Journal of Pediatric Gastroenterology & Nutrition:
The Gluten-Free Diet: A Nutritional Risk Factor for Adolescents with Celiac Disease?
Mariani, Paolo; Viti, Maria Grazia; Montouri, Monica; La Vecchia, Alessandra; Cipolletta, Elsa; Calvani, Luisa; Bonamico, Margherita
Istituto di Clinica Pediatrica Università "La Sapienza," Rome, Italy
Received October 7, 1997; revised February 12, 1998 and April 29, 1998; accepted May 14, 1998.
Address correspondence and reprint requests to Prof. M. Bonamico, Via Manlio di Veroli, 3/5, 00199 Rome, Italy.
Background: The gluten-free diet is the standard therapy for patients affected by celiac disease, although compliance with the diet is not optimal in adolescents or adults. Moreover, the gluten-free diet may induce nutritional imbalances.
Methods: Alimentary habits and diet composition were examined in 47 adolescents with celiac disease and 47 healthy aged-matched control subjects. All subjects compiled a 3-day alimentary record that allowed determination of their energy intakes; the macronutrient composition of their diets; and their iron, calcium, and fiber intakes. To evaluate compliance with the gluten-free diet, immunoglobulin A antigliadin and antiendomysium antibodies were assessed in all with celiac disease.
Results: The analysis of the records and the results of antibody levels showed that 25 subjects strictly followed dietetic prescriptions (group 1A), whereas 22 patients consumed gluten-containing food (group 1B). Those with celiac disease and control subjects (group 2) consumed a normocaloric diet. Lipid and protein consumption was high, however, and the consumption of carbohydrates low. Moreover, dietary levels of calcium, fiber, and especially in girls, iron, were low. These nutritional imbalances were significantly more evident in group 1A than in group 1B, as a consequence of poor alimentary choices. Moreover, in group 1A overweight and obesity were more frequent (72%) than in group 1B (51%) and in the control subjects (47%).
Conclusions: In people with celiac disease, adherence to a strict gluten-free diet worsens the already nutritionally unbalanced diet of adolescents, increasing elevated protein and lipid consumption. In the follow-up of patients with celiac disease, considerable effort has yet to be made to improve compliance with a gluten-free diet, and especially to control the nutritional balance of the diet in compliant patients.
The gluten-free diet represents the therapy for patients affected by celiac disease (CD) and must be adhered to throughout the patient's lifetime. However, several studies have shown that dietetic compliance in these patients frequently is not strict and that in adolescence correct diet is frequently neglected (1-5). Furthermore, it is well known that the alimentary patterns of healthy adolescents in industrialized countries are nutritionally unbalanced. In particular, they are often characterized by excessive consumption of energy, proteins, and fats, and a reduced intake of complex carbohydrates and fiber (6-10). Adherence to a strict gluten-free diet theoretically would worsen some of these alimentary excesses, because food prohibited in the diet of a patient with CD is mainly composed of complex carbohydrates.
The purpose of the present study was to evaluate compliance with diet in a group of adolescents with CD and to estimate their nutritional choices in intake of energy, macronutrients, iron, calcium and fiber and frequency of consumption of food.
MATERIALS AND METHODS
Forty-seven patients (group 1), 10 males and 37 females, aged from 10 to 20 years (mean age ± standard deviation, 15.2 ± 2.3 years; median age, 14.9 years), affected by CD diagnosed according to ESPGHAN criteria (11), were enrolled in the study. They were seen as outpatients at regular intervals at the Pediatric Clinic of Rome University "La Sapienza." Compliance with a gluten-free diet was evaluated by dietary record and verified by an assessment of antigliadin antibodies immunoglobulin (Ig) A and antiendomysium antibodies (12,13). Antigliadin antibody IgA was measured by enzyme-linked immunosorbent assay (Eurospital, Trieste, Italy) (14), and antiendomysium IgA was evaluated by an indirect immunofluorescence method (Biosystem, Milan, Italy). Sections from the distal portion of monkey esophagus were used as a substrate, and fluorescein-labeled goat antihuman IgA antibody was used as the second antibody. The patients' serum was diluted 2:5 in phosphate buffer (pH 7.2). The presence of a brilliant green network pattern under fluorescence microscope was taken as positive (12). No patient with IgA deficiency participated in the study.
