Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Nutrient intakes in adult and pediatric coeliac disease patients on gluten-free diet: a systematic review and meta-analysis

European Journal of Clinical Nutrition (2023)Cite this article

Subjects

Abstract

Celiac Disease (CD) continues to require a strict lifetime gluten-free diet (GFD) to maintain healthy status. Many studies have assessed the GFD nutritional adequacy in their cohorts, but an overall picture in adults and children would offer a lifetime vision to identify actionable areas of change. We aimed at assessing the nutrient intakes of adult and pediatric CD patients following a GFD diet and identifying potential areas of improvement. Systematic review was carried out across PubMed, Scopus and Scholar up to October 2022, including full-text studies that assessed the nutrient intakes of CD patients on GFD, in terms of macro- and/or micronutrients (absolute or percentage daily average). Random-effect meta-analysis and univariable meta-regression were applied to obtain pooled estimates for proportions and influencing variables on the outcome, respectively. Thirty-eight studies with a total of 2114 patients were included. Overall, the daily energy intake was 1995 (CI 1884–2106) Kcal with 47.8% (CI 45.7–49.8%) from carbohydrates, 15.5% (CI 14.8–16.2%) from proteins, and 35.8% (CI 34.5–37.0%) from fats. Of total fats, 13.2% (CI 12.4–14.0%) were saturated fats. Teenagers had the highest consumption of fats (94.9, CI 54.8–134.9 g/day), and adults presented insufficient dietary fiber intake (18.9 g, CI 16.5–21.4 g). Calcium, magnesium, and iron intakes were particularly insufficient in adolescence, whereas vitamin D was insufficient in all age groups. In conclusion, GFD may expose CD patients to high fat and low essential micronutrient intakes. Given GFD is a lifelong therapy, to prevent the occurrence of diseases (e.g. cardiovascular or bone disorders) dietary intakes need to be assessed on long-term follow-ups.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Main steps of the study.
Fig. 2: Random effect meta-analysis of average daily percentage intakes of macronutrients.
Fig. 3: Random effect meta-analysis of average daily absolute intakes of energy and macronutrients.
Fig. 4: Funnel plot visual inspection of average daily intakes of nutrients.

Data availability

Data will be made available upon request.

References

  1. Caio G, Volta U, Sapone A, Leffler DA, Catassi C, Fasano A. Coeliac disease: a comprehensive current review. BMC Med. 2019;17. https://doi.org/10.1186/s12916-019-1380-z.

  2. Vasagar B, Cox J, Herion JT, Ivanoff E. World epidemiology of non-coeliac gluten sensitivity. Minerva Gastroenterol Dietol. 2017;63:5–15. https://doi.org/10.23736/s1121-421x.16.02338-z.

    Article  PubMed  Google Scholar 

  3. Vici G, Belli L, Biondi M, Polzonetti V. Gluten free diet and nutrient deficiencies: a review. Clin Nutr. 2016;35:1236–41. https://doi.org/10.1016/j.clnu.2016.05.002.

    Article  CAS  PubMed  Google Scholar 

  4. Melini V, Melini F. Gluten-free diet: gaps and needs for a healthier diet. Nutrients. 2019;11. https://doi.org/10.3390/nu11010170.

  5. Martin J, Geisel T, Maresch C, Krieger K, Stein J. Inadequate nutrient intake in patients with coeliac disease: results from a German dietary survey. Digestion. 2013;87:240–6. https://doi.org/10.1159/000348850.

    Article  CAS  PubMed  Google Scholar 

  6. Shepherd SJ, Gibson PR. Nutritional inadequacies of the gluten-free diet in both recently-diagnosed and long-term patients with coeliac disease. J Hum Nutr Diet J Br Diet Assoc. 2013;26:349–58. https://doi.org/10.1111/jhn.12018.

    Article  CAS  Google Scholar 

  7. Wild D, Robins GG, Burley VJ, Howdle PD. Evidence of high sugar intake, and low fibre and mineral intake, in the gluten-free diet. Aliment Pharm Ther. 2010;32:573–81. https://doi.org/10.1111/j.1365-2036.2010.04386.x.

