Skip to main content
Top
Published in: Clinical and Experimental Medicine 1/2024

Open Access 01-12-2024 | Celiac Disease | Review

Metabolomics and lipidomics signature in celiac disease: a narrative review

Authors: Mohammad Rostami-Nejad, Nastaran Asri, Sajjad Bakhtiari, Ensieh Khalkhal, Sepehr Maleki, Mostafa Rezaei-Tavirani, Somayeh Jahani-Sherafat, Kamran Rostami

Published in: Clinical and Experimental Medicine | Issue 1/2024

Login to get access

Abstract

Celiac disease (CD) is a chronic immune-mediated inflammatory disease of the small intestine caused by aberrant immune responses to consumed gluten proteins. CD is diagnosed by a combination of the patients reported symptoms, serologic and endoscopic biopsy evaluation of the small intestine; and adherence to a strict gluten-free diet (GFD) is considered the only available therapeutic approach for this disorder. Novel approaches need to be considered for finding new biomarkers to help this disorder diagnosis and finding a new alternative therapeutic method for this group of patients. Metabolomics and lipidomics are powerful tools to provide highly accurate and sensitive biomarkers. Previous studies indicated a metabolic fingerprint for CD deriving from alterations in gut microflora or intestinal permeability, malabsorption, and energy metabolism. Moreover, since CD is characterized by increased intestinal permeability and due to the importance of membrane lipid components in controlling barrier integrity, conducting lipidomics studies in this disorder is of great importance. In the current study, we tried to provide a critical overview of metabolomic and lipidomic changes in CD.
Literature
2.
go back to reference Taraghikhah N, Ashtari S, Asri N, et al. An updated overview of spectrum of gluten-related disorders: clinical and diagnostic aspects. BMC Gastroenterol. 2020;20:258.PubMedPubMedCentralCrossRef Taraghikhah N, Ashtari S, Asri N, et al. An updated overview of spectrum of gluten-related disorders: clinical and diagnostic aspects. BMC Gastroenterol. 2020;20:258.PubMedPubMedCentralCrossRef
3.
go back to reference Calabrò A, Gralka E, Luchinat C, Saccenti E, Tenori L. A metabolomic perspective on coeliac disease. Autoimmune Dis. 2014;2014: 756138.PubMedPubMedCentral Calabrò A, Gralka E, Luchinat C, Saccenti E, Tenori L. A metabolomic perspective on coeliac disease. Autoimmune Dis. 2014;2014: 756138.PubMedPubMedCentral
5.
go back to reference Pepe A, Mandato C, Di Leo T, Boccia G, Lucaroni G, Franci G, et al. Celiac disease on the bed-side: embedding case finding and screening in hospitalized children. Nutrients. 2023;15(23). Pepe A, Mandato C, Di Leo T, Boccia G, Lucaroni G, Franci G, et al. Celiac disease on the bed-side: embedding case finding and screening in hospitalized children. Nutrients. 2023;15(23).
6.
go back to reference Lionetti E, Pjetraj D, Gatti S, Catassi G, Bellantoni A, Boffardi M, et al. Prevalence and detection rate of celiac disease in Italy: results of a SIGENP multicenter screening in school-age children. Dig Liver Dis. 2023;55(5):608–13.PubMedCrossRef Lionetti E, Pjetraj D, Gatti S, Catassi G, Bellantoni A, Boffardi M, et al. Prevalence and detection rate of celiac disease in Italy: results of a SIGENP multicenter screening in school-age children. Dig Liver Dis. 2023;55(5):608–13.PubMedCrossRef
7.
go back to reference Sciurti M, Fornaroli F, Gaiani F, et al. Genetic susceptibilty and celiac disease: what role do HLA haplotypes play? Acta Biomed. 2018;89:17–21.PubMed Sciurti M, Fornaroli F, Gaiani F, et al. Genetic susceptibilty and celiac disease: what role do HLA haplotypes play? Acta Biomed. 2018;89:17–21.PubMed
8.
