European Journal of Nutrition

, Volume 58, Issue 2, pp 775–783 | Cite as

Gluten-free-rendered products contribute to imbalanced diets in children and adolescents with celiac disease

  • I. Larretxi
  • E. Simon
  • L. Benjumea
  • J. Miranda
  • M. A. Bustamante
  • A. LasaEmail author
  • F. J. Eizaguirre
  • I. Churruca
Original Contribution



As well as adhering to the safe limit for gluten intake, a suitable gluten-free (GF) diet must also be nutritionally balanced. However, malnutrition has been observed in the population with celiac disease (CD). This is even more important in the case of children and adolescents, whose GF diet must also ensure their proper growth. The aim of the present study was to assess the diet quality of children and adolescents with CD to attain optimal nutritional status, determining the most relevant factors that affect a balanced diet.


Eighty-three children and adolescents with CD (9.2 ± 3.8 years) took part in the study. Height, weight and body composition were measured. An analysis of energy consumption and of the macronutrient distribution of their diet was carried out. Adherence to Mediterranean diet by KIDMED index was analyzed, and energy and nutrients intake.


The diet of participants was not balanced, containing more fat and less carbohydrate than recommended. Most children and adolescents revealed adequate body mass index and suitable body fat percentage. Two-thirds of them showed moderate or poor KIDMED index, the case of girls being remarkable. When the GF diet, containing GF-rendered foodstuffs, was compared to a similar type of diet but substituting GF products with their analogs containing gluten, important nutritional differences were revealed.


Even though celiac children and adolescents’ diet is unhealthy due to its inappropriate dietary pattern, following a diet based on GF products raises extra difficulty in complying with the nutritional recommendations.


Gluten-free products Celiac disease Dietary unbalance KIDMED index Children Adolescents 



This research was supported by grants from the University of the Basque Country (University-Society US12/10 and US15/06) and a grant from the Basque Government (Proyectos de Investigación Focalizada Agricultura PA15/01). Idoia Larretxi is a PhD scholar of the University of the Basque Country, UPV/EHU (Euskararen eta Etengabeko Prestakuntzaren arloko Errektoreordetza). We thank the collaboration of Hospital Universitario Donostia and “Federación Española de Asociaciones de Celiacos” (FACE), specifically that of Mireia Apraiz (EZE).

Author contributions

IL and MAB performed the anthropometric measurements and collected questionnaires. FJE and LB recruited the patients, performed anthropometric measurements and collected questionnaires. IC and ES carried out the experimental design and analyzed data. JM and AL wrote the manuscript.

Compliance with ethical standards

Conflict of interest

Authors declare no conflict of interest.

Supplementary material

394_2018_1685_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 KB)


