Changes in body mass index on a gluten-free diet in coeliac disease: A nationwide study☆

Article Outline

• Abstract
• 1. Introduction
• 2. Materials and methods
• 3. Results
• 4. Discussion
• 5. Learning points
• Conflict of interest statement
• Acknowledgements
• References
• Copyright

Abstract 

Objective

The clinical presentation of coeliac disease has changed and patients are often overweight at diagnosis. There is concern that patients might gain further weight while on a gluten-free diet (GFD). The aim of the study was to evaluate the impact of a GFD on the body mass index (BMI) in a nationwide cohort of coeliac patients and to determine variables predictive of favourable or unfavourable BMI changes.

Methods

We prospectively investigated weight and disease-related issues in 698 newly detected adults diagnosed due to classical or extraintestinal symptoms or by screening. BMI at diagnosis and after one year on a GFD were assessed and compared with that in the general population.

Results

At diagnosis, 4% of subjects were underweight, 57% normal, 28% overweight and 11% obese. On a GFD, 69% of underweight patients gained and 18% of overweight and 42% of obese lost weight; in the rest BMI remained stable. Changes were similar in both symptom- and screen-detected patients. The coeliac group had a more favourable BMI pattern than the general population. Favourable BMI changes were associated with subjects' self-rated expertise on GFD and young age at diagnosis, but not dietary counselling received.

Conclusions

BMI improved similarly in screen- and symptom-detected coeliac disease patients on a GFD.

Keywords: Body mass index, Coeliac disease, Gluten-free diet, Screen-detected

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1. Introduction 

Coeliac disease is one of the most common autoimmune-based disorders affecting about 1–2% of the population in the Western countries [1], [2], [3]. In the recent decades there have been several reports of a changing clinical picture of the disease. In particular, the proportion of patients suffering from classical gastrointestinal symptoms seems to be decreasing and an increasing number are diagnosed because of extraintestinal symptoms or screening in at-risk groups [4], [5]. At the same time, the proportion of patients who are rather over- than underweight at diagnosis is increasing [6], [7], [8], [9], [10]. More recently concern has increased for treated coeliac disease patients gaining weight on a gluten-free diet (GFD) concomitant with improved absorption of nutrients [8], as excessive weight gain may increase the risk of morbidity i.e., metabolic syndrome, type II diabetes mellitus and a higher risk of vascular diseases [11], [12]. This fear is supported by a recent study showing that an elevated body mass index (BMI) is associated with increased all-cause mortality [13]. This concern over weight gain applies especially to screen-detected coeliac disease patients, and it would thus be essential to evaluate the consequences of gluten-free dietary treatment on the BMI of coeliac patients today before any screening programs for the disease are instituted.

In Finland, a substantial proportion of coeliac disease diagnoses are made in primary healthcare and relatively mild and atypical symptoms dominate the clinical picture [14]. This augmented diagnostic approach has increased adult coeliac disease diagnoses twenty times during the past 30years, and the current clinical prevalence of 0.5% equals the figures found in many population screening studies [3], [14]. The aim of this nationwide prospective study was to assess the distribution of BMI at diagnosis in a large adult coeliac disease population containing both symptom- and screen-detected patients and to evaluate the impact of one year on a GFD on the BMI of the patients. In addition, variables predicting either favourable BMI changes or unfavourable weight gain were evaluated.

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2. Materials and methods 

Data for the study were obtained in a nationwide survey conducted in collaboration with the Finnish Coeliac Society. About 70% of newly diagnosed coeliac disease patients join the Society shortly after diagnosis. A validated questionnaire was mailed to all new members who joined the Society between February 2007 and May 2008. Those with biopsy-proven coeliac disease diagnosed within one year were considered eligible to the study. A follow-up questionnaire was sent to the respondents after one year. The questionnaires were developed in co-operation with the Coeliac Society, coeliac disease patients and clinical researchers [15]. They comprised questions on personal health status, including current height and weight, and symptoms and signs prior to the diagnosis of coeliac disease and after initiation of a gluten-free diet. Patients were also asked about their self-rated adherence to the diet, dietary counselling they received and follow-up visits. BMI was calculated as body weight/height² (kg/m²). The BMI values were categorized according to the World Health Organization (WHO) criteria as follows: <18.5kg/m² as underweight, 18.5–24.9kg/m² as normal weight, 25–29.9kg/m² as overweight and ≥30kg/m² as obese. Changes in BMI were classified as favourable if underweight patients gained weight, those with normal weight remained normal and overweight and obese patients lost weight. Weight gain was rated unfavourable if overweight or obese patients gained weight and those with normal weight became overweight or obese. Weight changes of at least three kilos were regarded as clinically relevant.

