Hepatic Steatosis in Patients with Celiac Disease: The Role of Packaged Gluten-Free Foods
Open accessAbstract
Background: An increased risk of nonalcoholic fatty liver disease (NAFLD) in patients with celiac disease (CD) adhering to a gluten-free diet (GFD) was recently reported. The nutritional composition of packaged gluten-free foods (PGFF) has been proposed as a possible cause. This hypothesis has not been investigated further, since a systematic structural nutritional interview for all patients would be problematic in clinical practice. Methods: We administered a simple questionnaire based on a Recency, Frequency, and Monetary value (RFM) analysis (a cornerstone of direct marketing segmentation) to consecutive CD patients on a GFD for >6 months and verified its association with NAFLD. Subgroup analyses were performed to understand whether specific patterns of PGFF consumption were significantly associated with NAFLD. Results: Amongst 147 patients (female 82%, median age 42 years), 45 (30.6%) had NAFLD. Total RFM score (adjusted odds ratio = 1.223, 95% CI: 1.059–1.413, p = 0.006), body mass index, and total cholesterol and triglycerides were independently related to NAFLD, and “Bread and bakery” (p = 0.002), “salty convenience” (p = 0.005), and “sweet convenience” (p = 0.049) products were significantly related with NAFLD. Also, questions about the number of purchased PGFF in the last month (monetary value) and different categories of PGFF consumed in the last week (recency) were particularly able to identify NAFLD patients. Conclusions: The specific GFD dietary habits of CD patients were correlated with the degree of risk of NAFLD. Information was obtained through a questionnaire which could be used in clinical practice to favor a patient-tailored approach and in future studies to verify the reproducibility of our results in different geographical areas.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In adolescents, high intakes of gluten-free bread, bakery products as well as sweet and salty convenience foods were associated with non-alcoholic fatty liver disease.
“In adolescents, high intakes of gluten-free bread, bakery products as well as sweet and salty convenience foods were associated with non-alcoholic fatty liver disease (93).”
From Gluten-free diet for pediatric patients with coeliac disease: A position paper from the ESPGHAN gastroenterology committee, special interest group in coeliac disease. (2024) · cites this paper as [93]
Results §3.4 reports that NAFLD was associated with higher consumption scores for gluten-free bread and bakery products and salty convenience foods, with some scores also higher for sweet convenience foods. But Results §3.1 describes a cohort with a median age of 42 years; the paper does not establish this association specifically in adolescents. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Increased risk of non-alcoholic fatty liver disease after diagnosis of celiac disease
Reilly, N. R., Lebwohl, B., Hultcrantz, R., Green, P. H. R., & Ludvigsson, J. F. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.01.013 · Cited by 110 · see citing works
Flagged first, then by citations
Research works printed but not linked: 27
- [1]Ludvigsson J.F. Leffler D.A. Bai J.C. Biagi F. Fasano A. Green P.H.R. Hadjivassiliou M. Kaukinen K. Kelly C.P. Leonard J.N. The Oslo Definitions for Coeliac Disease and Related Terms Gut 2013 62 43 52 10.1136/gutjnl-2011-301346 22345659 PMC3440559 · DOI · Paper page
- [2]Reilly N.R. Aguilar K. Hassid B.G. Cheng J. Defelice A.R. Kazlow P. Bhagat G. Green P.H. Celiac Disease in Normal-Weight and Overweight Children: Clinical Features and Growth Outcomes Following a Gluten-Free Diet J. Pediatr. Gastroenterol. Nutr. 2011 53 528 531 10.1097/MPG.0b013e3182276d5e 21670710 · DOI
- [3]Valletta E. Fornaro M. Cipolli M. Conte S. Bissolo F. Danchielli C. Celiac Disease and Obesity: Need for Nutritional Follow-up after Diagnosis Eur. J. Clin. Nutr. 2010 64 1371 1372 10.1038/ejcn.2010.161 20717130 · DOI
