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American Journal of Gastroenterology ISSN 0002-9270


C 2006 by Am. Coll. of Gastroenterology doi: 10.1111/j.1572-0241.2006.00750.x
Published by Blackwell Publishing

Overweight in Celiac Disease: Prevalence, Clinical


Characteristics, and Effect of a Gluten-Free Diet
William Dickey, M.D., Ph.D., F.A.C.G., and Natalie Kearney, B.Sc.
Departments of Gastroenterology and Dietetics, Altnagelvin Hospital, Londonderry, Northern Ireland, United
Kingdom

BACKGROUND: It is well established that a minority of celiac patients present with “classic” symptoms due to
malabsorption. However, few studies have focussed on the distribution of body mass index (BMI) in
celiac populations and its relationship to clinical characteristics, or on its response to treatment.
METHODS: We reviewed BMI measurements and other clinical and pathological characteristics from a
database of 371 celiac patients diagnosed over a 10-yr period and seen by a single
gastroenterologist. To assess response to gluten exclusion, we compared BMI at diagnosis and after
2 yr treatment in patients with serological support for dietary compliance.
RESULTS: Mean BMI was 24.6 kg/m2 (range 16.3–43.5). Seventeen patients (5%) were underweight (BMI
<18.5), 211 (57%) were normal, and 143 (39%) were overweight (BMI ≥25), including 48 (13% of
all patients) in the obese range (BMI ≥30.0). There was a significant association between low BMI
and female gender, history of diarrhea, reduced hemoglobin concentration, reduced bone mineral
density (BMD), osteoporosis, and higher grades (subtotal/total) of villous atrophy. Of patients
compliant with a gluten-free diet, 81% had gained weight after 2 yr, including 82% of initially
overweight patients.
CONCLUSIONS: Few celiac patients are underweight at diagnosis and a large minority is overweight; these are less
likely to present with classical features of diarrhea and reduced hemoglobin. Failed or delayed
diagnosis of celiac disease may reflect lack of awareness of this large subgroup. The increase in
weight of already overweight patients after dietary gluten exclusion is a potential cause of
morbidity, and the gluten-free diet as conventionally prescribed needs to be modified accordingly.
(Am J Gastroenterol 2006;101:2356–2359)

INTRODUCTION in the west of Northern Ireland. Celiac disease is diagnosed


by duodenal biopsy after initial investigation at our clinics or
Celiac disease is a genetically mediated autoimmune prox- referral from family practitioners or other hospital clinicians.
imal enteropathy triggered by the ingestion of gluten, with We reviewed a database of all patients newly diagnosed
a prevalence of 0.5–1% in European and American popu- as celiac over the 10-yr period November 1995 through
lations (1). Its clinical manifestations are extremely diverse October 2005. BMI, defined as body weight (kg)/height (m2 ),
and the “classic” celiac presentation, due to malabsorption, of was recorded before gluten exclusion was prescribed under
weight loss and diarrhea is increasingly the exception rather the supervision of hospital and community dietitians. The
than the rule (2). In a 1998 paper (3), we reported that only a World Health Organisation (WHO) defines BMI <18.5 as
minority of newly diagnosed celiacs fitted the stereotype of underweight, 18.5–24.9 as normal, and 25 or over as over-
underweight, with a high proportion having a body mass in- weight (and 30 or over as obese) (4). As these criteria are
dex (BMI) of 25 or over. In this study, we have reviewed BMI only applicable above the age of 20, younger patients were
in celiac patients diagnosed over a 10-yr period in order to excluded. Also, for this study, only patients with a Marsh
obtain an updated prevalence of overweight in celiac disease, III lesion (5) (villous atrophy with intraepithelial lympho-
to assess associated clinical characteristics, and to determine cytosis) were included. Additional data recorded for each
the impact of gluten exclusion on BMI. patient and used in analyses included age, gender, clini-
cal presentation, hemoglobin concentration, corrected (ion-
SUBJECTS AND METHODS ized) serum calcium levels, celiac serological testing (IgA
endomysial antibody was measured using the same indi-
Our department provides gastroenterology services for a rect immunofluorescence technique throughout the study pe-
mixed urban and rural population of approximately 270,000 riod), and grade of villous atrophy (partial, subtotal, or total).

