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2 January 2014

Celiac Disease and Overweight in Children: An Update

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1
Gastroenterology-Hepatology and Nutrition Unit, "Bambino Gesù" Children's Hospital, Piazza Sant'Onofrio 4, Rome 00165, Italy
2
Gastroenterology Unit, Pediatric Clinic of University, Piazza Giulio Cesare 11, Bari 70124, Italy
3
Epidemiology and Biostatistics Unit, "Bambino Gesù" Children's Hospital, Piazza Sant'Onofrio 4, Rome 00165, Italy
*
Author to whom correspondence should be addressed.
Nutrients2014, 6(1), 207-220;https://doi.org/10.3390/nu6010207
This article belongs to the Special Issue Nutrition and Celiac Disease
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Abstract

The clinical presentation of celiac disease in children is very variable and differs with age. The prevalence of atypical presentations of celiac disease has increased over the past 2 decades. Several studies in adults and children with celiac disease indicate that obesity/overweight at disease onset is not unusual. In addition, there is a trend towards the development of overweight/obesity in celiac patients who strictly comply with a gluten-free diet. However, the pathogenesis and clinical implications of the coexistence of classic malabsorption (e.g., celiac disease) and overweight/obesity remain unclear. This review investigated the causes and main clinical factors associated with overweight/obesity at the diagnosis of celiac disease and clarified whether gluten withdrawal affects the current trends of the nutritional status of celiac disease patients.

1. Introduction

Celiac disease (CD) is a life-long condition that affects the small intestine in genetically susceptible individuals [1]. The global prevalence ranges from 1% to 2% [2,3]. In children, the symptoms upon CD presentation are highly variable and are influenced by age. Very young children often present with “classic” symptoms including diarrhea, abdominal distension, and growth retardation [4,5,6]. Diarrhea and malabsorption represent the typical presentation of CD in young children [7], while abdominal pain, vomiting, and constipation are atypical gastrointestinal symptoms more common in older children and teenagers. Furthermore, in children, CD can be diagnosed on the basis of the occurrence of extra-intestinal conditions such as arthritis, neurological diseases, and anemia [8,9] or on the basis of screening procedures in the absence of gastrointestinal symptoms (typical or atypical) and in child or adolescent with CD- associated conditions [10].
The presentation of CD has changed over time. In the last 2 decades, diarrhea and malabsorption have progressively decreased as the mode of CD onset among both adults and children, whereas atypical manifestations have increased. Interestingly, many reports indicate that CD can be associated with overweight or normal weight; hence, malnutrition is not always present at CD presentation [4,6,11,12]. Therefore, CD and obesity can coexist during both childhood and adolescence. After the first 2 cases reported by Semeraro [13] and Conti-Nibali [14] in 1986 and 1987, respectively, there have been several reports of the coexistence of CD and obesity/overweight in children and adolescents in the last 2 decades [15,16,17,18,19].
At present, in pediatric [20,21,22,23,24,25,26,27] and adult [28,29,30,31,32,33] case series of CD, the body mass index (BMI) at diagnosis is within the normal range in many patients. Nevertheless, the pathogenesis and clinical implications of the coexistence of CD and overweight/obesity remain unclear. The clinical relevance of this association is highlighted by the observation that CD patients with normal weight or overweight at diagnosis have a higher risk of developing obesity after starting a gluten-free diet (GFD), which definitely improves intestinal absorption in these patients. Moreover, the GFD regimen appears to be associated with high lipid and protein intake, particularly in adolescents [20,29].
The key studies concerning the pathogenesis and clinical evidence of the association between CD and overweight/obesity in subjects aged <18 years are discussed below. This review investigated the causes and main clinical factors associated with overweight/obesity at CD diagnosis. In addition, this review aims to clarify if gluten withdrawal affects the trend of the nutritional status of CD patients.