- [4]Norsa L. Shamir R. Zevit N. Verduci E. Hartman C. Ghisleni D. Riva E. Giovannini M. Cardiovascular Disease Risk Factor Profiles in Children with Celiac Disease on Gluten-Free Diets World J. Gastroenterol. 2013 19 5658 5664 10.3748/wjg.v19.i34.5658 24039358 PMC3769902 · DOI
- [6]Tovoli F. Negrini G. Farì R. Guidetti E. Faggiano C. Napoli L. Bolondi L. Granito A. Increased Risk of Nonalcoholic Fatty Liver Disease in Patients with Coeliac Disease on a Gluten-Free Diet: Beyond Traditional Metabolic Factors Aliment. Pharmacol. Ther. 2018 48 538 546 10.1111/apt.14910 29984415 · DOI
- [7]European Association for the Study of the Liver (EASL) European Association for the Study of Diabetes (EASD) European Association for the Study of Obesity (EASO) EASL-EASD-EASO Clinical Practice Guidelines for the Management of Non-Alcoholic Fatty Liver Disease J. Hepatol. 2016 64 1388 1402 10.1016/j.jhep.2015.11.004 27062661 · DOI · Paper page
- [8]Simon T.G. Roelstraete B. Hartjes K. Shah U. Khalili H. Arnell H. Ludvigsson J.F. Non-Alcoholic Fatty Liver Disease in Children and Young Adults Is Associated with Increased Long-Term Mortality J. Hepatol. 2021 75 1034 1041 10.1016/j.jhep.2021.06.034 34224779 PMC8530955 · DOI
- [9]Tortora R. Capone P. De Stefano G. Imperatore N. Gerbino N. Donetto S. Monaco V. Caporaso N. Rispo A. Metabolic Syndrome in Patients with Coeliac Disease on a Gluten-Free Diet Aliment. Pharmacol. Ther. 2015 41 352 359 10.1111/apt.13062 25581084 · DOI
- [10]Hill I.D. Fasano A. Guandalini S. Hoffenberg E. Levy J. Reilly N. Verma R. NASPGHAN Clinical Report on the Diagnosis and Treatment of Gluten-Related Disorders J. Pediatr. Gastroenterol. Nutr. 2016 63 156 165 10.1097/MPG.0000000000001216 27035374 · DOI
- [11]Biagi F. Bianchi P.I. Marchese A. Trotta L. Vattiato C. Balduzzi D. Brusco G. Andrealli A. Cisarò F. Astegiano M. A Score That Verifies Adherence to a Gluten-Free Diet: A Cross-Sectional, Multicentre Validation in Real Clinical Life Br. J. Nutr. 2012 108 1884 1888 10.1017/S0007114511007367 22321199 · DOI · Paper page
- [12]Silvester J.A. Graff L.A. Rigaux L. Walker J.R. Duerksen D.R. Symptomatic Suspected Gluten Exposure Is Common among Patients with Coeliac Disease on a Gluten-Free Diet Aliment. Pharmacol. Ther. 2016 44 612 619 10.1111/apt.13725 27443825 PMC5283559 · DOI
- [13]Biagi F. Andrealli A. Bianchi P.I. Marchese A. Klersy C. Corazza G.R. A Gluten-Free Diet Score to Evaluate Dietary Compliance in Patients with Coeliac Disease Br. J. Nutr. 2009 102 882 887 10.1017/S0007114509301579 19331704 · DOI
- [14]Missbach B. Schwingshackl L. Billmann A. Mystek A. Hickelsberger M. Bauer G. König J. Gluten-Free Food Database: The Nutritional Quality and Cost of Packaged Gluten-Free Foods PeerJ 2015 3 e1337 10.7717/peerj.1337 26528408 PMC4627916 · DOI
- [15]Vergeer L. Franco-Arellano B. Tjong G.B. Bernstein J.T. L’Abbé M.R. The Level of Processing, Nutritional Composition and Prices of Canadian Packaged Foods and Beverages with and without Gluten-Free Claims Nutrients 2021 13 1183 10.3390/nu13041183 33918418 PMC8066194 · DOI
- [16]Myhrstad M.C.W. Slydahl M. Hellmann M. Garnweidner-Holme L. Lundin K.E.A. Henriksen C. Telle-Hansen V.H. Nutritional Quality and Costs of Gluten-Free Products: A Case-Control Study of Food Products on the Norwegian Marked Food Nutr. Res. 2021 65 10.29219/fnr.v65.6121 PMC8009084 33841066 · DOI
- [17]Lavriša Ž. Hribar M. Kušar A. Žmitek K. Pravst I. Nutritional Composition of Gluten-Free Labelled Foods in the Slovenian Food Supply Int. J. Environ. Res. Public Health 2020 17 8239 10.3390/ijerph17218239 PMC7664664 33171869 · DOI
- [18]Guennouni M. Khoudri N.E. Bourrhouat A. Hilali A. Nutritional Quality of Gluten-Free Products in Moroccan Supermarkets and e-Commerce Platforms Cereal Chem. 2020 97 912 920 10.1002/cche.10313 · DOI
- [19]Hamaguchi M. Kojima T. Itoh Y. Harano Y. Fujii K. Nakajima T. Kato T. Takeda N. Okuda J. Ida K. The Severity of Ultrasonographic Findings in Nonalcoholic Fatty Liver Disease Reflects the Metabolic Syndrome and Visceral Fat Accumulation Am. J. Gastroenterol. 2007 102 2708 2715 10.1111/j.1572-0241.2007.01526.x 17894848 · DOI