go back to reference Mansouri M, Dadfar M, Rostami-Nejad M, Ekhlasi G, Shahbazkhani A, Shahbazkhani B. The frequency of HLA-DQ2/DQ8 haplotypes and celiac disease among the first-degree relatives of patients with celiac disease. Gastroenterol Hepatol Bed Bench. 2021;14:36–43.PubMedPubMedCentral Mansouri M, Dadfar M, Rostami-Nejad M, Ekhlasi G, Shahbazkhani A, Shahbazkhani B. The frequency of HLA-DQ2/DQ8 haplotypes and celiac disease among the first-degree relatives of patients with celiac disease. Gastroenterol Hepatol Bed Bench. 2021;14:36–43.PubMedPubMedCentral
10.
go back to reference Martínez-Ojinaga E, Molina M, Polanco I, Urcelay E, Núñez C. HLA-DQ distribution and risk assessment of celiac disease in a Spanish center. Rev Esp Enferm Dig. 2018;110:421–6.PubMedCrossRef Martínez-Ojinaga E, Molina M, Polanco I, Urcelay E, Núñez C. HLA-DQ distribution and risk assessment of celiac disease in a Spanish center. Rev Esp Enferm Dig. 2018;110:421–6.PubMedCrossRef
11.
12.
go back to reference Caputo I, Lepretti M, Martucciello S, Esposito C. Enzymatic strategies to detoxify gluten: implications for celiac disease. Enzyme Res. 2010;2010: 174354.PubMedPubMedCentralCrossRef Caputo I, Lepretti M, Martucciello S, Esposito C. Enzymatic strategies to detoxify gluten: implications for celiac disease. Enzyme Res. 2010;2010: 174354.PubMedPubMedCentralCrossRef
13.
go back to reference Kamboj AK, Oxentenko AS. Clinical and histologic mimickers of celiac disease. Clin Transl Gastroenterol. 2017;8. Kamboj AK, Oxentenko AS. Clinical and histologic mimickers of celiac disease. Clin Transl Gastroenterol. 2017;8.
14.
go back to reference Sharma N, Bhatia S, Chunduri V, et al. Pathogenesis of celiac disease and other gluten related disorders in wheat and strategies for mitigating them. Front Nutr 2020;7. Sharma N, Bhatia S, Chunduri V, et al. Pathogenesis of celiac disease and other gluten related disorders in wheat and strategies for mitigating them. Front Nutr 2020;7.
15.
go back to reference Sollid LM. Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol. 2002;2(9):647–55.PubMedCrossRef Sollid LM. Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol. 2002;2(9):647–55.PubMedCrossRef
16.
go back to reference Rostami-Nejad M, Rostami K, Emami MH, Zali MR, Malekzadeh R. Epidemiology of celiac disease in Iran: a review. Middle East J Dig Dis. 2011;3:5.PubMedPubMedCentral Rostami-Nejad M, Rostami K, Emami MH, Zali MR, Malekzadeh R. Epidemiology of celiac disease in Iran: a review. Middle East J Dig Dis. 2011;3:5.PubMedPubMedCentral
17.
go back to reference Rostami-Nejad M, Razzaghi Z, Esmaeili S, Rezaei-Tavirani S, Akbarzadeh Baghban A, Vafaee R. Immunological reactions by T cell and regulation of crucial genes in treated celiac disease patients. Gastroenterol Hepatol Bed Bench. 2020;13:155–60.PubMedPubMedCentral Rostami-Nejad M, Razzaghi Z, Esmaeili S, Rezaei-Tavirani S, Akbarzadeh Baghban A, Vafaee R. Immunological reactions by T cell and regulation of crucial genes in treated celiac disease patients. Gastroenterol Hepatol Bed Bench. 2020;13:155–60.PubMedPubMedCentral
18.
go back to reference Ganji A, Moghbeli M. Type 1 diabetes and hyperthyroidism in a family with celiac disease after exposure to gluten: a rare case report. Clin Diabetes Endocrinol. 2018;4:24.PubMedPubMedCentralCrossRef Ganji A, Moghbeli M. Type 1 diabetes and hyperthyroidism in a family with celiac disease after exposure to gluten: a rare case report. Clin Diabetes Endocrinol. 2018;4:24.PubMedPubMedCentralCrossRef
20.