    Article  CAS  Google Scholar 

  8. Jones AL. The gluten-free diet: fad or necessity? Diabetes Spectr Publ Am Diabetes Assoc. 2017;30:118–23. https://doi.org/10.2337/ds16-0022.

    Article  Google Scholar 

  9. Niland B, Cash BD. Health benefits and adverse effects of a gluten-free diet in non–coeliac disease patients. Gastroenterol Hepatol. 2018;14:82–91.

    Google Scholar 

  10. Potter MDE, Brienesse SC, Walker MM, Boyle A, Talley NJ. Effect of the gluten-free diet on cardiovascular risk factors in patients with coeliac disease: a systematic review. J Gastroenterol Hepatol. 2018;33:781–91. https://doi.org/10.1111/jgh.14039.

    Article  PubMed  Google Scholar 

  11. Moher D, Liberati A, Tetzlaff J, Altam DG,PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9, W64.

    Article  PubMed  Google Scholar 

  12. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2011; http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.

  13. EFSA (European Food Safety Authority). Dietary reference values for nutrients summary report 2017—EFSA Supporting Publications-Wiley Online Library. 2017;e1521:98 pp. https://doi.org/10.2903/sp.efsa.2017.e15121.

  14. U.S. Dept of Agricoltureand U.S. Dept of Health and Human Services. Dietary guidelines for Americans, 2020-2025 and online materials|Dietary Guidelines for Americans. https://www.dietaryguidelines.gov/resources/2020-2025-dietary-guidelines-online-materials.

  15. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.

  16. Viechtbauer W. Conducting meta-analyses in R with the metafor Package. J Stat Softw. 2010;36:1–48. https://doi.org/10.18637/jss.v036.i03.

    Article  Google Scholar 

  17. Larretxi I, Simon E, Benjumea L, Miranda J, Bustamante MA, Lasa A, et al. Gluten-free-rendered products contribute to imbalanced diets in children and adolescents with coeliac disease. Eur J Nutr. 2019;58:775–83. https://doi.org/10.1007/s00394-018-1685-2.

    Article  CAS  PubMed  Google Scholar 

  18. Van Rossum C, Fransen H, Verkaik-Kloosterman J, Buurma-Rethans EJM, Ocke MC. Dutch National Food Consumption Survey 2007-2010: diet of children and adults aged 7 to 69 years. RIVM Rapp. 2011;350050006:148.

  19. Babio N, Alcázar M, Castillejo G, Recasens M, Martínez-Cerezo F, Gutiérrez-Pensado V, et al. Patients with coeliac disease reported higher consumption of added sugar and total fat than healthy individuals. J Pediatr Gastroenterol Nutr. 2017;64:63–9. https://doi.org/10.1097/MPG.0000000000001251.

    Article  CAS  PubMed  Google Scholar 

  20. Ballestero Fernández C, Varela-Moreiras G, Úbeda N, Alonso-Aperte E. Nutritional status in Spanish children and adolescents with coeliac disease on a gluten free diet compared to non-coeliac disease controls. Nutrients. 2019;11. https://doi.org/10.3390/nu11102329.

  21. Daniels SR, Pratt CA, Hayman LL. Reduction of risk for cardiovascular disease in children and adolescents. Circulation. 2011;124:1673–86. https://doi.org/10.1161/CIRCULATIONAHA.110.016170.

    Article  PubMed  PubMed Central  Google Scholar 

  22. McFarlane XA, Marsham J, Reeves D, Bhalla AK, Robertson DAF. Subclinical nutritional deficiency in treated coeliac disease and nutritional content of the gluten free diet. J Hum Nutr Diet. 1995;8:231–7. https://doi.org/10.1111/j.1365-277X.1995.tb00316.x.

    Article  Google Scholar 

  23. Quarpong W, Card TR, West J, Solaymani-Dodaran M, Logan RFA, Grainge MJ. Mortality in people with coeliac disease: long-term follow-up from a Scottish cohort. UEGJ. 2019;7:377–87. https://doi.org/10.1177/2050640618814662.

    Article  Google Scholar 

  24. Grzymisławska M, Puch E, Zawada A, Grzymisławski M. Do nutritional behaviors depend on biological sex and cultural gender? Adv Clin Exp Med. 2020;29:165–72. https://doi.org/10.17219/acem/111817.