2356
Overweight in Celiac Disease 2357

Table 1. Clinical Characteristics of All 371 Celiac Patients


BMI (kg/m2 ) <20 20–24.9 ≥25 p
Total number of patients (% of total) 43 (12) 185 (50) 143 (39)
Demographics
Female patients (%) 34 (79) 137 (74) 86 (60) 0.0030
Mean age, yr (range) 51 (21–90) 48 (20–85) 46 (20–80) 0.2279
Presentation
Patients reporting diarrhea (%) 20 (47) 61 (33) 39 (27) 0.0237
Mean hemoglobin concentration, g/dL (range) 11.8 (5.6–15.7) 12.2 (6.0–16.7) 12.6 (6.4–17.4) 0.0270
Mean serum ionized calcium, mmol/L (range) 2.27 (1.62–2.50) 2.30 (2.03–2.61) 2.31 (1.91–2.60) 0.2925
Serology, histology
EmA +ve patients (%) 35 (81) 158 (85) 114 (80) 0.6192
Patients with subtotal/total villous atrophy (%) 40 (93) 134 (72) 96 (67) 0.0028

Commencing in 2000, every newly diagnosed patient had a 211 (57%) were normal, and 143 (39%) were overweight ac-
dual-energy x-ray absorptiometry (DEXA) scan performed cording to WHO criteria; in this last category, 48 (13% of
within 4 wk of diagnosis. Bone mineral density (BMD) val- the total population studied) were obese with BMI ≥ 30.0.
ues were recorded for the lumbar spine (L2–4) and neck of By gender, 57 (50%) of 114 men and 86 (33%) women were
left femur, and expressed in absolute figures (g/cm2 ) and as overweight, and 17 (15%) men and 31 (12%) women were
the number of standard deviations above or below the mean obese.
BMD of young adults of the same sex. The WHO defines There was a trend towards higher BMI in later years that
osteoporosis as a T score < –2.5 (6). did not reach statistical significance: mean BMI of patients
To assess the effect of gluten exclusion on BMI, we se- diagnosed from 1995 through 2000 was 24.0 (range 17.0–
lected those patients, initially EmA seropositive, who had 40.9), compared with 24.9 (16.3–43.5) from 2001 through
disappearance of serum EmA within 12 months and who 2005 (p = 0.076).
maintained their seronegative status as an objective indicator As patients meeting the WHO criterion for underweight
of dietary compliance (7). BMI after 2 yr gluten exclusion numbered only 17, we used a modified categorization for
was compared with that recorded at diagnosis. analysis of clinical characteristics: BMI <20, 20–24.9, and
Statistical analysis was performed using a statistical soft- 25 or over.
ware package (InStat, GraphPad Software, San Diego, CA). There was a significant association between low BMI and
Discrete variables were analyzed using the χ 2 test for trend female gender, diarrhea, reduced hemoglobin concentration,
and continuous variables by the Mann-Whitney U test for and higher grades (subtotal/total) of villous atrophy (Table 1).
two categories, Kruskal-Wallis one-way analysis for three, The DEXA scan data of 265 patients who underwent scan-
and the Wilcoxon signed-ranks test for paired variables. In ning at diagnosis are shown in Table 2. There was a significant
all cases p < 0.05 was taken as significant. upward trend in BMD of both lumbar spine and neck of fe-
mur with increasing BMI. Osteoporosis was present in only
6% of overweight patients in spine and/or femur, compared
RESULTS
with 48% in patients with BMI <20.
Over the study period, 371 patients were diagnosed as celiac A total of 188 patients meeting the stated criteria for com-
on the basis of duodenal villous atrophy, of which 257 (69%) pliance had BMI data recorded after 2-yr gluten exclusion.
were female. Apart from five completely asymptomatic in- Mean BMI rose from 24.4 to 25.9. On gluten exclusion,
dividuals identified by voluntary family screening, all had weight gain was recorded in 152 (81%), no change in 8 (4%),
one or more symptoms leading to the diagnosis. Diarrhea and loss in 28 (15%). Table 3 shows the pattern of weight
was reported as a symptom by 120 (32%). The mean BMI change for each category. After treatment, 82% of initially
was 24.6 (95% confidence interval 24.1–25.1); median 23.7, overweight patients had gained further weight and the pro-
range 16.3–43.5. Seventeen patients (5%) were underweight, portion of patients in the overweight category increased from

Table 2. Bone Density Data of 265 Patients Who Had DEXA Scanning at Diagnosis
BMI <20 20–24.9 ≥25 p
Total number of patients (% of total) 25 (9) 133 (50) 107 (40)
Mean BMD lumbar spine- g/cm2 (range) 0.926 (0.548–1.293) 1.075 (0.500–1.553) 1.169 (0.681–1.613) <0.0001
Mean BMD femoral neck- g/cm2 (range) 0.768(0.465–1.017) 0.907 (0.467–1.234) 0.966 (0.622–1.465) <0.0001
Patients with osteoporosis lumbar spine (%) 11 (44) 29 (22) 3 (3) <0.0001
Patients with osteoporosis neck femur (%) 9 (36) 17 (13) 3 (3) <0.0001
Patients with osteoporosis at either site (%) 12 (48) 33 (25) 6 (6) <0.0001
2358 Dickey and Kearney

