easy to make patients change their unhealthy lifestyle [13]. Behavior therapy may only be successful in motivated patients, and motivation to dieting and exercising may be different according to age and sex. Personal motivation for change plays a pivotal role in behavior changes. According to the transtheoretical model proposed by Prochaska and DiClemente [14], behavioral changes occur through a defined sequence of the following qualitatively distinct five stages: (a) precontemplation (not thinking about changing the problem behavior within the next 6 months); (b) contemplation (intending to change in the next 6 months, but unwilling to start); (c) determination (planning to change in the next month, mostly having already tried unsuccessfully to change at least once in the past year); (d) action (making health-relevant changes in
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Research Article the behavior for as little as one day or as long as 6 months); (e) maintenance (having made behavioral changes for longer than 6 months) [15]. The different stages of change have been theorized to predict treatment participation to programs and dropout, as well as efficacy and long-term maintenance of improvement [15,16]. In addition, the transtheoretical model recommends that approaches need to be matched to the individual’s specific stage of change in order to be effective [15,17]. Accordingly, the proposed interventions may be less effective than programs that match patients’ readiness to change. Finally, the model has also been associated with the development of an effective approach to overcome resistance to change, namely, the motivational interview [18]. The aim of the study was to determine the stage of change and a series of psychological factors associated with motivation to change dietary habits and physical activity in NAFLD patients, as a prerequisite to refine strategies to implement behavior
changes in the population [19]. As far as we know, no study has evaluated the stage of change towards lifestyle modification in patients referred to tertiary centers for the assessment and treatment of their NAFLD.
Patients and methods Patients The study involved 138 consecutive NAFLD patients attending the centers of Bologna, Carpi (MO), Milan, Palermo and Turin, Italy, as part of a cooperative study within the European Union FP7 Health Program. They had been specifically referred to the institutions as 2nd level Centers for the assessment and treatment of NAFLD. Their anthropometric, clinical and biochemical characteristics are reported in Table 1. In all cases, the diagnosis was based on ‘‘bright liver’’ at ultrasonography, with/without elevated liver enzymes (alanine aminotransferase – ALT or g-glutamyl transpeptidase – GGT), negative hepatitis B and C virus tests,
Table 1. Characteristics of the NAFLD population. Data are presented as means ± SD or as number of cases (%).
Characteristics Age (yr) Education (%) Primary/secondary/commercial or vocational/degree Occupation (%) Employee/self-employed/housewife/retired Anthropometric data Body Mass Index (kg/m2) Waist circumference (cm) Clinical data Diabetes Hypertension Dyslipidemia Overweight (BMI, 25-29.9 kg/m2) Obesity (BMI, ≥30 kg/m2) Systolic pressure (mmHg) Diastolic pressure (mmHg) Biochemical tests Blood glucose (mg/dl) Fasting insulin (µU/ml) HOMA (%) Total cholesterol (mg/dl) HDL-cholesterol (mg/dl) Triglycerides (mg/dl) Aspartate aminostransferase (U/L) Alanine aminotransferase (U/L) γ-glutamyl-transpeptidase (U/L) Histology^ Steatosis (grade 1-3) Ballooning (score 0-2) Lobular inflammation (score 0-2) NASH Activity Score (1-7) Fibrosis (stage 0-4)
Males (n = 101) 44.0 ± 11.5
Females (n = 37) 57.5 ± 10.9*
1/9/54/36
3/18/64/15
63/32/0/5
17/22/41/20*
30.0 ± 5.3 104.8 ± 11.9
32.2 ± 5.0 103.2 ± 9.1
14 (14%) 34 (34%) 50 (50%) 50 (50%) 50 (50%) 128.1 ± 11.9 82.8 ± 9.0
11 (30%) 17 (46%) 20 (54%) 13 (35%) 23 (62%) 132.9 ± 12.7 85.1 ± 8.3
94.6 ± 19.5 15.9 ± 10.2 3.64 ± 2.37 199.2 ± 42.0 45.6 ± 10.4 171.1 ± 130.5 34.2 ± 18.1 55.4 ± 31.7 71.3 ± 81.6
103.6 ± 22.4 15.8 ± 6.0 4.11 ± 2.03 207.3 ± 39.5 51.8 ± 13.2* 171.6 ± 172.8 29.9 ± 15.6 40.5 ± 25.3* 58.9 ± 44.5
1.98 ± 0.63 1.25 ± 0.69 1.22 ± 0.71 4.45 ± 1.46 1.39 ± 1.02
1.93 ± 0.70 1.13 ± 0.52 1.13 ± 0.74 4.20 ± 1.42 1.07 ± 1.10
^n = 49 in men and n = 15 in women. ⁄ Significantly different from the corresponding value of males (p <0.025).
