Factors governing long-term adherence to a gluten-free diet in adult patients with coeliac disease
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1 Alimentary Pharmacology and Therapeutics Factors governing long-term adherence to a gluten-free diet in adult patients with coeliac disease J. Villafuerte-Galvez, R. R. Vanga, M. Dennis, J. Hansen, D. A. Leffler, C. P. Kelly & R. Mukherjee Celiac Center, Division of Gastroenterology, Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USA. Correspondence to: Dr R. Mukherjee, Celiac Center, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215, USA. rmukherj@bidmc.harvard.edu Publication data Submitted 28 January 2015 First decision 14 February 2015 Resubmitted 22 June 2015 Accepted 25 June 2015 EV Pub Online 23 July 2015 This article was accepted for publication after full peer-review. SUMMARY Background A strict gluten-free diet is the cornerstone of treatment for coeliac disease. Studies of gluten-free diet adherence have rarely used validated instruments. There is a paucity of data on long-term adherence to the gluten-free diet in the adult population. Aims To determine the long-term adherence to the gluten-free diet and potential associated factors in a large coeliac disease referral centre population. Methods We performed a mailed survey of adults with clinically, serologically and histologically confirmed coeliac disease diagnosed 5 years prior to survey. The previously validated Celiac Disease Adherence Test was used to determine adherence. Demographic, socio-economic and potentially associated factors were analysed with adherence as the outcome. Results The response rate was 50.1% of 709 surveyed, the mean time on a glutenfree diet years. Adequate adherence (celiac disease adherence test score <13) was found in 75.5% of respondents. A higher level of education was associated with adequate adherence (P = 0.002) even after controlling for household income (P = ). Perceptions of cost, effectiveness of the gluten-free diet, knowledge of the gluten-free diet and self-effectiveness at following the gluten-free diet correlated with adherence scores (P < 0.001). Conclusions Long-term adherence to a gluten-free diet was adequate in >75% of respondents. Perceived cost remains a barrier to adherence. Perceptions of effectiveness of gluten-free diet as well as its knowledge, are potential areas for intervention. Aliment Pharmacol Ther 2015; 42: doi: /apt.13319
2 J. Villafuerte-Galvez et al. INTRODUCTION Coeliac disease (CeD) is a chronic, inflammatory, autoimmune disease of the small intestine induced by ingestion of proline-rich and glutamine-rich gluten proteins in wheat, rye and barley in genetically susceptible individuals. 1, 2 The estimated prevalence of CeD ranges from 1:70 to 1:200 based on antibody screening studies and confirmatory intestinal biopsy data from the USA, Canada, South America, Australia and most Western and Middle Eastern countries. 3 Recent data indicate that the prevalence appears to be rising worldwide. 4, 5 The cornerstone of recommended treatment for CeD is the strict, complete and lifelong elimination of gluten from the diet and nondietary sources. 6 Clinical and histological remission through strict adherence to the gluten-free diet (GFD) has been associated with improvements in nutritional deficiencies, depression 7 and infertility 8 as well as a decrease in the risk of osteoporosis 9, 10 and gastrointestinal malignancies. 11 Although the GFD is proven to be a safe and effective therapy, it is not ideal. The GFD is typically more expensive than a non-gfd, not readily available in many settings and often of suboptimal nutritional value. In addition, patients often report that the GFD is restrictive and difficult to follow especially when eating away from home. All of these factors can significantly impact adherence. 12, 13 In fact, in one recent study, patients with CeD reported that the burden of treatment with the GFD was similar or higher to that of type I diabetes mellitus. 14 A recent systematic review of factors associated with GFD adherence in adult patients with CeD found rates for strict adherence to range from 42% to 91% depending on population and study definitions of adherence. 