2. Clinical Evidence of CD and Overweight/Obesity

2.1. Summary of the Main Case Reports

The first pediatric case report [13] by Semeraro et al., in 1986 describes an obese 14-year-old girl who had been diagnosed with CD at the age of 1 year on the basis of a clinical condition characterized by malabsorption, diarrhea, and stunted growth (i.e., weight in the 7th percentile). The girl was started on a GFD, and had a normal weight at 2 years of age; however, she was overweight at 5 years of age and obese at 10. She had a negative family history for endocrine diseases and CD but a positive family history for obesity.
There are other reports of the development of obesity in children on a GFD who initially had malabsorption. For example Czaja-Bulsa et al. [15] describe the case of an 18-year-old boy with growth failure (i.e., <3rd percentile) and chronic diarrhea following gluten introduction and before CD diagnosis. However, after gluten withdrawal, his weight increased to the 97th percentile at 5 years of age despite persistent mucosal atrophy. More recently, Balamtekin et al. [19] reported a similar case of a 21-month-old child with the classic condition of malabsorption (i.e., chronic diarrhea, failure to thrive, and abdominal distension) at CD onset. After 11 years on a GFD, the child became obese (weight, >97th percentile).
Meanwhile, there are other reports of children with overweight/obesity at the time of CD diagnosis. The first published report describes a 5-year-old girl with obesity, short stature, and recurrent abdominal pain. The diagnosis of CD was suspected on the basis of family history, i.e., a sister with CD. A GFD attenuated the symptoms and improved height and weight growth [14]. Furthermore, in 2001, Franzese et al. [16] reported the case of a patient with steatohepatitis associated with obesity resistant to a low-calorie diet, in which CD was diagnosed on the basis of moderate persistent hypertransaminasemia. In 2006, Oso and Fraser [17] diagnosed CD in an obese teenager who had recurrent episodes of diarrhea, especially after eating spaghetti. At diagnosis, blood tests revealed low iron, GFD feeding normalized iron level, and the symptoms disappeared. However, the patient continued to gain weight (10 kg over 6 months) during follow-up. In 2009, Arslan et al. [18] reported the case of a 7-year-old obese patient with CD (weight, >95th percentile; weight/height ratio, 167%) suspected of having Hashimoto’s thyroiditis and affected by hypochromic anemia unresponsive to iron therapy. Moreover, Balamtekin et al. [19] describe the case of a 17-year-old obese girl with weight >97th percentile and a BMI of 32.9 with epigastric pain and vomiting. CD was diagnosed on the basis of the gastrointestinal symptoms, and the symptoms disappeared after a GFD was started. Nevertheless, her weight continued to increase.