  1. 1.
    Bai JC, Ciacci C (2017) World gastroenterology organisation global guidelines: celiac disease February 2017. J Clin Gastroenterol 51(9):755–768. CrossRefPubMedGoogle Scholar
  2. 2.
    Ludvigsson JF, Leffler DA, Bai JC, Biagi F, Fasano A, Green PH, Hadjivassiliou M, Kaukinen K, Kelly CP, Leonard JN, Lundin KE, Murray JA, Sanders DS, Walker MM, Zingone F, Ciacci C (2013) The Oslo definitions for coeliac disease and related terms. Gut 62(1):43–52. CrossRefPubMedGoogle Scholar
  3. 3.
    Catassi C, Gatti S, Fasano A (2014) The new epidemiology of celiac disease. J Pediatr Gastroenterol Nutr 59(Suppl 1):S7–S9. CrossRefPubMedGoogle Scholar
  4. 4.
    Mariné M, Farre C, Alsina M, Vilar P, Cortijo M, Salas A, Fernández-Bañares F, Rosinach M, Santaolalla R, Loras C, Marquès T, Cusí V, Hernández MI, Carrasco A, Ribes J, Viver JM, Esteve M (2011) The prevalence of coeliac disease is significantly higher in children compared with adults. Aliment Pharmacol Ther 33(4):477–486. CrossRefPubMedGoogle Scholar
  5. 5.
    Capristo E, Malandrino N, Farnetti S, Mingrone G, Leggio L, Addolorato G, Gasbarrini G (2009) Increased serum high-density lipoprotein-cholesterol concentration in celiac disease after gluten-free diet treatment correlates with body fat stores. J Clin Gastroenterol 43(10):946–949. CrossRefPubMedGoogle Scholar
  6. 6.
    Wierdsma NJ, van Bokhorst-de van der Schueren MA, Berkenpas M, Mulder CJ, van Bodegraven AA (2013) Vitamin and mineral deficiencies are highly prevalent in newly diagnosed celiac disease patients. Nutrients 5(10):3975–3992. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Dickey W, Kearney N (2006) Overweight in celiac disease: prevalence, clinical characteristics, and effect of a gluten-free diet. Am J Gastroenterol 101(10):2356–2359. CrossRefPubMedGoogle Scholar
  8. 8.
    Snyder J, Butzner JD, DeFelice AR, Fasano A, Guandalini S, Liu E, Newton KP (2016) Evidence-informed expert recommendations for the management of celiac disease in children. Pediatrics. CrossRefPubMedGoogle Scholar
  9. 9.
    Valitutti F, Trovato CM, Montuori M, Cucchiara S (2017) Pediatric celiac disease: follow-up in the spotlight. Adv Nutr 8(2):356–361. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Wild D, Robins GG, Burley VJ, Howdle PD (2010) Evidence of high sugar intake, and low fibre and mineral intake, in the gluten-free diet. Aliment Pharmacol Ther 32(4):573–581. CrossRefPubMedGoogle Scholar
  11. 11.
    Whitton C, Nicholson SK, Roberts C, Prynne CJ, Pot GK, Olson A, Fitt E, Cole D, Teucher B, Bates B, Henderson H, Pigott S, Deverill C, Swan G, Stephen AM (2011) National diet and nutrition survey: UK food consumption and nutrient intakes from the first year of the rolling programme and comparisons with previous surveys. Br J Nutr 106(12):1899–1914. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Størsrud S, Hulthén LR, Lenner RA (2003) Beneficial effects of oats in the gluten-free diet of adults with special reference to nutrient status, symptoms and subjective experiences. Br J Nutr 90(1):101–107. CrossRefPubMedGoogle Scholar
  13. 13.
    Thompson T, Dennis M, Higgins LA, Lee AR, Sharrett MK (2005) Gluten-free diet survey: are Americans with coeliac disease consuming recommended amounts of fibre, iron, calcium and grain foods? J Hum Nutr Diet 18(3):163–169. CrossRefPubMedGoogle Scholar
  14. 14.
    Miranda J, Lasa A, Bustamante MA, Churruca I, Simon E (2014) Nutritional differences between a gluten-free diet and a diet containing equivalent products with gluten. Plant Foods Hum Nutr 69(2):182–187. CrossRefPubMedGoogle Scholar
  15. 15.
    Thompson T (1999) Thiamin, riboflavin, and niacin contents of the gluten-free diet: is there cause for concern? J Am Diet Assoc 99(7):858–862. CrossRefPubMedGoogle Scholar
  16. 16.
    Saturni L, Ferretti G, Bacchetti T (2010) The gluten-free diet: safety and nutritional quality. Nutrients 2(1):16–34. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Dell’Olio D, Palma L, Malorgio E, Ansaldi Balocco N (1995) What do celiac children eat? Dietary analysis of a group of children with celiac disease on a diet. Minerva Gastroenterol Dietol 41(4):269–273PubMedGoogle Scholar
  18. 18.
    Ohlund K, Olsson C, Hernell O, Ohlund I (2010) Dietary shortcomings in children on a gluten-free diet. J Hum Nutr Diet 23(3):294–300. CrossRefPubMedGoogle Scholar
  19. 19.