All subjects compiled a 3-day alimentary record (2 weekdays plus Sunday) to evaluate energy consumption; percentage distribution of macronutrients; and calcium, iron and fiber intakes. An informative talk about how to compile the record and a dietetic interview to verify food weights in grams preceded the recording.
As a control group (group 2), we evaluated 47 healthy adolescents, 13 males and 34 females (mean age ± standard deviation, 15.7 ± 2.3 years; median age: 15.2 years) who compiled an alimentary record in a similar modality. As in the case of group 1, all subjects in the control group were middle and high school students in the Rome area.
Thirty of the 47 adolescents with CD (64%) reported strict compliance with a gluten-free diet, 14 (30%) admitted consumption of prohibited food once or twice a week, 3 (6%) acknowledged consuming a gluten-containing diet. However, when serologic markers were evaluated, 5 (16%) of the 30 patients who reported a strict gluten-free diet were antigliadin antibody IgA- and/or antiendomysium antibody-positive.
On the basis of these data, the actual compliance with the diet of our patients was 53% (25/47). It was therefore possible to compare the alimentary consumption of the 25 adolescents who complied with dietary prescriptions (group 1A) and that of the remaining 22 subjects who are gluten-containing foods (group 1B).
The patients of groups 1A and 1B did not show significant differences in distribution by sex, median age, weight (mean ± standard deviation, 52.5 ± 19 vs. 48.8 ± 17.6 kg, respectively) and height (mean ± standard deviation, 156.6 ± 25 vs. 152 ± 24 cm, respectively). Nutrient intake was compared with the Italian recommended consumption of nutrients (LARN 1996) (15) and with the United States recommended daily allowances (RDAs) (16). Statistical analysis was performed using Student's t-test.
Total energy consumption; the macronutrient division; and the iron, calcium, and fiber intakes in adolescents with CD and in control subjects, together with the reference values are shown in Table 1. Average percentages of nutrient intake (in comparison with RDAs) in the group with CD and in the control group, respectively, were: energy, 110.4 ± 26.3% and 117 ± 28%; carbohydrates, 71.5 ± 16.4% and 73 ± 16.8%; lipids, 106 ± 25% and 104.6 ± 24.7%; proteins, 129 ± 29.3% and 140 ± 31.7%. The percentages of subjects with adequate intakes of iron, calcium and fiber were similar in the group with CD (27%, 21% and 13%, respectively) and in the control group (21%, 17%, and 22%).
Total energy intake; the macronutrient division; and iron, calcium and fiber intakes in adolescents with CD complying with a gluten-free diet (group 1A) and in those consuming a gluten-containing diet (group 1B) are shown in Table 2. Average percentages of nutrient intake (in comparison with RDAs) in group 1A and in group 1B patients, respectively, were: calories, 115.2 ± 27.4% and 106 ± 25.2%; carbohydrates, 68 ± 15.6% and 75 ± 17%; lipids, 107 ± 25.4% and 105.3 ± 24.9%; proteins, 154 ± 35% and 109 ± 24%; calcium, 70 ± 36% and 50 ± 25%; and iron in males, 90 ± 31% and 72.8 ± 25% and in females, 88 ± 30.8% and 65 ± 22%. The frequency of consumption of different kinds of food inferred from alimentary records of the two groups of patients with CD is reported in Table 3. The distribution of real body weight (RBW) in patients with CD (groups 1A and 1B) and in control subjects is shown in Table 4.
The percentage of adolescents with CD who strictly follow a gluten-free diet varies from 43% to 81%, according to several studies (2,17-20); in the present study this percentage was 53%, confirming the need to make every effort to undertake a proper follow-up of patients with CD. On the whole, the alimentary habits of our patients show nutritional imbalances. In fact, compared with the Italian LARN (15) and to the United States RDA (16), our patients' diets are hyperproteinic and hyperlipidic and contain low amounts of carbohydrates, iron, calcium, and fiber.