15 Interestingly, the review found no difference in adherence rates in screen- vs. symptom-detected coeliac patients. There is a paucity of published studies addressing long-term GFD adherence, particularly in adult patients. Data from Europe and Latin America have investigated factors related to GFD adherence primarily in children, with mean duration on the GFD from 6 months to 9 years No previous US study has investigated factors that govern long-term adherence ( 5 years) on a GFD. The goal of this survey study was to determine the factors that govern long-term adherence to the GFD in adult US patients with CeD using the validated Celiac Disease Adherence Test (CDAT) 21 and Likert-like scale questions. PATIENTS AND METHODS Study population Patients aged 18 years or older with a definite diagnosis of CeD based on a combination of their clinical presentation, positive antibodies (ttg-iga, AGA and EMA) and a duodenal biopsy with findings consistent with Marsh I to Marsh III categories were selected from the Institutional Review Board (IRB)-approved Celiac Center Patient and Serum Databases (PSDB) at Beth Israel Deaconess Medical Center (BIDMC), Boston, MA. This database includes all patients with a diagnosis of CeD that have received clinical care at the BIDMC Celiac Center at least once since For this study, only patients who had been on a GFD for a minimum of 5 years were included. This study was approved by the IRB. Data collection Relevant clinical and demographic data for each subject were extracted from the PSDB into a secure electronic worksheet. The identifying information collected included subject name and address that were used to mail the surveys and to obtain median household income estimates. The surveys were mailed between December 2011 and December By responding to the survey, the subject consented to participate in the study. A USA $5 gift card was offered as compensation to those who responded to the mail-in survey. The mailing contained the following: (i) A letter explaining the goal of the study as well as the risks and benefits of participating, (ii) A socio-demographic data sheet, (iii) The CDAT and (iv) Four additional Likert-like scale questions exploring factors potentially associated with GFD adherence. The CDAT is a questionnaire consisting of seven items on a Likert-type scale that was previously validated in a similar patient population. 21 The sum of the numeric value for the seven items is a score ranging from 5 to 35; lower scores reflect better adherence to a GFD. A score of 13 or less was previously determined to accurately predict an adequate adherence taking the assessment of an expert dietitian as the gold standard. Serological normalisation was defined as a level of tissue transglutaminase IgA antibody below 20 during the period including from 1 year prior to 3 years after the administration of the survey. If multiple values were available, the one closer to the administration of the survey was chosen. 754 Aliment Pharmacol Ther 2015; 42:
3 Long-term adherence to GFD in adults with coeliac disease Paper survey data were inputted into the electronic worksheet. At the end of the collection period, returned envelopes were counted and patients who had not responded to the survey were considered nonrespondents. The median annual household income for each subject was inputted based on postal address. Every subject was assigned the median household income of the block where their address is located based on the 2010 US Census Data as provided by Geolytics, Inc., Branchburg, NJ. Statistical analysis Complete data were analysed on an available case basis. Parametric analysis was used for continuous variables as per the central limit theorem. Student t tests, ANOVA, Spearman s test and v 2 tests were used as appropriate. Linear regression models were used to adjust correlations for covariates. When multiple pairwise comparisons were performed, we adjusted the P-value with the Bonferroni correction. P-values were considered significant below Data for this study were stored in a secure Microsoft Excel document. Stata 12 (StataCorp LP, College Station, TX) was used for statistical analysis and graphics. RESULTS Response to survey We mailed the survey to 709 subjects. At the end of the collection period, 355 (51.1%) subjects had responded to the survey. The distribution of socio-demographic and clinical variables between respondents and nonrespondents is shown in Table 1. Respondents and nonrespondents differed significantly only for having a tissue transglutaminase IgA antibody assay available around the time of the survey. They, nonetheless, did not differ significantly for frequency of serological normalisation. Adherence to the GFD Among the respondents, 75.5% had adequate GFD adherence (CDAT score 13). The mean time on a GFD was years and the mean CDAT score for all