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

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Abstract

Purpose

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.

Methods

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.

Results

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.

Conclusions

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.

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References

  1. Bai JC, Ciacci C (2017) World gastroenterology organisation global guidelines: celiac disease February 2017. J Clin Gastroenterol 51(9):755–768. https://doi.org/10.1097/MCG.0000000000000919

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1136/gutjnl-2011-301346

    Article  PubMed  Google Scholar 

  3. Catassi C, Gatti S, Fasano A (2014) The new epidemiology of celiac disease. J Pediatr Gastroenterol Nutr 59(Suppl 1):S7–S9. https://doi.org/10.1097/01.mpg.0000450393.23156.59

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1111/j.1365-2036.2010.04543.x

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1097/MCG.0b013e3181978e4d

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.3390/nu5103975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1111/j.1572-0241.2006.00750.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1542/peds.2015-3147

    Article  PubMed  Google Scholar 

  9. Valitutti F, Trovato CM, Montuori M, Cucchiara S (2017) Pediatric celiac disease: follow-up in the spotlight. Adv Nutr 8(2):356–361. https://doi.org/10.3945/an.116.013292

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1111/j.1365-2036.2010.04386.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1017/S0007114511002340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1079/BJN2003872

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1111/j.1365-277X.2005.00607.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1007/s11130-014-0410-4

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/S0002-8223(99)00205-9

    Article  CAS  PubMed  Google Scholar 

  16. Saturni L, Ferretti G, Bacchetti T (2010) The gluten-free diet: safety and nutritional quality. Nutrients 2(1):16–34. https://doi.org/10.3390/nu20100016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):269–273

    PubMed  Google Scholar 

  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. https://doi.org/10.1111/j.1365-277X.2010.01060.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1097/00005176-199811000-00004

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1097/01.mpg.0000228102.89454.eb

    Article  CAS  PubMed  Google Scholar 

  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):296–300

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.clnu.2003.10.018

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.bone.2010.06.008

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1111/jhn.12125

    Article  CAS  PubMed  Google Scholar 

  25. Pietzak MM (2005) Follow-up of patients with celiac disease: achieving compliance with treatment. Gastroenterology 128(4 Suppl 1):S135–S141. https://doi.org/10.1053/j.gastro.2005.02.025

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1080/003655200750024146

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1136/bmj.320.7244.1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1111/j.2047-6310.2012.00064.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1136/bmj.39238.399444.55

    Article  PubMed  PubMed Central  Google Scholar 

  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, Bilbao

    Google Scholar 

  31. World Health Organization (2010) Global recommendations on physical activity for health. WHO, Geneva

    Google Scholar 

  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. https://doi.org/10.1017/S1368980012005368

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.14306/renhyd.18.3.84

    Article  Google Scholar 

  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):242–252

    PubMed  Google Scholar 

  35. Russolillo G, Marques I (2008) Food portion sizes album. Imagen Comunicación Multimedia, Madrid

    Google Scholar 

  36. FESNAD (2010) Dietary reference intakes (DRI) for spanish population, 2010. Act Diet 14 (4):196–197. https://doi.org/10.1016/S1138-0322(10)70039-0

    Article  Google Scholar 

  37. Gobierno Vasco (2005) Encuesta de nutrición 2005. Departamento de Sanidad del Gobierno Vasco, Vitoria-Gasteiz

    Google Scholar 

  38. European Food Safety Authority (2017) Dietary reference values for nutrients summary report. EFSA Support Publ 14 (12):e15121E–n/a. https://doi.org/10.2903/sp.efsa.2017.e15121

    Article  Google Scholar 

  39. Aranceta J, Serra-Majem L (2001) Dietary guidelines for the Spanish population. Public Health Nutr 4(6A):1403–1408

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.7717/peerj.1337

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1038/ejcn.2016.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1007/s00394-015-0927-9

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1038/ijo.2016.59

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1079/PHN2004556

    Article  PubMed  Google Scholar 

  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):937–939

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1046/j.1365-2036.2002.01283.x

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1159/000348850

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1159/000084738

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1155/2013/163687

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1111/jhn.12026

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1097/MPG.0000000000001251

    Article  CAS  PubMed  Google Scholar 

  52. Papadaki S, Mavrikaki E (2015) Greek adolescents and the Mediterranean diet: factors affecting quality and adherence. Nutrition 31(2):345–349. https://doi.org/10.1016/j.nut.2014.09.003

    Article  PubMed  Google Scholar 

  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, Geneva

    Google Scholar 

  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. https://doi.org/10.3148/cjdpr-2014-022

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1017/S0007114515002056

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

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).

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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.

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Correspondence to A. Lasa.

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Larretxi, I., Simon, E., Benjumea, L. et al. Gluten-free-rendered products contribute to imbalanced diets in children and adolescents with celiac disease. Eur J Nutr 58, 775–783 (2019). https://doi.org/10.1007/s00394-018-1685-2

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