    Mariani P, Viti MG, Montuori M, La Vecchia A, Cipolletta E, Calvani L, Bonamico M (1998) The gluten-free diet: a nutritional risk factor for adolescents with celiac disease? J Pediatr Gastroenterol Nutr 27(5):519–523. CrossRefPubMedGoogle Scholar
  20. 20.
    Hopman EG, le Cessie S, von Blomberg BM, Mearin ML (2006) Nutritional management of the gluten-free diet in young people with celiac disease in the Netherlands. J Pediatr Gastroenterol Nutr 43(1):102–108. CrossRefPubMedGoogle Scholar
  21. 21.
    Ferrara P, Cicala M, Tiberi E, Spadaccio C, Marcella L, Gatto A, Calzolari P, Castellucci G (2009) High fat consumption in children with celiac disease. Acta Gastroenterol Belg 72(3):296–300PubMedGoogle Scholar
  22. 22.
    Rujner J, Socha J, Syczewska M, Wojtasik A, Kunachowicz H, Stolarczyk A (2004) Magnesium status in children and adolescents with coeliac disease without malabsorption symptoms. Clin Nutr 23(5):1074–1079. CrossRefPubMedGoogle Scholar
  23. 23.
    Blazina S, Bratanic N, Campa AS, Blagus R, Orel R (2010) Bone mineral density and importance of strict gluten-free diet in children and adolescents with celiac disease. Bone 47(3):598–603. CrossRefPubMedGoogle Scholar
  24. 24.
    Kautto E, Ivarsson A, Norström F, Högberg L, Carlsson A, Hörnell A (2014) Nutrient intake in adolescent girls and boys diagnosed with coeliac disease at an early age is mostly comparable to their non-coeliac contemporaries. J Hum Nutr Diet 27(1):41–53. CrossRefPubMedGoogle Scholar
  25. 25.
    Pietzak MM (2005) Follow-up of patients with celiac disease: achieving compliance with treatment. Gastroenterology 128(4 Suppl 1):S135–S141. CrossRefPubMedGoogle Scholar
  26. 26.
    Valdimarsson T, Toss G, Löfman O, Ström M (2000) Three years’ follow-up of bone density in adult coeliac disease: significance of secondary hyperparathyroidism. Scand J Gastroenterol 35(3):274–280. CrossRefPubMedGoogle Scholar
  27. 27.
    Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320(7244):1240–1243. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cole TJ, Lobstein T (2012) Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes 7(4):284–294. CrossRefPubMedGoogle Scholar
  29. 29.
    Cole TJ, Flegal KM, Nicholls D, Jackson AA (2007) Body mass index cut offs to define thinness in children and adolescents: international survey. BMJ 335(7612):194. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Fernández C, Lorenzo H, Vrotsou K, Aresti U, Rica I, Sánchez E (2011) Curvas y tablas de crecimiento (Estudios Longitudinal y Transversal). Fundación Faustino Orbegozo Eizaguirre, BilbaoGoogle Scholar
  31. 31.
    World Health Organization (2010) Global recommendations on physical activity for health. WHO, GenevaGoogle Scholar
  32. 32.
    Bel-Serrat S, Mouratidou T, Pala V, Huybrechts I, Börnhorst C, Fernández-Alvira JM, Hadjigeorgiou C, Eiben G, Hebestreit A, Lissner L, Molnár D, Siani A, Veidebaum T, Krogh V, Moreno LA (2014) Relative validity of the children’s eating habits questionnaire-food frequency section among young European children: the IDEFICS study. Public Health Nutr 17(2):266–276. CrossRefPubMedGoogle Scholar
  33. 33.
    Rodríguez VM, Elbusto-Cabello A, Alberdi-Albeniz M, De la Presa-Donado A, Gómez-Pérez de Mendiola F, Portillo-Baquedano MP, Churruca-Ortega I (2014) Validación de un nuevo registro alimentario precodificado. Revista Española de Nutrición Humana y Dietética. Revista Española de Nutrición Humana y Dietética. CrossRefGoogle Scholar
  34. 34.
    Rodríguez IT, Ballart JF, Pastor GC, Jordà EB, Val VA (2008) Validation of a short questionnaire on frequency of dietary intake: reproducibility and validity. Nutr Hosp 23(3):242–252Google Scholar
  35. 35.
    Russolillo G, Marques I (2008) Food portion sizes album. Imagen Comunicación Multimedia, MadridGoogle Scholar
  36. 36.
    FESNAD (2010) Dietary reference intakes (DRI) for spanish population, 2010. Act Diet 14 (4):196–197. CrossRefGoogle Scholar
  37. 37.
    Gobierno Vasco (2005) Encuesta de nutrición 2005. Departamento de Sanidad del Gobierno Vasco, Vitoria-GasteizGoogle Scholar
  38. 38.
    European Food Safety Authority (2017) Dietary reference values for nutrients summary report. EFSA Support Publ 14 (12):e15121E–n/a. CrossRefGoogle Scholar
  39. 39.
    Aranceta J, Serra-Majem L (2001) Dietary guidelines for the Spanish population. Public Health Nutr 4(6A):1403–1408PubMedGoogle Scholar
  40. 40.