the respondents was See Figure 1 for distribution of CDAT scores. The average time on a GFD did not differ significantly between the respondents who were adequately adherent and the respondents who were inadequately adherent. Achieving serological normalisation, defined as a ttg IgA antibody around the time of the survey below 20, was significantly more frequent (P = 0.012) in patients with adequate GFD adherence (87.2%) as compared to those with inadequate adherence (66.7%). Socio-demographic and clinical variables that were acquired through the survey and our clinical database were compared between subjects above and below the cut-off score of 13 for CDAT as reported in Table 2. The level of education differed significantly between the subjects with adequate and inadequate adherence (v 2 Percent Adequate adherence n = 265 Inadequate adherence n = CDAT Score Figure 1 Distribution of CDAT score in respondents (N = 351). Table 1 Response to the survey Respondents Nonrespondents P-value n (%) 355 (50.1) 354 (49.9) Gender (% Female) Age in years (mean s.d.) Location % Massachusetts % New England Time on a GFD in years (mean s.d.) ttg available around time of survey (%) Serological normalisation (ttg-iga <20 around time of survey), % Median household Income in thousands of US dollars (mean s.d.) Aliment Pharmacol Ther 2015; 42:
4 J. Villafuerte-Galvez et al. Table 2 Adherence in the respondents (n = 355) GFD adherence Adequate (CDAT < 13) Inadequate (CDAT 13) P-value % Age in years (mean s.d.) Age at diagnosis in years (mean s.d.) Gender (% Female) Marital status (%) Single Married Separated Divorced Education (%) High school College Graduate Postgraduate Median household Income in thousands of US dollars (mean s.d.) Time on a GFD in years (mean s.d.) ttg available around time of survey (%) Serological normalisation (ttg-iga <20 around time of survey) (%) test, P = 0.002). Furthermore, a significant inverse correlation was found between the CDAT score and the education level (Spearman q = , P = ) as illustrated in Figure 2. This finding remained significant after adjustment for median household income (P = ). No other socio-demographic variables were associated with an adequate or inadequate GFD adherence. Patient perception affecting GFD adherence The four factors hypothesised to be correlated with adherence based on previously published reports were: (i) the cost of a GFD, (ii) the perceived effectiveness of a GFD, (iii) the perceived knowledge of the GFD and (iv) the perceived self-effectiveness at following a GFD. A statistically significant correlation was found between all four factors and the CDAT score (Table 3). Respondents were divided regarding cost as a limiting factor in GFD adherence nearly 40% of respondents strongly or somewhat agreed of whom 65.9% had adequate adherence. In contrast, more than 50% strongly or somewhat disagreed that cost was a factor limiting adherence of whom 83.6% had adequate adherence. Interestingly, there was a marginally significant correlation (P = 0.039, q = ) between agreement that cost is a barrier to GFD adherence and having a lower CDAT Score High school n = 39 College n = 150 Graduate n = 93 Post-Graduate n = 61 Figure 2 Celiac Disease Adherence Test (CDAT) score by education. median household income. Over 80% (219/260, 84.2%) of the respondents that classified their knowledge of the GFD as good or excellent had adequate adherence vs. about 50% (46/91, 50.5%) of those who classified their knowledge of the GFD as fair to poor. Close to 80% of respondents considered the GFD to help with their symptoms, and over 85% of these respondents were 756 Aliment Pharmacol Ther 2015; 42:
5 Long-term adherence to GFD in adults with coeliac disease Table 3 Factors potentially correlated with adherence Potential factors Cost Perceived effectiveness of GFD Knowledge Selfeffectiveness Questions assessing potential associated factors Likert-type scale answers Spearman s test Cost makes adherence to a Strongly Somewhat Neither agree Somewhat Strongly q P-value gluten-free diet difficult for me agree agree nor disagree disagree disagree (% with answer) < CDAT (mean s.d.) Adequate GFD adherence (% CDAT <13) I do not feel the gluten-free Strongly Somewhat Neither agree Somewhat Strongly q P-value diet is helping my symptoms agree agree nor disagree disagree disagree (% with answer) < CDAT (mean s.d.) Adequate GFD adherence (% CDAT < 13) My knowledge of the Excellent Good Fair Poor Terrible q P-value gluten-free diet is... (% with answer) < CDAT (mean s.d.) Adequate