The feasibility and test-retest reliability of the questionnaires as well as face and content validity of the tested items were pre-tested by a group of coeliac disease members of the Finnish Coeliac Society, as previously described [15]. The repeatability of reported height was also measured and in 95% of cases the difference between reported height at baseline and at follow-up was less than two standard deviations. All clinical data were blindly coded before the analysis. Informed consent was obtained from all study subjects after a full written explanation of the aims of the study.

All subjects who were at least 16years old and had a biopsy-proven coeliac disease diagnosis were enrolled in the study. Patients were classified into three study groups as follows: I, patients with classical symptoms (dyspepsia, flatulence, abdominal pain, diarrhoea, iron deficiency anaemia, weight loss etc.); II, patients with extraintestinal symptoms (for example dermatitis herpetiformis, neurological complaints, arthralgia or infertility); and III, those who were identified by screening in at-risk groups such as first-degree relatives of coeliac disease patients and those with type 1 diabetes mellitus, autoimmune thyroid disease, Sjögren's syndrome or selective IgA deficiency. A subgroup of screen-detected initially asymptomatic patients was also analyzed separately. Patients who were less than 29years of age at diagnosis were considered young [16].

For comparison, data from 207 consecutive untreated biopsy-proven coeliac disease patients (median age 49years, range 18–79, 62% female) were collected from a local referral centre. Of them, follow-up data after one year on a strict serology-confirmed GFD were available of 141 patients. Weight and height of these patients were measured by healthcare personnel. Ethical approval was obtained from the Ethical Committee of Tampere University Hospital. All participants gave written informed consent.

Data for comparison to the Finnish general population during the same period (2007–2008) were attained from an annual postal survey conducted by the National Institute for Health and Welfare since 1978. The survey is entitled “Health Behaviour and Health among the Finnish Adult Population” and is mailed to a random sample of 5000 Finnish adults (15–64years old) each year [17], [18]. In this survey, differing from the WHO definition, underweight is categorized as BMI less than 20kg/m². This was thus the limit used in comparisons to the general population. We also limited comparison to responders of the same age (16–64years old).

Statistical analysis was carried out using Statistical Package for Social Sciences for Windows software (SPSS version 17.0, SPSS Inc., Chicago, IL, USA). All testing was two-sided and p<0.05 was considered statistically significant. Chi square test was used in cross tabulations and McNemar test for evaluating change within the groups. Binary logistic regression analyses were used to estimate associations between BMI and demographics, dietary counselling or follow-up. These results are shown as odds ratios (OR) and 95% confidence intervals (CI).

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3. Results 

The study questionnaires were mailed to 1864 individuals joining the Finnish Coeliac Society and 1062 (57%) responded. The age and sex distributions did not differ from those of non-responders. A total of 364 individuals were excluded: 157 had not been diagnosed within a year, 132 were under 16years old, 73 did not have biopsy-proven coeliac disease and 2 yielded insufficient data. The final analyses were thus conducted on 698 adults, of whom 677 (97%) also responded in the follow-up survey. Altogether 490 (70%) of the respondents suffered from classical and 62 (9%) from extraintestinal symptoms, and the remaining 146 (21%) subjects were detected by screening. Of the screen-detected group, 23 reported having been totally asymptomatic prior to the diagnosis. Characteristics of the patients in the different study groups are shown in Table 1. Age and sex distributions and socioeconomic index did not differ between the groups (Table 1). At diagnosis, 4% of all patients were underweight, 57% normal weight, 28% overweight and 11% obese. The percentages were similar in both screen- and symptom-detected patients (Table 1). Of the referral centre coeliac disease controls, 2% were underweight, 48% normal weight, 36% overweight and 13% obese at diagnosis.

Table 1. Characteristics of coeliac disease patients in different study groups at diagnosis, body mass index (BMI) according to WHO criteria.

	Study groups			Subgroup analysis
	Classical symptoms n=490	Extraintestinal symptoms n=62	Screen-detected, all n=146	Screen-detected, asymptomatic n=23
Female, %a, b	77	68	80	91
Median age (range/years)a, b	49 (16–84)	54 (20–75)	52 (18–82)	44 (19–82)
BMI at diagnosis, %a, b
Underweight	4	2	3	4
Normal weight	58	48	56	61
Overweight	27	34	29	22
Obese	11	16	12	13
Socio-economic index, %a, b
I	26	31	24	13
II	54	61	56	52
III	13	7	12	13
Student	7	2	8	22
The place of diagnosis, %b
Primary healthcare	41	27	45	44
Secondary healthcare	40	37	34	35
Tertiary healthcare	8	19	13	17
Private clinic	12	16	9	4
Referral to a dietician, %a, b	76	79	73	77