go back to reference Vacca M, Porrelli A, Calabrese FM, et al. How metabolomics provides novel insights on celiac disease and gluten-free diet: a narrative review. Front Microbiol. 2022;13: 859467.PubMedPubMedCentralCrossRef Vacca M, Porrelli A, Calabrese FM, et al. How metabolomics provides novel insights on celiac disease and gluten-free diet: a narrative review. Front Microbiol. 2022;13: 859467.PubMedPubMedCentralCrossRef
21.
go back to reference Martín-Masot R, Mota-Martorell N, Jové M, Maldonado J, Pamplona R, Nestares T. Alterations in one-carbon metabolism in celiac disease. Nutrients. 2020;12:3723.PubMedPubMedCentralCrossRef Martín-Masot R, Mota-Martorell N, Jové M, Maldonado J, Pamplona R, Nestares T. Alterations in one-carbon metabolism in celiac disease. Nutrients. 2020;12:3723.PubMedPubMedCentralCrossRef
22.
go back to reference Claudino WM, Quattrone A, Biganzoli L, Pestrin M, Bertini I, Di Leo A. Metabolomics: available results, current research projects in breast cancer, and future applications. J Clin Oncol. 2007;25:2840–6.PubMedCrossRef Claudino WM, Quattrone A, Biganzoli L, Pestrin M, Bertini I, Di Leo A. Metabolomics: available results, current research projects in breast cancer, and future applications. J Clin Oncol. 2007;25:2840–6.PubMedCrossRef
23.
go back to reference Calabrò A, Gralka E, Luchinat C, Saccenti E, Tenori L. A metabolomic perspective on coeliac disease. Autoimmune Dis. 2014;2014. Calabrò A, Gralka E, Luchinat C, Saccenti E, Tenori L. A metabolomic perspective on coeliac disease. Autoimmune Dis. 2014;2014.
24.
go back to reference Bhawal R, Fu Q, Anderson E, Gibson G, Zhang S. Serum metabolomic and lipidomic profiling reveals novel biomarkers of efficacy for benfotiamine in Alzheimer's disease. Int J Mol Sci 2021;22. Bhawal R, Fu Q, Anderson E, Gibson G, Zhang S. Serum metabolomic and lipidomic profiling reveals novel biomarkers of efficacy for benfotiamine in Alzheimer's disease. Int J Mol Sci 2021;22.
25.
go back to reference Shahid M, Yeon A, Kim J. Metabolomic and lipidomic approaches to identify biomarkers for bladder cancer and interstitial cystitis (Review). Mol Med Rep. 2020;22:5003–11.PubMedPubMedCentralCrossRef Shahid M, Yeon A, Kim J. Metabolomic and lipidomic approaches to identify biomarkers for bladder cancer and interstitial cystitis (Review). Mol Med Rep. 2020;22:5003–11.PubMedPubMedCentralCrossRef
26.
27.
go back to reference Clish C. Metabolomics: an emerging but powerful tool for precision medicine. Mol Case Stud. 2015;1: a000588.ADSCrossRef Clish C. Metabolomics: an emerging but powerful tool for precision medicine. Mol Case Stud. 2015;1: a000588.ADSCrossRef
28.
go back to reference Daviss B. Growing pains for metabolomics: the newest’omic science is producing results–and more data than researchers know what to do with. Scientist. 2005;19:25–9. Daviss B. Growing pains for metabolomics: the newest’omic science is producing results–and more data than researchers know what to do with. Scientist. 2005;19:25–9.
29.
go back to reference Lempp M, Farke N, Kuntz M, Freibert SA, Lill R, Link H. Systematic identification of metabolites controlling gene expression in E. coli. Nat Commun. 2019;10(1):4463.ADSPubMedPubMedCentralCrossRef Lempp M, Farke N, Kuntz M, Freibert SA, Lill R, Link H. Systematic identification of metabolites controlling gene expression in E. coli. Nat Commun. 2019;10(1):4463.ADSPubMedPubMedCentralCrossRef
30.
go back to reference Belhaj MR, Lawler NG, Hoffman NJ. Metabolomics and lipidomics: expanding the molecular landscape of exercise biology. Metabolites. 2021;11. Belhaj MR, Lawler NG, Hoffman NJ. Metabolomics and lipidomics: expanding the molecular landscape of exercise biology. Metabolites. 2021;11.