772
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JOURNAL OF HEPATOLOGY negative history of alcohol intake (<40 g/day in men and <20 g/day in women), autoimmune disease or use of hepatotoxic drugs. The diagnosis was confirmed by liver biopsy in 64 cases and 47% of them were classified as definite NASH [20]. All subjects received a comprehensive evaluation of their metabolic and clinical status, and completed the motivation questionnaires during the first visit or at entry into a web-based educational protocol for healthy nutrition and regular physical activity, also intended to favor weight loss (7–10% of initial weight), by creating a daily calorie deficit of approximately 500 kcal. No data on habitual diet and physical activity were systematically collected at entry.
Table 2. Stages of change towards healthy diet and habitual physical activity in the NAFLD population.
Healthy diet
Questionnaire Motivation to change was tested by the EMME-3 questionnaire for healthy diet and habitual physical activity [21], derived from a previously validated tool for individuals with alcohol problems [22]. The questionnaire consists of two parallel sets of instruments (for diet and physical activity, respectively): (a) an 18-item questionnaire (MAC 2) on a Likert scale from 0 (totally false) to 6 (totally true); (b) a set of 6 visual analog scales (VAS) from 0 to 100. A third part of the test, containing 9 brief descriptions (PORTRAITS) of imaginary people, confirmatory of the same motivational components of the MAC 2 questionnaire, was not used in this setting. The answers to the different questions are summed up to evaluate motivation to change according to the transtheoretical model of stages of change [23] (precontemplation, contemplation, determination, action, maintenance) using 10 statements, two for each stage. The scores of the five stages provide a graphic summary of the stage-of-change profile. The area with the highest score was considered as the prevalent stage of change. The remaining eight questions of MAC 2R, combined with the VAS responses, provide scores on discrepancy, self-efficacy, importance, temptation, readinessto-change and stabilization-of-change. Discrepancy refers to the contradiction between what one is or behaves like and what one aims to be or behave like, related to personal ‘‘image of self’’, values, goals and expectations [24]. When habitual diet and low physical activity are considered as threats to health, individuals perceive a need for change, but they may be unable to make the desired changes [25]. Discrepancy (also named internal fracture) reflects concern and dissatisfaction with the present situation (need for change) and the perceived importance of change (desire for change). Self-efficacy, as defined by Bandura [26], is the perceived confidence in attaining and maintaining the predefined goals of change. It has been extensively evaluated in the area of alcohol abstinence as a key factor in dealing with highrisk situations and reaching the desired targets [27,28]. Importance and temptation are defined as the importance attributed to the new lifestyle and the attractive value of the old lifestyle; finally readiness-tochange and stabilization-of-change offer a summary assessment of the stage of change. The questionnaires demonstrated good internal consistency with theoretical assumptions, reliability and concurrent validity in a large study of 431 subjects, most of whom were overweight or obese [21]. Clinical, anthropometric and biochemical measurements The presence of associated diseases (diabetes, dyslipidemia, hypertension) was recorded on the basis of patients’ history and associated drug treatment. Height and weight were measured on a standard scale at half centimeter and kilogram. Waist circumference was measured with a tape at the midpoint between the lower rib limit and the superior iliac spine. Obesity was diagnosed in the presence of body mass index (BMI, weight (in kg)/height2 (in m)) P30 kg/m2. A score (from 0 to 5) of ‘‘metabolic’’ severity was calculated as the sum of five features (diabetes, dyslipidemia, hypertension, obesity and alanine aminotransferase (ALT)>40 U/L), each being assigned one point. Glucose and lipid levels were measured in the fasting state by standard techniques. Insulin was measured by an immuno-enzymometric assay (AIA-PACK IRI, AIA-1200 system, Tosoh Co., Tokyo, Japan) with intra- and interassay CVs for quality control <7%. Insulin resistance (homeostasis model assessment – HOMA) was calculated as the product of blood glucose (mg/dL) and fasting insulin (lU/ mL), divided by 405 [29]. Statistical analysis A descriptive analysis of the database was carried out by means of parametric or non-parametric tests, as appropriate. The very few missing answers in the questionnaires (less than 1%) were replaced by intermediate values. The results were also split by gender, age (<45 vs. P45 years) and severity of liver disease (for
⁄
Physical activity
Males
Females
Males
Pre-contemplation
28 ± 18
34 ± 22
20 ± 18
Females 18 ± 23
Contemplation
65 ± 22
67 ± 27
68 ± 19
68 ± 17
Determination
73 ± 22
73 ± 20
67 ± 27
72 ± 23
Action
68 ± 21
56 ± 22*
47 ± 29
29 ± 25*
Maintenance
58 ± 28
53 ± 26
38 ± 28
42 ± 29
Discrepancy
48 ± 28
61 ± 22*
57 ± 26
67 ± 17*
Importance
86 ± 11
86 ± 17
75 ± 22
84 ± 15*
Self-effectiveness
74 ± 15
66 ± 24
71 ± 17
67 ± 21
Temptation
58 ± 23
58 ± 26.7
37 ± 24
31 ± 21
Readiness-to-change
73 ± 23
67 ± 28
69 ± 22
70 ± 28
Stabilization-of-change
66 ± 20
60 ± 22
57 ± 26.5
50 ± 29
Significantly different from the corresponding value of males, p <0.025.