After one year on dietary treatment, 33% of all coeliac disease patients had gained and 16% lost at least 3kg. There were no differences between subjects with classical or extraintestinal symptoms and the screen-detected group. However, in the screen-detected asymptomatic group the percentages were 13% and 26%, respectively, which differed significantly from the other groups (p=0.046). Favourable changes or BMI remaining normal were noted in 62% of the study subjects, the percentages being similar in both screen- and symptom-detected patients. Equal favourable changes in BMI were evident also in referral centre controls, among whom the percentage was 57%. After a GFD, 2% of all patients were underweight, 54% normal weight, 34% overweight and 11% obese. The percentages were analogous in all study groups. BMI and weight changes categorized according to the initial BMI are shown in Table 2. A GFD resulted in 69% of initially underweight patients achieving normal weight. Of those of normal weight, 87% remained in the same BMI category. Weight loss was observed in 18% of overweight and 42% of obese patients, respectively. Dietary compliance was similar in all groups and 89% reported being on a strict GFD.

Table 2. Weight and body mass index (BMI) changes in different BMI categories after one year on a gluten-free diet according to WHO criteria for BMI.

The coeliac group as a whole had BMI significantly lower than that in the general population both at diagnosis and after one year on a GFD (Table 3). Interestingly, in a gender sub-analysis the male patients had significantly lower BMI than the controls at diagnosis (11% underweight, 49% normal weight, 28% overweight and 12% obese, versus 4%, 39%, 41% and 16% respectively, p<0.001) but not in the follow-up (3%, 49%, 35% and 13% versus 4%, 40%, 40% and 15% respectively, p=0.323), whereas in female patients the BMI did not differ from that of the controls at diagnosis (11% underweight, 51% normal weight, 26% overweight and 12% obese, versus 11%, 46%, 29% and 14% respectively, p=0.258), but was notably lower on dietary treatment (8%, 51%, 32% and 10%, versus 10%, 46%, 28% and 16% respectively, p=0.002).

Table 3. Body mass index (BMI) of coeliac disease patients in different study groups at diagnosis and after one year on a gluten-free diet compared to a sample of the general population in 2007 and 2008 (limited to 16–64years old, see Materials and methods).

	BMI (kg/m2)				P value (compared to controls)
	Underweight <20	Normal weight 20–24.9	Overweight 25–29.9	Obese ≥30
All coeliac disease patients, n=589 (%)
At diagnosis	11	51	27	12	<0.001
On a gluten-free diet	7	50	32	11	0.004
Classical symptoms, n=416 (%)a
At diagnosis	11	53	25	11	<0.001
On a gluten-free diet	6	53	29	11	0.004
Extraintestinal symptoms, n=51 (%)b
At diagnosis	8	43	31	18	0.950
On a gluten-free diet	4	44	44	8	0.220
Screen-detected, all, n=122 (%)b
At diagnosis	12	47	30	12	0.310
On a gluten-free diet	9	44	38	9	0.280
Screen-detected, asymptomatic, n=18 (%)b
At diagnosis	28	39	22	11	0.020
On a gluten-free diet	28	39	28	6	0.010
Population controls (%)
2007, n=3186	8	43	34	15
2008, n=3139	7	44	33	16

Analyses of variables predicting favourable changes in BMI revealed that only self-assessed expertise on GFD (OR 2.0, 95% CI 1.05–3.7) and young age at diagnosis (OR 2.1, 95% CI 1.2–3.6) were associated with improved BMI. Gender, clinical presentation, dietary counselling and whether the disease was diagnosed in primary, secondary or tertiary healthcare had no impact on BMI. None of the parameters assessed was associated with unfavourable weight gain. Adherence to a GFD was not associated with either favourable or unfavourable changes in BMI.

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4. Discussion 

Recent population-based studies have shown that the mean BMI is increasing in the Western countries, and currently approximately half of the adult population are overweight or obese (Table 4). Significantly, a similar trend was seen in coeliac disease patients in the present study as only a few per cent were underweight at diagnosis, whereas almost 40% were overweight or obese. Here, however, it must be noted that our study population consisted mainly of patients with mild if any symptoms and only few suffered from a severe disease. Interestingly, analogous results were obtained in a recent study from the UK in which 5% of the patients were underweight and 39% overweight or obese [8]. In the study in question, 81% of the patients gained weight on a GFD and, after two years on dietary treatment, 51% were overweight or obese. Nevertheless, when compared to the UK findings, the dietary response in our coeliac group was the opposite, as while on a GFD the overweight and obese patients lost and underweight patients gained weight. When compared to the general population, there were more patients of normal BMI in the coeliac disease group than in the population controls both at diagnosis and in the follow-up. There were some design differences between the UK and the present study that may have impacted the results. The UK study was retrospective and the study period was two years. In addition, the study population was smaller and comprised antibody positive patients that had converted negative after one year on a GFD and were seen by a single gastroenterologist. Moreover, in the present study only weight changes of at least three kilos were considered which might explain the different percentages of those who gained weight on a GFD. However, a parallel trend to our results was demonstrated in a recent American study in which the majority of treated coeliac disease patients either attained or remained normal weight and showed a more favourable BMI pattern both at diagnosis and on treatment than the general population [9].