31.
go back to reference Aimetti M, Cacciatore S, Graziano A, Tenori L. Metabonomic analysis of saliva reveals generalized chronic periodontitis signature. Metabolomics. 2012;8:465–74.CrossRef Aimetti M, Cacciatore S, Graziano A, Tenori L. Metabonomic analysis of saliva reveals generalized chronic periodontitis signature. Metabolomics. 2012;8:465–74.CrossRef
32.
go back to reference Maher AD, Cloarec O, Patki P, et al. Dynamic biochemical information recovery in spontaneous human seminal fluid reactions via 1H NMR kinetic statistical total correlation spectroscopy. Anal Chem. 2009;81(1):288–95.PubMedCrossRef Maher AD, Cloarec O, Patki P, et al. Dynamic biochemical information recovery in spontaneous human seminal fluid reactions via 1H NMR kinetic statistical total correlation spectroscopy. Anal Chem. 2009;81(1):288–95.PubMedCrossRef
33.
34.
go back to reference Wishart DS. Metabolomics for investigating physiological and pathophysiological processes. Physiol Rev. 2019;99(4):1819–75.PubMedCrossRef Wishart DS. Metabolomics for investigating physiological and pathophysiological processes. Physiol Rev. 2019;99(4):1819–75.PubMedCrossRef
35.
go back to reference Roberts LD, Souza AL, Gerszten RE, Clish CB. Targeted metabolomics. Curr Protoc Mol Biol. 2012;98:30.2.1-.2.24. Roberts LD, Souza AL, Gerszten RE, Clish CB. Targeted metabolomics. Curr Protoc Mol Biol. 2012;98:30.2.1-.2.24.
36.
go back to reference Gowda GAN, Zhang S, Gu H, Asiago V, Shanaiah N, Raftery D. Metabolomics-based methods for early disease diagnostics. Expert Rev Mol Diagn. 2008;8:617–33.PubMedCrossRef Gowda GAN, Zhang S, Gu H, Asiago V, Shanaiah N, Raftery D. Metabolomics-based methods for early disease diagnostics. Expert Rev Mol Diagn. 2008;8:617–33.PubMedCrossRef
37.
go back to reference Cox DG, Oh J, Keasling A, Colson KL, Hamann MT. The utility of metabolomics in natural product and biomarker characterization. Biochim Biophys Acta Gen Subj. 2014;1840:3460–74.CrossRef Cox DG, Oh J, Keasling A, Colson KL, Hamann MT. The utility of metabolomics in natural product and biomarker characterization. Biochim Biophys Acta Gen Subj. 2014;1840:3460–74.CrossRef
38.
go back to reference Bertini I, Calabrò A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–7.PubMedCrossRef Bertini I, Calabrò A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–7.PubMedCrossRef
39.
go back to reference Garreta-Lara E, Gómez-Canela C, Campos B, Barata C, Tauler R, Lacorte S. Combined targeted/untargeted analytical and chemometric approaches in the characterization of Daphnia magna metabolomic changes under bisphenol A exposure. Microchem J. 2021;165: 106150.CrossRef Garreta-Lara E, Gómez-Canela C, Campos B, Barata C, Tauler R, Lacorte S. Combined targeted/untargeted analytical and chemometric approaches in the characterization of Daphnia magna metabolomic changes under bisphenol A exposure. Microchem J. 2021;165: 106150.CrossRef
40.
go back to reference Zhang X, Zhu X, Wang C, Zhang H, Cai Z. Non-targeted and targeted metabolomics approaches to diagnosing lung cancer and predicting patient prognosis. Oncotarget. 2016;7:63437.PubMedPubMedCentralCrossRef Zhang X, Zhu X, Wang C, Zhang H, Cai Z. Non-targeted and targeted metabolomics approaches to diagnosing lung cancer and predicting patient prognosis. Oncotarget. 2016;7:63437.PubMedPubMedCentralCrossRef
41.
go back to reference Roberts LD, Souza AL, Gerszten RE, Clish CB. Targeted metabolomics. Curr Protoc Mol Biol. 2012;98(1):30.2.1-.2.24. Roberts LD, Souza AL, Gerszten RE, Clish CB. Targeted metabolomics. Curr Protoc Mol Biol. 2012;98(1):30.2.1-.2.24.