    Article  PubMed  Google Scholar 

  25. Kautto E, Rydén PJ, Ivarsson A, Olsson C, Norström F, Högberg L, et al. What happens to food choices when a gluten-free diet is required? A prospective longitudinal population-based study among Swedish adolescent with coeliac disease and their peers. J Nutr Sci. 2014;3:e2. https://doi.org/10.1017/jns.2013.24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cardo A, Churruca I, Lasa A, Navarro V, Vázquez-Polo M, Perez-Junkera G, et al. Nutritional imbalances in adult celiac patients following a gluten-free diet. Nutrients. 2021;13:2877. https://doi.org/10.3390/nu13082877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Di Nardo G, Villa MP, Conti L, Ranucci G, Pacchiarotti C, Principessa L, et al. Nutritional deficiencies in children with celiac disease resulting from a gluten-free diet: a systematic review. Nutrients. 2019;11:1588. https://doi.org/10.3390/nu11071588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Caeiro C, Pragosa C, Carreira Cruz M, Pereira CD, Gonçalves Pereira S. The role of pseudocereals in celiac disease: reducing nutritional deficiencies to improve well-being and health. J Nutr Metab. 2022. https://doi.org/10.1155/2022/8502169.

    Article  PubMed  PubMed Central  Google Scholar 

  29. WW Jamieson JA, Gill K, Fisher S, English M. Development of a Canadian food composition database of gluten-free products. Foods. 2022;11:2215. https://doi.org/10.3390/foods11152215.

    Article  CAS  Google Scholar 

  30. Macêdo MIP, Albuquerque MDFM, Tahan S, de MoraisIs MB. Is there any association between overweight, physical activity, fat and fiber intake with functional constipation in adolescents? Scand J Gastroenterol. 2020;55:414–20. https://doi.org/10.1080/00365521.2020.1749878.

  31. Slavin JL. Position of the American Dietetic Association: health implications of dietary fiber. J Am Diet Assoc. 2008;108:1716–31. https://doi.org/10.1016/j.jada.2008.08.007.

    Article  PubMed  Google Scholar 

  32. Bailey ADL, Fulgoni III VL, Shah N, Patterson AC, Gutierrez-Orozco F, Mathews RS, et al. Nutrient intake adequacy from food and beverage intake of US children aged 1-6 years from NHANES 2001-2016. Nutrients. 2021;13. https://doi.org/10.3390/nu13030827.

  33. U.S. Dept of Agriculture - Economic Research Service. Food Availability and consumption Data System. 2012. https://www.ers.usda.gov/data-products/food-availability-per-capita-data-system/.

Download references

Author information

Author notes

  1. These authors contributed equally: Monica Gessaroli, Leonardo Frazzoni, Usama Sikandar.

Authors and Affiliations

  1. Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy

    Monica Gessaroli, Usama Sikandar, Andrea Pession, Rocco Maurizio Zagari, Lorenzo Fuccio & Maria Luisa Forchielli

  2. IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy

    Leonardo Frazzoni, Gabriele Bronzetti, Andrea Pession, Rocco Maurizio Zagari, Lorenzo Fuccio & Maria Luisa Forchielli

  3. Health Sciences and Technologies Interdepartmental Center for Industrial Research (CIRI-SDV), University of Bologna, Bologna, Italy

    Maria Luisa Forchielli

Authors
  1. Monica Gessaroli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonardo Frazzoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Usama Sikandar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriele Bronzetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea Pession
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rocco Maurizio Zagari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lorenzo Fuccio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Luisa Forchielli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Concept and design: MG, LFrazzoni and MLF. Analysis and interpretation of the data: MG, LFrazzoni, LFuccio and MLF. Drafting of the article: all authors. Collection and assembly of data: MG, LFrazzoni and US. Critical revision of the article for important intellectual content: all authors. Final approval of the article: all authors.

Corresponding author

Correspondence to Maria Luisa Forchielli.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gessaroli, M., Frazzoni, L., Sikandar, U. et al. Nutrient intakes in adult and pediatric coeliac disease patients on gluten-free diet: a systematic review and meta-analysis. Eur J Clin Nutr (2023). https://doi.org/10.1038/s41430-023-01280-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41430-023-01280-0

Search

Advanced search

Quick links