As far as we know, only a few prior reports have been published on the alimentary habits of patients with CD, and these always concerned children on a gluten-free diet. Polito et al. (21) and Rea et al. (22) observed an excess in energy, animal protein, and lipid intake, which is partially responsible for the high percentage of overweight patients. However, Ansaldi et al. (23) observed a hypocaloric diet with the same macronutrient imbalances.
In our study, the presence of a control group of healthy adolescents and the division of those with CD in two subgroups according to their compliance with the diet allowed us to define better the nutritional choices that are induced by the elimination of gluten from the diet.
Comparing the alimentary habits of these groups, we noted that the nutritional imbalance of the diet of patients with CD was not the consequences of the elimination of gluten from the diet, because even the healthy adolescents' diet was hyperproteinic and hyperlipidic and therefore, low in carbohydrates. Moreover, an adequate amount of iron, calcium, and fiber was part of the diet in only 20% of all adolescents, with or without CD. These results are not surprising. They confirm results of nutritional investigations of adolescents in industrialized countries during recent years (6-10).
The relevant data are those obtained through the comparison of nutritional choices of patients with CD who consume a strict gluten-free diet with those of patients with CD who consume a gluten-containing diet. Energy intake was higher in group 1A than in group 1B, particularly in the girls; but this difference did not reach statistical significance. As far as the percentage distribution of macronutrients is concerned, protein intake was significantly higher and carbohydrate intake was significantly lower in group 1A patients than in group 1B patients. Furthermore, patients with CD complying with a strict gluten-free diet consumed a higher amount of lipids than the gluten-consuming group, although these data are not statistically significant. Even fiber consumption was significantly reduced in subjects consuming a gluten-free diet, whereas intakes of iron and calcium were increased. Therefore, in patients with CD, adherence to a strict gluten-free diet worsens the already nutritionally unbalanced diet of all adolescents, increasing the already elevated protein and lipid consumption.
To understand the origin of these incorrect dietary habits, we evaluated the frequency of consumption of different kinds of foods. It was obvious that among patients with CD consuming a gluten-free diet the reduced consumption of some foods containing carbohydrates such as bread, pizza, or pasta was not counterbalanced by an increase of alimentary items of the same group (rice, corn, and potatoes). Group 1A patients preferred food with a high amount of protein (meat, eggs, legumes) and snacks with a high content of lipids much more often than group 1B patients. The greater consumption of meat and legumes by group 1A patients was responsible for the higher intake of iron and fiber.
There was no connection between the calcium intake recorded, which was greater among patients in group 1A, and the frequency of milk consumption and its products, which was similar in the two subgroups. Basically, a diligent analysis of alimentary records showed a greater consumption of parmesan cheese in patients in group 1A, possibly to make pasta more appetizing.
The distribution of real body weight in patients with CD revealed a greater percentage of overweight and obese adolescents among those who complied with dietetic prescriptions (72%) than among subjects consuming an unrestricted diet (51%). We speculate that the dietetic habits (high energy, protein and lipid intake, combined with low carbohydrate consumption) in patients with CD consuming a gluten-free diet with a normal small bowel mucosa could cause a disturbance in the growth pattern.
The results of the present study provide a discouraging description of the alimentary habits of adolescents with CD, in the poor compliance with diet in a high percentage of subjects and in the presence of nutritional imbalances, particularly in those consuming a strict gluten-free diet. This last observation could be partially explained by the adolescents' infrequent consumption of gluten-free commercial foods, because of poor palatability, and the cost and difficulty of obtaining more palatable food. To solve these problems, it would be useful if a nutritionist advised patients on dietary control during periodic medical checks, particularly during adolescence.
In conclusion, our results show that, paradoxically, in adolescents with CD, a strict gluten-free diet may be a nutritional risk factor, altering the already unbalanced diet commonly consumed by healthy adolescents, because it leads these subjects to incorrect alimentary choices.