42.
go back to reference Bernini P, Bertini I, Luchinat C, Tenori L, Tognaccini A. The cardiovascular risk of healthy individuals studied by NMR metabonomics of plasma samples. J Proteome Res. 2011;10:4983–92.PubMedCrossRef Bernini P, Bertini I, Luchinat C, Tenori L, Tognaccini A. The cardiovascular risk of healthy individuals studied by NMR metabonomics of plasma samples. J Proteome Res. 2011;10:4983–92.PubMedCrossRef
43.
go back to reference Bartsch T, Alfke K, Wolff S, Rohr A, Jansen O, Deuschl G. Focal MR spectroscopy of hippocampal CA-1 lesions in transient global amnesia. Neurology. 2008;70:1030–5.PubMedCrossRef Bartsch T, Alfke K, Wolff S, Rohr A, Jansen O, Deuschl G. Focal MR spectroscopy of hippocampal CA-1 lesions in transient global amnesia. Neurology. 2008;70:1030–5.PubMedCrossRef
44.
go back to reference Oakman C, Tenori L, Claudino W, et al. Identification of a serum-detectable metabolomic fingerprint potentially correlated with the presence of micrometastatic disease in early breast cancer patients at varying risks of disease relapse by traditional prognostic methods. Ann Oncol. 2011;22:1295–301.PubMedCrossRef Oakman C, Tenori L, Claudino W, et al. Identification of a serum-detectable metabolomic fingerprint potentially correlated with the presence of micrometastatic disease in early breast cancer patients at varying risks of disease relapse by traditional prognostic methods. Ann Oncol. 2011;22:1295–301.PubMedCrossRef
45.
go back to reference Sánchez E, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Bacteroides species associated with coeliac disease. J Clin Pathol. 2010;63:1105–11.PubMedCrossRef Sánchez E, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Bacteroides species associated with coeliac disease. J Clin Pathol. 2010;63:1105–11.PubMedCrossRef
46.
go back to reference Fathi F, Ektefa F, Oskouie AA, et al. NMR based metabonomics study on celiac disease in the blood serum. Gastroenterol Hepatol Bed Bench. 2013;6:190.PubMedPubMedCentral Fathi F, Ektefa F, Oskouie AA, et al. NMR based metabonomics study on celiac disease in the blood serum. Gastroenterol Hepatol Bed Bench. 2013;6:190.PubMedPubMedCentral
47.
go back to reference Khalkhal E, Rezaei-Tavirani M, Fathi F, et al. Screening of altered metabolites and metabolic pathways in celiac disease using NMR spectroscopy. Biomed Res Int. 2021;2021. Khalkhal E, Rezaei-Tavirani M, Fathi F, et al. Screening of altered metabolites and metabolic pathways in celiac disease using NMR spectroscopy. Biomed Res Int. 2021;2021.
48.
go back to reference Yuan C, Graham M, Staley C, Subramanian S. Mucosal microbiota and metabolome along the intestinal tract reveal a location-specific relationship. Msystems. 2020;5:e00055-e120.PubMedPubMedCentralCrossRef Yuan C, Graham M, Staley C, Subramanian S. Mucosal microbiota and metabolome along the intestinal tract reveal a location-specific relationship. Msystems. 2020;5:e00055-e120.PubMedPubMedCentralCrossRef
49.
go back to reference McHardy IH, Goudarzi M, Tong M, et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome. 2013;1:17.PubMedPubMedCentralCrossRef McHardy IH, Goudarzi M, Tong M, et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome. 2013;1:17.PubMedPubMedCentralCrossRef
50.
go back to reference Leonard MM, Kenyon V, Valitutti F, Pennacchio-Harrington R, Piemontese P, Francavilla R, et al. Cohort profile: celiac disease genomic, environmental, microbiome and metabolome study; a prospective longitudinal birth cohort study of children at-risk for celiac disease. PLoS ONE. 2023;18(3): e0282739.PubMedPubMedCentralCrossRef Leonard MM, Kenyon V, Valitutti F, Pennacchio-Harrington R, Piemontese P, Francavilla R, et al. Cohort profile: celiac disease genomic, environmental, microbiome and metabolome study; a prospective longitudinal birth cohort study of children at-risk for celiac disease. PLoS ONE. 2023;18(3): e0282739.PubMedPubMedCentralCrossRef
51.