- [20]Chalasani N. Younossi Z. Lavine J.E. Diehl A.M. Brunt E.M. Cusi K. Charlton M. Sanyal A.J. American Gastroenterological Association American Association for the Study of Liver Diseases The Diagnosis and Management of Non-Alcoholic Fatty Liver Disease: Practice Guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology Gastroenterology 2012 142 1592 1609 10.1053/j.gastro.2012.04.001 22656328 · DOI
- [21]Bardella M.T. Fredella C. Prampolini L. Molteni N. Giunta A.M. Bianchi P.A. Body Composition and Dietary Intakes in Adult Celiac Disease Patients Consuming a Strict Gluten-Free Diet Am. J. Clin. Nutr. 2000 72 937 939 10.1093/ajcn/72.4.937 11010934 · DOI
- [22]Barone M. Della Valle N. Rosania R. Facciorusso A. Trotta A. Cantatore F.P. Falco S. Pignatiello S. Viggiani M.T. Amoruso A. A Comparison of the Nutritional Status between Adult Celiac Patients on a Long-Term, Strictly Gluten-Free Diet and Healthy Subjects Eur. J. Clin. Nutr. 2016 70 23 27 10.1038/ejcn.2015.114 26173865 · DOI
- [23]Babio N. Alcázar M. Castillejo G. Recasens M. Martínez-Cerezo F. Gutiérrez-Pensado V. Masip G. Vaqué C. Vila-Martí A. Torres-Moreno M. Patients With Celiac Disease Reported Higher Consumption of Added Sugar and Total Fat Than Healthy Individuals J. Pediatr. Gastroenterol. Nutr. 2017 64 63 69 10.1097/MPG.0000000000001251 27128207 · DOI · Paper page
- [24]Zuccotti G. Fabiano V. Dilillo D. Picca M. Cravidi C. Brambilla P. Intakes of Nutrients in Italian Children with Celiac Disease and the Role of Commercially Available Gluten-Free Products J. Hum. Nutr. Diet. Off. J. Br. Diet. Assoc. 2013 26 436 444 10.1111/jhn.12026 23252793 · DOI
- [25]Jamieson J.A. Weir M. Gougeon L. Canadian Packaged Gluten-Free Foods Are Less Nutritious than Their Regular Gluten-Containing Counterparts PeerJ 2018 6 e5875 10.7717/peerj.5875 30416886 PMC6225834 · DOI
- [26]Romão B. Botelho R.B.A. Alencar E.R. da Silva V.S.N. Pacheco M.T.B. Zandonadi R.P. Chemical Composition and Glycemic Index of Gluten-Free Bread Commercialized in Brazil Nutrients 2020 12 2234 10.3390/nu12082234 PMC7468724 32726985 · DOI
- [27]Brandi G. De Lorenzo S. Candela M. Pantaleo M.A. Bellentani S. Tovoli F. Saccoccio G. Biasco G. Microbiota, NASH, HCC and the Potential Role of Probiotics Carcinogenesis 2017 38 231 240 10.1093/carcin/bgx007 28426878 · DOI
- [28]Rinninella E. Cintoni M. Raoul P. Triarico S. Dionisi T. Gasbarrini G.B. Gasbarrini A. Mele M.C. The Healthy Gluten-Free Diet: Practical Tips to Prevent Metabolic Disorders and Nutritional Deficiencies in Celiac Patients Gastroenterol. Insights 2021 12 166 182 10.3390/gastroent12020015 · DOI
Cited by
Sorted by citations
Luque, V., Crespo‐Escobar, P., Hård af Segerstad, E. M., Koltai, T., Norsa, L., Roman, E., Vreugdenhil, A., Fueyo‐Díaz, R., & Ribes‐Koninckx, C. (2024) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/jpn3.12079 · Cited by 32 · see citing works
- Authors
- Raiteri, A., Granito, A., Faggiano, C., Giamperoli, A., Catenaro, T., Negrini, G., & Tovoli, F.
- Affiliations
- University of Bologna (IT)
- Corresponding author
- Tovoli, Francesco
- Venue
- Nutrients
- Publisher
- MDPI AG
- Published
- 2022-07-18
- Volume
- 14
- Issue
- 14
- Pages
- 2942
- ISSN
- 2072-6643 (ISSN-L)
- PMC
- PMC9316041
- OpenAlex
- W4285802444
- Cited by
- 20
- References
- 1
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 9 · 2023: 3
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nutrients (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by)
- Topics
- Health Sciences › Medicine › Gastroenterology › Celiac Disease Research and Management
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Nursing › Nutrition and Dietetics › Food composition and properties
- Keywords
- celiac disease, non-alcoholic fatty liver disease, hepatic steatosis, gluten-free diet, dietary habits, RFM analysis, convenience foods, bakery products, body mass index, cholesterol, triglycerides
- MeSH terms
- Adult, Celiac Disease, Female, Humans, Reproducibility of Results, Foods, Specialized, Diet, Gluten-Free, Non-alcoholic Fatty Liver Disease
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review