    Missbach B, Schwingshackl L, Billmann A, Mystek A, Hickelsberger M, Bauer G, König J (2015) Gluten-free food database: the nutritional quality and cost of packaged gluten-free foods. PeerJ 3:e1337. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zhong VW, Lamichhane AP, Crandell JL, Couch SC, Liese AD, The NS, Tzeel BA, Dabelea D, Lawrence JM, Marcovina SM, Kim G, Mayer-Davis EJ (2016) Association of adherence to a Mediterranean diet with glycemic control and cardiovascular risk factors in youth with type I diabetes: the SEARCH Nutrition Ancillary Study. Eur J Clin Nutr 70(7):802–807. CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Esteban-Cornejo I, Izquierdo-Gomez R, Gómez-Martínez S, Padilla-Moledo C, Castro-Piñero J, Marcos A, Veiga OL (2016) Adherence to the Mediterranean diet and academic performance in youth: the UP&DOWN study. Eur J Nutr 55 (3):1133–1140. CrossRefPubMedGoogle Scholar
  43. 43.
    Martin-Calvo N, Chavarro JE, Falbe J, Hu FB, Field AE (2016) Adherence to the Mediterranean dietary pattern and BMI change among US adolescents. Int J Obes (Lond) 40(7):1103–1108. CrossRefGoogle Scholar
  44. 44.
    Serra-Majem L, Ribas L, Ngo J, Ortega RM, García A, Pérez-Rodrigo C, Aranceta J (2004) Food, youth and the Mediterranean diet in Spain. Development of KIDMED, Mediterranean Diet Quality Index in children and adolescents. Public Health Nutr 7(7):931–935. CrossRefPubMedGoogle Scholar
  45. 45.
    Bardella MT, Fredella C, Prampolini L, Molteni N, Giunta AM, Bianchi PA (2000) Body composition and dietary intakes in adult celiac disease patients consuming a strict gluten-free diet. Am J Clin Nutr 72(4):937–939CrossRefPubMedGoogle Scholar
  46. 46.
    Hallert C, Grant C, Grehn S, Grännö C, Hultén S, Midhagen G, Ström M, Svensson H, Valdimarsson T (2002) Evidence of poor vitamin status in coeliac patients on a gluten-free diet for 10 years. Aliment Pharmacol Ther 16(7):1333–1339. CrossRefPubMedGoogle Scholar
  47. 47.
    Martin J, Geisel T, Maresch C, Krieger K, Stein J (2013) Inadequate nutrient intake in patients with celiac disease: results from a german dietary survey. Digestion 87(4):240–246. CrossRefPubMedGoogle Scholar
  48. 48.
    Moreno LA, Mesana MI, Fleta J, Ruiz JR, González-Gross M, Sarría A, Marcos A, Bueno M, Group AS (2005) Overweight, obesity and body fat composition in spanish adolescents. The AVENA Study. Ann Nutr Metab 49(2):71–76. CrossRefPubMedGoogle Scholar
  49. 49.
    Pérez-Farinós N, López-Sobaler AM, Dal Re M, Villar C, Labrado E, Robledo T, Ortega RM (2013) The ALADINO study: a national study of prevalence of overweight and obesity in Spanish children in 2011. Biomed Res Int 2013:163687. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Zuccotti G, Fabiano V, Dilillo D, Picca M, Cravidi C, Brambilla P (2013) Intakes of nutrients in Italian children with celiac disease and the role of commercially available gluten-free products. J Hum Nutr Diet 26(5):436–444. CrossRefPubMedGoogle Scholar
  51. 51.
    Babio N, Alcázar M, Castillejo G, Recasens M, Martínez-Cerezo F, Gutiérrez-Pensado V, Masip G, Vaqué C, Vila-Martí A, Torres-Moreno M, Sánchez E, Salas-Salvadó J (2017) Patients with celiac disease reported higher consumption of added sugar and total fat than healthy individuals. J Pediatr Gastroenterol Nutr 64(1):63–69. CrossRefPubMedGoogle Scholar
  52. 52.
    Papadaki S, Mavrikaki E (2015) Greek adolescents and the Mediterranean diet: factors affecting quality and adherence. Nutrition 31(2):345–349. CrossRefPubMedGoogle Scholar
  53. 53.
    Inchley J, Currie D, Young T, Samdal O, Torsheim T, Augustson L, Mathison F, Aleman-Diaz A, Molcho M, Weber M, Barnekow V (2016) Growing up unequal. HBSC 2016 study (2013/2014 survey). World Health Organization, GenevaGoogle Scholar
  54. 54.
    Kulai T, Rashid M (2014) Assessment of nutritional adequacy of packaged gluten-free food products. Can J Diet Pract Res 75(4):186–190. CrossRefPubMedGoogle Scholar
  55. 55.
    Wu JH, Neal B, Trevena H, Crino M, Stuart-Smith W, Faulkner-Hogg K, Yu Louie JC, Dunford E (2015) Are gluten-free foods healthier than non-gluten-free foods? An evaluation of supermarket products in Australia. Br J Nutr 114(3):448–454. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Gluten Analysis Laboratory of the University of the Basque Country, Department of Nutrition and Food ScienceUniversity of the Basque Country (UPV/EHU)VitoriaSpain
  2. 2.Department of Pediatric GastroenterologyHospital Universitario DonostiaSan SebastiánSpain
  3. 3.Department of Nutrition and Food Science, Faculty of PharmacyUniversity of the Basque Country (UPV/EHU)Vitoria-GasteizSpain

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