go back to reference DaFonte TM, Valitutti F, Kenyon V, Locascio JJ, Montuori M, Francavilla R, et al. Zonulin as a biomarker for the development of celiac disease. Pediatrics. 2023. DaFonte TM, Valitutti F, Kenyon V, Locascio JJ, Montuori M, Francavilla R, et al. Zonulin as a biomarker for the development of celiac disease. Pediatrics. 2023.
52.
go back to reference Leonard MM, Valitutti F, Karathia H, Pujolassos M, Kenyon V, Fanelli B, et al. Microbiome signatures of progression toward celiac disease onset in at-risk children in a longitudinal prospective cohort study. Proc Natl Acad Sci USA. 2021;118(29). Leonard MM, Valitutti F, Karathia H, Pujolassos M, Kenyon V, Fanelli B, et al. Microbiome signatures of progression toward celiac disease onset in at-risk children in a longitudinal prospective cohort study. Proc Natl Acad Sci USA. 2021;118(29).
53.
go back to reference Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci. 2011;108:4578–85.ADSPubMedCrossRef Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci. 2011;108:4578–85.ADSPubMedCrossRef
54.
go back to reference Vacca M, Porrelli A, Calabrese FM, et al. How metabolomics provides novel insights on celiac disease and gluten-free diet: a narrative review. Front Microbiol. 2022;13. Vacca M, Porrelli A, Calabrese FM, et al. How metabolomics provides novel insights on celiac disease and gluten-free diet: a narrative review. Front Microbiol. 2022;13.
55.
go back to reference Sanz Y, Palma GD, Laparra M. Unraveling the ties between celiac disease and intestinal microbiota. Int Rev Immunol. 2011;30:207–18.PubMedCrossRef Sanz Y, Palma GD, Laparra M. Unraveling the ties between celiac disease and intestinal microbiota. Int Rev Immunol. 2011;30:207–18.PubMedCrossRef
56.
go back to reference Sánchez E, Donat E, Ribes-Koninckx C, Fernández-Murga ML, Sanz Y. Duodenal-mucosal bacteria associated with celiac disease in children. Appl Environ Microbiol. 2013;79:5472–9.ADSPubMedPubMedCentralCrossRef Sánchez E, Donat E, Ribes-Koninckx C, Fernández-Murga ML, Sanz Y. Duodenal-mucosal bacteria associated with celiac disease in children. Appl Environ Microbiol. 2013;79:5472–9.ADSPubMedPubMedCentralCrossRef
57.
go back to reference Sanz Y, Sánchez E, Marzotto M, Calabuig M, Torriani S, Dellaglio F. Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol. 2007;51:562–8.PubMedCrossRef Sanz Y, Sánchez E, Marzotto M, Calabuig M, Torriani S, Dellaglio F. Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol. 2007;51:562–8.PubMedCrossRef
58.
go back to reference Wacklin P, Kaukinen K, Tuovinen E, et al. The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease. Inflamm Bowel Dis. 2013;19(5):934–41.PubMedCrossRef Wacklin P, Kaukinen K, Tuovinen E, et al. The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease. Inflamm Bowel Dis. 2013;19(5):934–41.PubMedCrossRef
59.
go back to reference Kalliomäki M, Satokari R, Lähteenoja H, et al. Expression of microbiota, Toll-like receptors, and their regulators in the small intestinal mucosa in celiac disease. J Pediatr Gastroenterol Nutr. 2012;54:727–32.PubMedCrossRef Kalliomäki M, Satokari R, Lähteenoja H, et al. Expression of microbiota, Toll-like receptors, and their regulators in the small intestinal mucosa in celiac disease. J Pediatr Gastroenterol Nutr. 2012;54:727–32.PubMedCrossRef
60.