Table 4. Body mass index in untreated coeliac disease patients and control subjects in different studies according to WHO criteria for body mass index.

ND not defined.

One interesting aspect in the present study is that we were able to assess the impact of a GFD on BMI in a substantial number of both symptom- and screen-detected coeliac disease patients. At diagnosis, the BMI profile was parallel in all study groups. In addition, the positive effects of the diet on BMI were similar regardless of whether the disease was detected due to classical or extraintestinal symptoms or by active screening. Similarly, in a population-based cohort of screen-detected children with initially low BMI, a significant increase in BMI was noted on a GFD [19]. The finding that male coeliac disease patients had a lower BMI than the general population at diagnosis but not after dietary treatment whereas the results among female patients were the opposite is a subject for further studies. The difference might be explained by different dietary habits between male and female patients. Female patients might have adopted a healthier life-style after being placed on dietary treatment which had resulted in improved BMI. In addition, male could have suffered from more severe symptoms than female.

It has been suggested by some authors that specialized follow-up and dietary counselling are essential for the appropriate management of coeliac disease [9], [20]. In Finland an increasing number of coeliac patients are diagnosed in primary healthcare by internalists or general physicians (Table 1). Subsequently, only a minority of patients are seen by gastroenterologists or investigated in special clinics with expertise in coeliac disease. However, there were no differences in the management of the disease and the results achieved between the different healthcare levels. In addition, the dietary counselling offered and reported compliance in the present cohort were comparable to those in previous studies [7], [21], [22].

In the present study, we could not find any association between dietary counselling received and changes in BMI. In Finland, patients are offered dietary advice from the healthcare system and patient organisations. In contrast, in the USA study dietary counselling was an important factor in obtaining beneficial changes in BMI [9]. Additionally, in the UK study the authors suggested that dieticians should modify advice depending on BMI [8]. Opposite results obtained in the present study might be due to differences in the management of coeliac disease and dietary counselling offered between the countries. In the UK study, overweight and obese patients suffered from milder symptoms than their counterparts [8]. However, in the present study clinical presentation had no significant impact on BMI outcome. Nevertheless, a self-rated good level of knowledge of the diet was associated with a beneficial BMI outcome. However, the self-rated level of knowledge of a gluten-free diet as predictor of improved BMI outcome in coeliac disease patients can be biased as the participants of the current study may have been the most highly motivated to adopt a healthier diet in general. In addition, diagnosis at younger age was associated with improved BMI. Changing one's dietary habits might be easier to those diagnosed at young age. In contrast, we could not determine any variables predicting unfavourable weight gain. This may be due to the fact that multiple factors have an impact on BMI and changes in weight, as is also seen at the population level.

Weight and height in the present study were self-reported, which might in theory have led to underestimation of the actual BMI. Nevertheless, BMI measured by self-reported height and weight has been shown to be reliable and valid in epidemiological studies [23], [24]. In addition, the control data from a sample of the general population was similarly based on self-reported values. Our results are also supported by parallel BMI results observed in coeliac disease controls obtained from the referral centre. One benefit of this study setting was that we were thus able to collect nation-representative data. However, our results might be applicable only to members of coeliac disease community. Other limitation to the present study was that the follow-up time was rather short. Typically, the most significant clinical and histological changes in the intestines occur within the first year on a GFD. However, it has been shown that full histological recovery in coeliac disease may sometimes take longer than 12months [25], [26] which might have an additional impact on BMI. The study also lacked a dietary questionnaire and thus it was impossible to verify if changes is BMI were linked to the normalization of intestinal absorptive function or to a different caloric intake.

In conclusion, the BMI profile of the coeliac disease group resembled that of the general population, being still significantly more favourable. Treatment with a gluten-free diet induced similarly beneficial changes in BMI in both symptom- and screen-detected coeliac disease patients, this improvement being slightly associated with young age at diagnosis and self-rated expertise on the diet.

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5. Learning points 

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Conflict of interest statement 

None to declare.

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Acknowledgements 

This study and the Coeliac Disease Study Group are supported by the Academy of Finland Research Council for Health, the Competitive Research Funding of the Pirkanmaa Hospital District, the Sigrid Juselius Foundation, the Foundation for Paediatric Research, the Ehrnrooth Foundation and the Finnish Coeliac Society, the Finnish Foundation for Gastroenterological Research, the Duodecim and the Finnish Medical Foundation.

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