cases where a liver biopsy was available, NASH vs. non-NASH, either fatty liver or ‘‘borderline’’ [20]) and metabolic involvement (0–2 features vs. 3–5). Comparison between motivational profiles for nutrition and physical activity was performed by Student t test for paired data. Logistic regression analyses were also carried out to determine factors associated with the probability of having precontemplation or contemplation as the prevalent stages of change vs. determination, action or maintenance. For this purpose, age (continuous), gender, education and job status (nominal) were considered as independent variables and either prevalent precontemplation or contemplation as dependent variable. Although several scales were considered, they belong to only two questionnaires for diet and physical activity; for this reason, the significance limit was set at p <0.025.
Results Clinical data The population under study was in a wide age range (19– 73 years) and was characterized by male prevalence and a high level of education, overweight or obesity and associated metabolic diseases (Table 1). The HOMA index was suggestive of insulin resistance (>2.7) in 64% of cases. At the time of analyses, liver enzymes (either ALT or GGT) were elevated in 58% of cases. At histology, the NAS score indicated the presence of NASH in 30/ 64 cases (47%). Fibrosis was severe (stage 2–4) in 26/64 cases (41%). Stages of change The stages of change towards healthy diet and habitual physical activity and the associated psychological factors are reported in Table 2 and Fig. 1. In both males and females, the individual profiles were extremely variable, with significantly lower scores of action and higher scores of discrepancy for both healthy diet and physical activity in females. Notably, the score of importance was significantly lower in males. The prevalent stage of change (highest scores in individual profile) is represented in Fig. 2. As to healthy diet, no cases scored the highest point in the precontemplation stage, 36% were in the contemplation stage, the rest being engaged in either determination or action or maintenance. The distribution was considerably different for habitual physical activity, with over 50% of cases (69/ 138) in either the precontemplation or contemplation stage.
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773
50 40 n po cy rta Se nc lfef e fi Te cac y m pt at R i ea on d St ine ab s iliz s at io n
Im
D
50 40 30 20 10 0
Habitual physical activity Prevalent stage of change (No. of cases)
Prevalent stage of change (No. of cases)
Healthy diet
60
70 60 50 40 30 20 10 0
Fig. 2. Prevalent stage of change towards healthy diet and habitual physical activity in NAFLD. Note that a much higher number of cases are in the precontemplation or contemplation stages for physical activity (and a much lower number in action or maintenance), compared to stages for healthy diet.
In relation to the severity of metabolic involvement, no differences between subjects with 0–2 metabolic complications (n = 118) vs. 3–5 (n = 18) were observed in the different scores of questionnaires (not reported in detail), with the notable exception of determination for physical activity, which was much higher (81 ± 14 vs. 66 ± 2; p = 0.023) in subjects with more complicated diseases. In relation to age, the score of contemplation in the healthy diet questionnaire differed between subjects aged less than 45 years (70.8 ± 19.5), compared to subjects aged 45 or more (61.6 ± 26.2; p = 0.024). In addition, older people with NAFLD had higher scores of determination in the physical activity area (74.7 ± 19.6 vs. 60.1 ± 30.2; p = 0.008) but lower scores of action (37.3 ± 28.1 vs. 49.0 ± 29.2; p = 0.018), as well as higher discrepancy (64.0 ± 20.9 vs. 54.2 ± 27.4; p = 0.019). 774
Ac tio M ai n nt en an ce
D
C
is
ep a cr is D
Fig. 1. Mean scores of stage of change and other psychological variables related to healthy diet (light blue circles) and habitual physical activity (black circles) in subjects with NAFLD. Data are presented as means ± 95% confidence intervals.