2.2. Summary of Case Series

At present, few case series have been published on this topic. Valletta et al. [24] report the prevalence of overweight (BMI z-score > +1) and obesity (BMI z-score > +2) to be 11% and 3%, respectively, in 149 children newly diagnosed with CD between 1991 and 2007. The authors found that after initiating a GFD, the BMI z-score increased significantly and the percentage of overweight subjects almost doubled. In a retrospective study, Venkatasubramani et al. [22] report 5% of patients had a BMI > 95th percentile among 143 patients with CD diagnosed between 1986 and 2003. Among the obese patients, the most common symptoms at onset were abdominal pain, diabetes, and diarrhea.
Brambilla et al. [25] compared 150 children with CD on a GFD with 288 healthy sex- and age-matched children. They also retrospectively evaluated changes in BMI from CD diagnosis to the last clinical evaluation. The median BMI of CD patients was significantly lower than that of the healthy controls. In particular, children with CD were less frequently overweight or obese (12% vs. 23.3%) and more frequently underweight (16% vs. 4.5%) than the controls. However, after GFD feeding, the number of underweight subjects decreased significantly, while the number of overweight subjects increased slightly.
Reilly et al. [26] studied 142 children with newly diagnosed CD from 2000 to 2008. Nearly 19% of patients had a high BMI at diagnosis (12.6% overweight and 6% obese), while 74.5% had a normal BMI. Meanwhile, the BMI of 75% of the patients with high BMI at diagnosis decreased on a GFD. Among patients with a normal BMI at diagnosis, weight z-scores increased significantly after diet treatment and 13% became overweight. Interestingly, in that survey, the initial symptom in 28% of overweight CD patients was abdominal pain and the diagnosis was made on the basis of the screening test in a asymptomatic portion of the population by 28%. Venkatasubramani et al. [22] also found abdominal pain is one of the most common features of CD presentation in overweight patients. Another important aspect of their survey results is that the CD diagnosis was made on the basis of the screening test in at least 25% of overweight patients. Brambilla et al. [25] suggest that identifying CD patients on the basis of screening tests, and not symptoms, may increase the probability of finding overweight or obese subjects at CD diagnosis.
In a cross-sectional multicenter study, Norsa et al. [27] enrolled 114 children with CD in serologic remission, who were on a GFD for at least 1 year. The anthropometric measurements at diagnosis revealed that 9.6%, 76.3%, 8.8%, and 5.3% were underweight (BMI < 5th percentile), had normal weight (BMI = 5–85th percentile), were overweight (BMI = 85–95th percentile), and were obese (BMI > 95th percentile), respectively. After gluten withdrawal, the prevalence of overweight and obesity increased to 11.4% and 8%, respectively.
In a prospective case–control study, Barera et al. [34] found reduced fat mass, decreased bone mineral content, and lower lean body mass in the limbs of 29 children newly diagnosed with CD compared to healthy controls; all patients were normalized (i.e., approaching corresponding parameters in the control population) on a GFD. Table 1 summarizes the main results of the abovementioned reports.
Table
Table 1. Prevalence of overweight/obesity in CD.
Table 1. Prevalence of overweight/obesity in CD.
Author (Year)Country (Sample Size)Overweight/Obesity at Presentation (%)Overweight/Obesity after Initiating a GFD (%)Reference
Aurangzeb (2010)Australia & New Zealand (n = 25)20.8/0ND/ND[21]
Venkatasubramani (2010)Milwaukee, WI, USA (n = 143)ND/5ND/3[22]
Balamtekin (2010)Ankara, Turkey (n = 220)ND/0.5ND/ND[23]
Valletta et al. (2010)Italy (n = 149)11/321/4[24]
Reilly et al. (2010)NY, USA (n = 142)12.6/620/4[26]
Norsa et al. (2011)Italy & Israel (n = 114)8.8/5.311.5/8.8[27]
Brambilla et al. (2011)Italy (n = 150)11.3/0.79.4/0[25]
GFD: gluten-free diet; ND: not done.
A clarification regarding the methodology of these studies should be made: in adults and children, the main criterion for defining overweight/obesity is BMI (or Quetelet index), which is calculated by dividing weight (in kg) by height (in m) squared. BMI is an expression of the weight “adjusted” to stature and is an index of adiposity; it is most strongly correlated with body fat and less correlated with stature. Despite its limitations, BMI is easy to calculate and widely used, especially in large-scale studies, to assess the risks of diseases. The internationally accepted age- and sex-standardized threshold values of BMI for nutritional status in adults are those proposed by the World Health Organization [35]. However, the curves of children’s weight and height vary with growth, following development during puberty (with its consequences on body composition), and sex. Therefore, references for different age groups (i.e., the distribution of percentiles with cut-off points) are necessary. There are many different percentile tables based on data from reference populations that also have very different anthropometric characteristics. Ideally, the study population should be compared with tables based on national curves. Alternatively, the International Obesity Task Force (IOTF), which is the main organization of childhood obesity scholars, have validated tables with mean percentiles derived from cross-sectional studies of different populations (e.g., the USA, Brazil, Hong Kong, Singapore, Holland, and Great Britain) to enable international comparisons [36].
In this regard, the abovementioned studies have a discrete methodological heterogeneity. Although all are based on the calculation of BMI, they used different categorizations in various case series, such as the BMI percentile, BMI z-score, and IOTF cut-off point. In addition, different studies were conducted on geographically diverse populations, and only a few studies compared the case population with a control population [21,25].

4. Conclusions

Overweight/obesity is more common in children with CD than previously recognized. The prevalence of overweight in CD patients at diagnosis ranges from 8.8% to 20.8% [21,24,25,26,27], whereas that in CD patients on a GFD ranges from 9.4% to 21% [23,24,25,26]. Meanwhile, the prevalence of obesity in CD patients at diagnosis ranges from 0% to 6% [21,22,23,24,25,26,27], whereas that in CD patients on a GFD ranges from 0% to 8.8% [22,24,25,26,27]. Overweight/obesity is more frequent in newly diagnosed CD patients diagnosed on the basis of abdominal pain [22,26] and on the basis of screening procedures [25,26]. During follow-up, it is possible the unpalatability of gluten-free foods leads a preference for foods with high caloric fat and protein contents. However, the occurrence of overweight may be explained by the global trend toward overweight/obesity in children [39] including CD patients. An unconfirmed but nonetheless interesting hypothesis is that the development of overnutrition status is due to the compensatory high energetic yield secondary to the slow functional adaptation of the atrophic mucosa [13]. Therefore, mounting evidence suggests CD should be considered even in overweight/obese children in appropriate clinical settings.

Conflicts of Interest

The authors declare no conflict of interest.

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Effects of Vitamin A Supplementation on Iron Status Indices and Iron Deficiency Anaemia: A Randomized Controlled Trial
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