Although in the past years there has been great improvement in diagnostic tools for CD, we believe the moment has come to devote more attention to problems regarding a correct follow-up of CD, not only the compliance with diet, but also the nutritional balance of the diet itself.
1. Montgomery AMP, Goka AKJ, Kumar PJ, Earthing MJG, Clark ML. Low gluten diet in the treatment of adult celiac disease: Effect on jejunal morphology and serum antigluten antibodies. Gut
2. Colaco J, Egan-Mitchell B, Stevens FM, Eottrell PF, McCarthy CF, McNichol F. Compliance with gluten-free diet in coeliac disease. Arch Dis Child
3. Kumar PJ, Walker-Smith J, Milla P, Harris G, Colyer J, Halliday R. The teenage coeliac: Follow-up study of 102 patients. Arch Dis Child
4. Kokkonen J, Viitanen A, Simila S. Coping with a coeliac diet after adolescence. Helv Paediatr Acta
5. Mayer M, Greco L, Troncone R, Auricchio S, Marsh MN. Compliance of adolescents with coeliac disease with a gluten-free diet. Gut
6. Giovannini M, Galluzzo C, Scaglioni S, et al. Indagine nutrizionale nel comune di Milano: Dati antropometrici, intake calorici e abitudini alimentari in età scolare. Riv Ital Pediatr
7. Pinelli L, Cirillo D, Golinelli M, et al. Indagini su apporti alimentari e dati antropometrici nell' età scolare. Rilievi su un campione di 1177 bambini del comune di Verona. Riv Ital Pediatr
8. Spyckerelle Y, Herbert B, Didelot-Barthélemy L, Bairati I, Deschamps JP. Alimentation des adelescentes en Lorraine. Arch Fr Pediatr
9. Skinner JD, Salvetti NN, Enzel EM. Appalachian adolescent's eating patterns and nutrient intakes. J Am Diet Assoc
10. Doyle W, Jenkins S, Crawford MA, Puvandendran K. Nutritional status of schoolchildren in an inner city area. Arch Dis Child
11. Walker-Smith JA, Guandalini S, Schmitz J, Shmerling DH, Visakorpi JK. Revised criteria for diagnosis of coeliac disease. Arch Dis Child
12. Burgin-Wolff A, Gaze H, Hadzielimovic F, et al. Antigliadin and antiendomysium antibody determination for coeliac disease. Arch Dis Child
13. Gemme G, Delogu A, Nobili F, et al. Anticorpi antiendomisio: Ruolo attuale nella diagnosi di malattia celiaca a confronto con gli anticorpi antigliadina. Pediatr Med Chir
14. Savilahti E, Perkkio M, Kalimo K. IgA antigliadin antibodies: A marker of mucosal damage in childhood coeliac disease. Lancet
15. Società Italiana di Nutrizione Umana. Livelli di assunzione raccomandati di energia e nutrienti per la popolazione italiana. LARN Revisione
16. Recommended daily allowances. Nutr Rev
17. Savilahti E, Simmel O, Koskimies S, Riva A, Akerblorn HK. Celiac disease in insulin-dependent diabetes mellitus. J Pediatr
18. Maki M, Lahdehaho ML, Halstromm O, Viander M, Visakorpi JK. Postpubertal challenge in coeliac disease. Arch Dis Child
19. Ljungman G, Myrdal U. Compliance in teenagers with coeliac disease: A Swedish follow-up study. Acta Paediatr
20. Bardella MT, Molteni N, Prampolini L, et al. Need for follow-up in coeliac disease. Arch Dis Child
21. Polito C, Olivieri AC, Marchese L, et al. Weight overgrowth of coeliac children on gluten-free diet. Nutr Res
22. Rea F, Polito C, Marotta A, et al. Restoration of body composition in celiac children after one year of gluten-free diet. J Pediatr Gastroenterol Nutr
23. Ansaldi N, Palma L, Dell' Olio D, Malorgio E, Che cosa mangiano i bambini celiaci? Analisi dietologica su un gruppo di celiaci a dieta. Riv Ital Pediatr
This article has been cited 52 time(s).