Pre-contemplation Contemplation Determination Action Maintenance
pl at et io n er m in at io n
pl at io n
60
30 25 20 15 10 5 0 -5 -10 -15
cr ep Im anc po y r Se tan c lfef e fic a Te m cy pt at R i ea on di ne St ab s iliz s at io n
70
on
nt em Pr eco Score difference (%)
80
30
70
30 25 20 15 10 5 0 -5 -10
te m
n Ac tio M ai n nt en an ce
n
at io in
et er
m
n
at io pl
at io C
on
te m
pl te m -c on Pr e
90 Mean score (%)
Score difference (%)
Healthy diet Habitual physical activity
80 70 60 50 40 30 20 10
D
Mean score (%)
Research Article
Fig. 3. Differences in mean score of stage of change and other psychological variables related to healthy diet and physical activity. Positive values indicate higher scores in the healthy diet questionnaire; negative values indicate higher scores in habitual physical activity. All scores not crossing the zero line stand for a statistically significant difference between a healthy diet and habitual physical activity.
Finally, in relation to the histological severity of liver disease, no significant differences were observed between subjects with fibrosis stage 0–1 vs. subjects with fibrosis 2–4 or in subjects with NASH vs. non-NASH, either fatty liver or borderline (not reported in detail). Logistic regression analysis identified male gender (Odds ratio (OR), 4.51; 95% confidence interval (CI), 1.69–12.08) and age (OR, 1.70; 1.20–2.43 per decade) as the sole independent parameters predicting a prevalent score in the precontemplation or contemplation area for healthy diet. No predictors were identified in the area of physical activity. Paired comparison between healthy diet and physical activity questionnaires Fig. 3 In individual NAFLD patients, precontemplation was significantly higher (by 10 points) in the area of healthy diet, but also the gaps in action and maintenance were positive (by 20 and 15 points, respectively). The difference in discrepancy was significantly negative, but patients reported a more intense temptation towards the original unhealthy behavior in the diet area (temptation), although the new nutritional lifestyle was regarded as more stable (stability), compared to changes attained in the area of physical activity. These differences were not remarkably different in relation to gender, with the exception of importance (only significant in males, 11.3 ± 21.3; p <0.001). Significant differences were observed in relation to age. The gap in determination (12.8 ± 36.9 vs. 1.8 ± 23.9; p = 0.006) was significantly different from zero, and much higher, only in patients aged <45 years, whereas the gap in discrepancy was only significant and much more negative in older people (12.4 ± 25.0 vs. 2.0 ± 28.2; p = 0.021).
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JOURNAL OF HEPATOLOGY Discussion This is the first study where a comprehensive analysis of motivation to change was carried out in a relatively large cohort of NAFLD patients attending tertiary centers for the evaluation of their metabolic liver disease, before entering specific behaviorchange programs. The results indicate that motivational profiles are variable in the NAFLD population and a large number of cases have scarce readiness to change, particularly in the area of physical activity. The low level of readiness for change and motivation highlights the importance of using individually tailored evidencebased techniques to implement behavior changes in these groups. Behavior-change theories were developed to explain the reasons why individuals change their behavioral patterns. They include the learning theory [30], the social cognitive theory [31], theories of reasoned action and planned behavior [32], the transtheoretical model [33] and the health action process approach [34]. The interest in behavioral change theories, particularly in the transtheoretical model, has increased in the last decade due to their possible application to medical problems requiring a behavioral change, such as adherence to treatments [35,36], weight management [37], and smoking cessation [38] The solidity of the transtheoretical model in the area of eating disorders and weight control has been criticized [39], but the model offers the theoretical basis to develop stage-matched approaches during the initial consultation, in order to improve the outcome of treatment of patients with unhealthy behaviors. The questionnaires we used produce a stage-of-change profile for both diet and physical activity. They do not fix patients into a single stage and make it possible to score and to classify individuals in multiple, frequently adjacent stages, in relation to specific circumstances. This is sometimes perceived as a limit of the model [40], but might become a strength allowing for a more comprehensive assessment of the whole process, where the prevalent stage may be identified [41]. The questionnaire also evaluates the components of readiness to change indicated by motivational interviewing described by Miller and Rollnick [18], in particular discrepancy and self-efficacy. The concept of discrepancy is based on the perception of a fracture between present behavior and what a person would like to be or to behave like, i.e., the difference between the present situation and the goals to be pursued [42]. This fracture may act as a stimulus to change, unless it becomes so large that changing is considered a threat for the person, bigger than that due to the present unhealthy situation. The Bandura’s concept of self-efficacy relates to the personal feeling of being able to pursue the desired goals, largely based on previous personal experience [26,43]. The importance of self-efficacy in the process of change has been extensively investigated and is considered one of the most important drives to success [27]. Whereas questionnaires testing self-efficacy are largely available, no questionnaire is available for measuring discrepancy in the area of metabolic diseases. The tool should provide an assessment of concerns, stress and dissatisfaction with the present status compared with expected goals, beyond a mere analysis of positive and negative consequences or a cost-benefit balance [44]. The results indicate important differences in the stage of change towards a healthy diet and habitual physical activity in NAFLD, similar to what observed in type 2 diabetes [45]. The positive finding is that nearly no cases have precontemplation