GFD adherence (% CDAT < 13) Since the time you were None of A little of Half of Most of All of q P-value diagnosed with coeliac the time the time the time the time the time disease, you have followed a strict gluten-free diet... (% with answer) < CDAT (mean s.d.) Adequate GFD adherence (% CDAT < 13) found to have adequate adherence. In contrast, close to 20% who were unsure or felt that the GFD did not improve their symptoms, nearly 50% (49.3%) were adequately adherent. Of these four factors, the two that showed the strongest correlation with adherence were self-effectiveness (q = ) and knowledge of the GFD (q = ). We further assessed whether the level of education was correlated with the perceived knowledge of the GFD and found this correlation to be significant (P = , q = ) as illustrated in Figure 3. However, after correcting for education level, the perceived knowledge of the GFD remained correlated with the CDAT score (adjusted P < 0.001). DISCUSSION When measuring adherence to a GFD, factors such as a protracted learning curve or patient s perception of increased burden of treatment could render initial measurements of adherence during the first years after diagnosis unrepresentative of lifelong adherence. Therefore, measuring adherence in the long-term is likely a more representative marker of ongoing and future adherence. No known previous US study has directly addressed the question of long-term GFD adherence, specifically, more than 5 years after CeD diagnosis. Our study is, to the best of our knowledge, the largest long-term GFD adherence study in the USA. We found an adequate adherence rate of 75.5% with 24.5% not adhering closely to the diet. Our adequate adherence rate is consistent with rates of 75.8% in a prior study with our institution s Celiac Center patients. 26 Canadian population studies in adult patients with CeD have found adherence rates between 68% and 90%, consistent with our study s findings. 13 However, in the literature, the adherence rates vary from 33.7% 22 to 95%. 23 Possible reasons for this variability include the use of different methodologies to determine adherence, differential response bias, the time since diagnosis in the patient population and the nature of the study population itself (community/country, reference centre patients, support group patients, Internet-recruited patients). Therefore, comparability between studies is limited and population-specific data are necessary. Aliment Pharmacol Ther 2015; 42:
6 J. Villafuerte-Galvez et al. 100% 90% 80% 70% PERCENT 60% 50% 40% 30% 20% 10% 0% High school College Graduate Postgraduate n = 39 n = 150 n = 93 n = 61 Education level Excellent Good Fair Poor Terrible Figure 3 Knowledge of GFD by education level. One of the strengths of our study is the novel use of the previously validated test to determine CeD adherence (CDAT) yielding both quantitative and qualitative measures of adherence to a GFD. Using the CDAT, this study was able to correlate key patient factors with GFD adherence. Another novel aspect of this study was the incorporation of median annual household income data as correlated with adherence. This study explored a number of key factors correlated with GFD adherence. The issue of cost as a barrier to GFD adherence has been described previously. A US study in 2007 found that on average a standard gluten-free product basket was 240% more expensive than its gluten-containing counterpart. A similar study in the UK in 2011 found that 11 of 19 gluten-free products studied were significantly more expensive than their gluten-containing counterparts. Also, the price of the gluten-free products was at least 2% but as high as 518% more expensive than their gluten-containing 24, 25 counterparts. Our patient population is almost evenly divided on whether they consider cost to be an obstacle to adherence. The cohort of respondents that considered cost to be a limiting factor for adherence have significantly higher CDAT scores and lower rates of adequate adherence. Nevertheless, respondents with an adequate adherence did not have significantly different median annual household income as compared to respondents with inadequate adherence. This finding raises the question of whether perception of cost vs. actual economic limitation is an obstacle to GFD adherence. Another key factor that was explored in this study was education and the perception of knowledge of the gluten-free diet as factors in adherence. A higher education level was correlated with better adherence independent of median household