Table 3. Effect of 2-yr Gluten Exclusion on BMI Category in 188 Patients


BMI Category After 2 yr
Initial BMI Category No. of Patients Patients Increasing Weight (%) <20 20–24.9 ≥25
<20 27 25 (93) 7 (26%) 18 (67%) 2 (7%)
20–24.9 94 72 (77) 1 (1%) 64 (68%) 29 (31%)
≥25 67 55 (82) 3 (4%) 64 (96%)

26% (67 patients) to 51% (95). Eleven patients in the over- (subtotal or total) in the low BMI group. There was no as-
weight and two in the normal BMI categories had BMIs in sociation between EmA positivity and BMI, in keeping with
the obese category after 2 yr, while only two patients left the observation by us and others (12, 13) that the clinical char-
obese group. acteristics of EmA negative patients do not differ from those
Records did not allow retrospective analysis of dietary ad- who are EmA positive. The variation in BMI may reflect
vice given regarding calorie restriction or of caloric intake of variations in the percentage of small bowel involved by the
patients before and after gluten exclusion. enteropathy. It is also possible that some untreated celiacs
modify their diets through trial and error to avoid symptoms
associated with the ingestion of gluten: this could also ex-
DISCUSSION plain the reduced prevalence of diarrhea among overweight
patients. While weight gain in underweight patients is ex-
This study included a large number of patients recruited from pected and desired following dietary gluten exclusion, this
a defined catchment area over a 10-yr period who underwent a was also observed in patients with normal BMI, of whom
standard protocol of initial investigation and follow-up under almost a third had entered the overweight category after 2
the supervision of a single gastroenterologist. As a result, yr, and in overweight patients. Studies of response to diet
we believe that the data included for analysis are valid and suggest that gluten exclusion is associated with a significant
reliable. To our knowledge, no similar study of BMI and increase in body fat stores, though these have been conducted
related clinical characteristics has been published to date. on patients with BMI significantly lower than healthy controls
In a small survey of 50 newly diagnosed patients that we (14, 15).
published in 1996 (3), 22% had BMI <20, 44% in the range There was a striking relationship between BMI and bone
20–24.9, and 34% ≥25. The current, larger study of patients density measurements. Only 6% of overweight patients had
diagnosed over a decade confirms that a minority (only 5%) osteoporosis in either lumbar spine or neck of femur, com-
of celiacs meet the WHO criteria for underweight at diagno- pared with 48% of patients with BMI <20. Previous studies
sis and that many (39%: 33% of women, 50% of men) are have reported a high prevalence of osteoporosis among celiac
overweight, with 13% (12% of women, 15% of men) in the patients (16, 17) prompting a call for routine DEXA scanning
obese category. These figures are similar to those of the gen- in all at diagnosis (18) and this has been our practice since
eral population of Northern Ireland: public health surveys of 2000. However, reduced BMD does not appear to translate
adults indicate that 27–58% of women and 47–58% of men into a large increase in fracture risk (19). Furthermore, a re-
are overweight and that 11–21% of women and 13–16% of cent English study of 43 patients found osteoporosis of the
men are obese (8). There has been little focused interest in hip and spine in only 7% and 14%, respectively, and ques-
BMI in celiac disease, though various studies that included tioned whether DEXA scanning is needed for all patients
BMI values as part of their patient demographics indicate (20). Their small study found a significant correlation be-
that celiac patients overweight at diagnosis are commonly tween BMI and BMD at the hip, but not at the spine. Though
observed. In a study comparing Finnish celiacs detected by analysis of other factors predictive of osteoporosis was be-
screening with those identified through symptoms (9), mean yond the remit of this study, BMI should be considered as
BMIs were 26.6 and 24.6, respectively, with 19% and 14% one important consideration in selecting celiac patients for
obese. West et al. (10) reported that of 2,649 English celiacs DEXA scanning.
with recorded BMI, 6% were underweight, 66% were normal, In conclusion, few celiac patients meet the underweight
and 28% were overweight (including 5% obese) by WHO cri- stereotype and almost half are overweight. Failure to recog-
teria. A recent North American study (11) found that 28% of nize this undoubtedly contributes to failed and delayed diag-
male celiacs (33% of females) had BMI less than 20, 41% nosis (21, 22), particularly as other “classic” symptoms like
(32%) 20–24.9, and 31% (26%) ≥25.0 (with 15% of men and diarrhea are less common in heavier patients. A high pro-
12% of women in the obese category). portion of overweight patients will gain further weight with
Our celiac patients with BMI <20 had significantly lower gluten exclusion. This represents a potential cause of morbid-
hemoglobin concentrations and were more likely to report ity that may counteract any benefits of diagnosis, particularly
diarrhea as a symptom, in keeping with a malabsorption pre- in patients identified by screening (1). Dietetic advisors need
sentation less evident in their overweight counterparts. This to recognize this and modify advice depending on BMI at
correlated with a higher prevalence of severe villous atrophy diagnosis.
Overweight in Celiac Disease 2359

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