as the prevalent stage in both lifestyle areas, a result indicative of patients’ awareness of the importance of lifestyle in the pathogenesis of disease and of its change for a successful treatment. Notably, the score of precontemplation was 10 points lower in the physical activity area, but also the scores of action or maintenance were lower by 20–25 points. Apparently, almost all patients were aware of the importance of physical activity, but many felt unable to start or maintain an exercise program. This is also reflected in the 10-point higher discrepancy score. Discrepancy is expected to have a powerful effect in the initial phase of the process of change, being the drive to determination also at low discrepancy values, with high levels not necessarily associated to higher readiness-to-change. Specific activity programs have been developed [46] or suggested in metabolic disorders [47], but the barriers and difficulties to implement physical activity also in the area of NAFLD are well known [48]. They might be further increased by the presence of fatigue [49], a common symptom of NAFLD unrelated to disease severity. This difficulty is well expressed by the comparison between young and old patients, with older patients having higher scores of determination (i.e., willingness to start exercising) but lower scores of action (i.e., active practice of physical activity), resulting in higher levels of discrepancy. The very low levels of temptation measured in the area of physical activity might reflect the scarce participation in exercise programs, limiting the attraction towards old, unhealthy sedentary behaviors. This conclusion carries out important therapeutic considerations: therapists should help patients find reasonable and attainable programs and levels of physical activity, to avoid frustration and the attrition generated by high discrepancy levels. The severity of liver disease, measured either by the presence of multiple metabolic disorders or by the histological severity, had a very scarce impact on motivation to change. Notably, also the presence of elevated liver enzymes did not systematically drive motivation to change. Thirty years after the recognition that NAFLD may be a threat for health, leading to cirrhosis [50] and even hepatocellular carcinoma [51], its impact on the community remains modest and not sufficient to activate the process of change. This is also the case for most disorders related to unhealthy lifestyles, whose clinical awareness is largely underestimated in the community. Specific programs devoted to general practitioners to increase their role in counseling and treatment are welcome [52], as well as are multidisciplinary interventions delivered by dedicated teams [53]. A limitation of the study is the lack of systematic data on habitual diet and physical activity in our cohort. A recent overview of data collected in different countries confirmed that, independently of obesity, unbalanced nutrition and sedentary behaviors are associated with NAFLD [54]. In both males and females of our cohort, the average BMI was in the obesity range, indicating that, whatever the present lifestyle, it was insufficient to maintain body frame in a healthy range and making counseling for diet and physical activity a priority. Longitudinal studies are expected to verify whether the stage of change really predicts adherence to behavior programs and lifestyle changes. In conclusion, the study provides evidence that NAFLD patients have a large variability in their readiness to change both their diet and physical activity, and a large subgroup is not ready to enter parallel modification programs on both sides. Behavior is fluid and people can move between stages. Defining stages of change and motivation offers the opportunity to improve clinical
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Research Article care of people with NAFLD through individual programs and specific treatment strategies, exploiting the powerful potential of targeted behavioral counseling. Behavioral counseling provides people with the knowledge, self-efficacy, beliefs and tools to achieve and sustain a better lifestyle, both diet and physical activity, possibly improving the ultimate outcome of NAFLD patients.
[12]
[13]
[14] [15]
Financial support The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. HEALTH-F2– 2009-241762 for the project FLIP. EC and SM are supported by a specific research contract within the same program.
[16] [17] [18] [19]
[20]
Conflict of interest The authors who have taken part in this study declared that they do not have anything to disclose regarding funding or conflict of interest with respect to this manuscript. Acknowledgements
[21]
[22]
[23]
The authors are indebted to Arianna Mazzotti (Bologna), Marianna Porzio (Milan), Alessia Procaccini (Modena), Maria Rosa Barcellona (Palermo) and Chiara Rosso (Turin) for systematic collection of data.
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