income. A higher education level was also associated with better self-perceived knowledge of the GFD. Nonetheless, respondents perceived knowledge of the GFD remains independently correlated with better adherence even after correcting for education level. These findings may translate into clinical practice by providing patients with self-perceived poor or fair knowledge of the GFD with increased dietary counselling regardless of the patient s education level. Our findings of a higher proportion of serological normalisation in patients with adequate adherence as compared to those with inadequate adherence are consistent with previous findings 27 that support that adherence to the diet is key for serological normalisation or clinical improvement. However, serology cannot be reliably used as a marker of adherence to a GFD in patients with CeD. Our study has some limitations that are important to note. As in any survey study, there will be a group of nonrespondents for whom it is impossible to rule out 758 Aliment Pharmacol Ther 2015; 42:
7 Long-term adherence to GFD in adults with coeliac disease the possibility of different adherence behaviour. However, we assessed the respondent and nonrespondent group for differences in gender, age, location, time on a GFD and median household income and found no differences. We did find a significant difference in the availability of tissue transglutaminase IgA samples in the period around the administration of the survey. This likely reflects a lesser involvement with healthcare and use of health services in the nonrespondent subpopulation rather than a different clinical behaviour as supported by the absence of difference in the proportion of patients with serological normalisation. A previous study with a mail-in survey for functional gastrointestinal disorders having a 52% response rate reviewed medical records of a subset of nonrespondents and found no significant difference in gastrointestinal symptoms or diagnoses but did find differences in healthcare usage behaviour concluding that a nonresponse bias seems to be nonsubstantial in this type of study. 28 In summary, adequate long-term adherence to a GFD was observed in the majority of CeD patients that responded to our survey but one quarter of those who responded reported poor adherence. Factors associated with inadequate adherence were a lower education level and a negative perception of patients own knowledge of the GFD as well as of their own self-effectiveness in following the diet. Factors such as patient age, gender, time on a GFD and median household income were not associated with GFD adherence. These findings bring to light the challenge of designing proven, cost-effective strategies to improve long-term GFD adherence in the poorly adherent population. Future studies should focus on developing and testing interventions for this non-adherent group. Such interventions might target increased knowledge of the GFD and perceptions of the importance of close adherence. AUTHORSHIP Guarantor of the article: Javier Villafuerte-Galvez. Author contributions: Javier Villafuerte-Galvez: statistical analysis, analysis and interpretation of data, drafting of manuscript. Rohini Vanga: Data acquisition. Melinda Dennis: Study concept and design. Joshua Hansen: Study concept and design, data acquisition. Daniel Leffler: Study concept and design, critical revision of manuscript, study supervision. Ciaran Kelly: Study concept and design, critical revision of manuscript, study supervision. Rupa Mukherjee: Study concept and design, data acquisition, analysis and interpretation of data, drafting of manuscript. ACKNOWLEDGEMENT Declaration of personal interests: None for Drs Villafuerte-Galvez, Vanga, Mukherjee, Melinda Dennis and Joshua Hansen. Daniel Leffler has served as a consultant for and/or received research support from the following: Alba Therapeutics, Alvine Pharmaceuticals, Shire Therapeutics, Ironwood Pharmaceuticals, Genzyme, Glenmark Pharmaceuticals, GI Supply, Pfizer, Coronado Biosciences, Bioline Rx, Inova Diagnostics, Prometheus Laboratories. Dr Ciaran P Kelly has acted as a consultant and scientific advisor to Alba Therapeutics, Alvine Pharmaceuticals, ImmunosanT and Pfizer Inc. Declaration of funding interests: None. REFERENCES 1. Di Sabatino A, Corazza GR. Coeliac disease. Lancet 2009; 373: Ludvigsson JF, Leffler DA, Bai JC et al. The Oslo definitions for coeliac disease and related terms. Gut 62: Schuppan D, Junker Y, Barisani D. 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