Frontiers in Human NeuroscienceGluten- and casein-free dietary intervention for autism spectrum conditionsFrontiers in Human Neuroscience
World Journal of GastroenterologyCardiovascular disease risk factor profiles in children with celiac disease on gluten-free dietsWorld Journal of Gastroenterology
Specific features of rehabilitation in patients with gluten-sensitivity celiac disease
Terapevticheskii Arkhiv, 85(1):
DigestionInadequate Nutrient Intake in Patients with Celiac Disease: Results from a German Dietary SurveyDigestion
Revista De Nutricao-Brazilian Journal of Nutrition
Nutritional evaluation and food intake of celiac disease patients compliant or not with a gluten-free diet
Revista De Nutricao-Brazilian Journal of Nutrition, 26(3):
Journal of Psychosomatic ResearchCoeliac disease, diet adherence and depressive symptomsJournal of Psychosomatic Research
American Journal of Gastroenterology
Radioimmunoassay to detect antitransglutaminase autoantibodies is the most sensitive and specific screening method for celiac disease
American Journal of Gastroenterology, 96(5):
American Journal of Clinical Nutrition
Body composition and dietary intakes in adult celiac disease patients consuming a strict gluten-free diet
American Journal of Clinical Nutrition, 72(4):
European Journal of Gastroenterology & Hepatology
Consumption of gluten-free products: should the threshold value for trace amounts of gluten be at 20, 100 or 200 p.p.m.?
European Journal of Gastroenterology & Hepatology, 18():
Scandinavian Journal of GastroenterologyTef in the diet of celiac patients in The NetherlandsScandinavian Journal of Gastroenterology
Trends in Food Science & TechnologyNutritive value of pseudocereals and their increasing use as functional gluten-free ingredientsTrends in Food Science & Technology
Digestive Diseases and SciencesIntestinal permeability in long-term follow-up of patients with celiac disease on a gluten-free dietDigestive Diseases and Sciences
Alimentary Pharmacology & TherapeuticsClinical trial: B vitamins improve health in patients with coeliac disease living on a gluten-free dietAlimentary Pharmacology & Therapeutics
Biomedicine & Pharmacotherapy
Clinical features of coeliac disease today
Biomedicine & Pharmacotherapy, 54(7):
GastroenterologyConsequences of testing for celiac diseaseGastroenterology
GastroenterologyDietary guidelines and implementation for celiac diseaseGastroenterology
Acta PaediatricaA boy with coeliac disease and obesityActa Paediatrica
Alimentary Pharmacology & TherapeuticsFuture research on coeliac disease - a position report from the European multistakeholder platform on coeliac disease (CDEUSSA)Alimentary Pharmacology & Therapeutics
Alimentary Pharmacology & TherapeuticsRadioimmunological detection of anti-transglutaminase autoantibodies in human saliva: a useful test to monitor coeliac disease follow-upAlimentary Pharmacology & Therapeutics
Digestive Diseases and SciencesA Comparison of Antibody Testing, Permeability Testing, and Zonulin Levels with Small-Bowel Biopsy in Celiac Disease Patients on a Gluten-Free DietDigestive Diseases and Sciences
Journal of Food Quality
Physicochemical properties of gluten-free pancakes from rice and sweet potato flours
Journal of Food Quality, 29(1):
European Food Research and TechnologyEvaluation of the nutritional quality of the lipid fraction of gluten-free biscuitsEuropean Food Research and Technology
PediatricsDiagnosing Celiac disease with a positive serological test and without an intestinal biopsyPediatrics
World Journal of GastroenterologyA Brazilian experience of the self transglutaminase-based test for celiac disease case finding and diet monitoringWorld Journal of Gastroenterology
Journal of Human Nutrition and Dietetics
The everyday life of adolescent coeliacs: issues of importance for compliance with the gluten-free diet
Journal of Human Nutrition and Dietetics, 21(4):
American Journal of Clinical Nutrition
Body composition in children with celiac disease and the effects of a gluten-free diet: a prospective case-control study
American Journal of Clinical Nutrition, 72(1):
Acta DiabetologicaBody composition in coeliac disease adolescents on a gluten-free diet: a longitudinal studyActa Diabetologica
Alimentary Pharmacology & Therapeutics
Evidence of poor vitamin status in coeliac patients on a gluten-free diet for 10 years
Alimentary Pharmacology & Therapeutics, 16(7):
Health Technology Assessment
Autoantibody testing in children with newly diagnosed type 1 diabetes mellitus
Health Technology Assessment, 8():
Pediatric Clinics of North AmericaNutritional Deficiencies in Children on Restricted DietsPediatric Clinics of North America
Journal of Human Nutrition and DieteticsDietary shortcomings in children on a gluten-free dietJournal of Human Nutrition and Dietetics
American Journal of Gastroenterology
Assessment of body composition by bioelectrical impedance in adolescent patients with celiac disease
American Journal of Gastroenterology, 94():
American Journal of Gastroenterology
Importance of gluten in the induction of endocrine autoantibodies and organ dysfunction in adolescent celiac patients
American Journal of Gastroenterology, 95(7):
Clinical features of children with screening-identified evidence of celiac disease
Canadian Journal of Gastroenterology
Long-term follow-up of individuals with celiac disease: An evaluation of current practice guidelines
Canadian Journal of Gastroenterology, 21(9):
Food MicrobiologySourdough in gluten-free bread-making: An ancient technology to solve a novel issue?Food Microbiology
Journal of Human Nutrition and Dietetics
Gluten-free diet survey: are Americans with coeliac disease consuming recommended amounts of fibre, iron, calcium and grain foods?
Journal of Human Nutrition and Dietetics, 18(3):
European Food Research and TechnologyIdentification of lactic acid bacteria isolated from oat sourdoughs and investigation into their potential for the improvement of oat bread qualityEuropean Food Research and Technology
Trends in Food Science & TechnologyRecent advances in the formulation of gluten-free cereal-based productsTrends in Food Science & Technology
Acta Gastro-Enterologica Belgica
High fat consumption in children with celiac disease
Acta Gastro-Enterologica Belgica, 72(3):
Digestive and Liver DiseaseImpact of gluten-free diet on cardiovascular risk factors. A retrospective analysis in a large cohort of coeliac patientsDigestive and Liver Disease
Nutrition Metabolism and Cardiovascular DiseasesChanges of body mass index in celiac children on a gluten-free dietNutrition Metabolism and Cardiovascular Diseases
Current Opinion in GastroenterologyVitamin D status in gastrointestinal and liver diseaseCurrent Opinion in Gastroenterology
Journal of Pediatric Gastroenterology and NutritionObesity in an 18-Year-Old Boy With Untreated Celiac DiseaseJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionAntiendomysial Antibody Detection in Biopsy Culture Allows Avoidance of Gluten Challenge in Celiac ChildrenJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionNutritional Management of the Gluten-free Diet in Young People with Celiac Disease in The NetherlandsJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionAtypical Celiac Disease Presenting as Obesity-Related Liver DysfunctionJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionCompliance With Gluten-free Diet in Children With Coeliac DiseaseJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionBone Quantitative Ultrasound and Bone Mineral Density in Children with Celiac DiseaseJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionTreatment Regimen Adherence in Pediatric GastroenterologyJournal of Pediatric Gastroenterology and Nutrition
Journal of Pediatric Gastroenterology and NutritionLiving Well With Celiac Disease?Journal of Pediatric Gastroenterology and Nutrition
Adolescents; Alimentary habits; Celiac disease; Gluten-free diet
© 1998 Lippincott Williams & Wilkins, Inc.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Highlight selected keywords in the article text.
Data is temporarily unavailable. Please try again soon.