go back to reference Girbovan A, Sur G, Samasca G, Lupan I. Dysbiosis a risk factor for celiac disease. Med Microbiol Immunol. 2017;206:83–91.PubMedCrossRef Girbovan A, Sur G, Samasca G, Lupan I. Dysbiosis a risk factor for celiac disease. Med Microbiol Immunol. 2017;206:83–91.PubMedCrossRef
61.
go back to reference Leonard MM, Karathia H, Pujolassos M, et al. Multi-omics analysis reveals the influence of genetic and environmental risk factors on developing gut microbiota in infants at risk of celiac disease. Microbiome. 2020;8:130.PubMedPubMedCentralCrossRef Leonard MM, Karathia H, Pujolassos M, et al. Multi-omics analysis reveals the influence of genetic and environmental risk factors on developing gut microbiota in infants at risk of celiac disease. Microbiome. 2020;8:130.PubMedPubMedCentralCrossRef
62.
go back to reference Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci. 2009;106:3698–703.ADSPubMedPubMedCentralCrossRef Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci. 2009;106:3698–703.ADSPubMedPubMedCentralCrossRef
63.
go back to reference Shi T, Feng Y, Liu W, et al. Characteristics of gut microbiota and fecal metabolomes in patients with celiac disease in Northwest China. Front Microbiol. 2022;13:1020977.PubMedPubMedCentralCrossRef Shi T, Feng Y, Liu W, et al. Characteristics of gut microbiota and fecal metabolomes in patients with celiac disease in Northwest China. Front Microbiol. 2022;13:1020977.PubMedPubMedCentralCrossRef
64.
go back to reference Girdhar K, Dogru YD, Huang Q, et al. Dynamics of the gut microbiome, IgA response, and plasma metabolome in the development of pediatric celiac disease. Microbiome. 2023;11:9.PubMedPubMedCentralCrossRef Girdhar K, Dogru YD, Huang Q, et al. Dynamics of the gut microbiome, IgA response, and plasma metabolome in the development of pediatric celiac disease. Microbiome. 2023;11:9.PubMedPubMedCentralCrossRef
65.
go back to reference Tjellström B, Stenhammar L, Högberg L, et al. Gut microflora associated characteristics in children with celiac disease. Am J Gastroenterol. 2005;100:2784–8.PubMedCrossRef Tjellström B, Stenhammar L, Högberg L, et al. Gut microflora associated characteristics in children with celiac disease. Am J Gastroenterol. 2005;100:2784–8.PubMedCrossRef
66.
go back to reference Caminero A, Nistal E, Herrán AR, et al. Differences in gluten metabolism among healthy volunteers, coeliac disease patients and first-degree relatives. Br J Nutr. 2015;114:1157–67.PubMedCrossRef Caminero A, Nistal E, Herrán AR, et al. Differences in gluten metabolism among healthy volunteers, coeliac disease patients and first-degree relatives. Br J Nutr. 2015;114:1157–67.PubMedCrossRef
67.
go back to reference Portincasa P, Bonfrate L, Vacca M, et al. Gut microbiota and short chain fatty acids: implications in glucose homeostasis. Int J Mol Sci. 2022;23. Portincasa P, Bonfrate L, Vacca M, et al. Gut microbiota and short chain fatty acids: implications in glucose homeostasis. Int J Mol Sci. 2022;23.
68.
go back to reference Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol. 2011;11:1–21.CrossRef Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol. 2011;11:1–21.CrossRef
69.
go back to reference Khalkhal E, Rezaei-Tavirani M, Fathi F, et al. Screening of altered metabolites and metabolic pathways in celiac disease using NMR spectroscopy. Biomed Res Int. 2021;2021:1798783.PubMedPubMedCentralCrossRef Khalkhal E, Rezaei-Tavirani M, Fathi F, et al. Screening of altered metabolites and metabolic pathways in celiac disease using NMR spectroscopy. Biomed Res Int. 2021;2021:1798783.PubMedPubMedCentralCrossRef
70.
go back to reference Farnetti S, Zocco MA, Garcovich M, Gasbarrini A, Capristo E. Functional and metabolic disorders in celiac disease: new implications for nutritional treatment. J Med Food. 2014;17:1159–64.PubMedCrossRef Farnetti S, Zocco MA, Garcovich M, Gasbarrini A, Capristo E. Functional and metabolic disorders in celiac disease: new implications for nutritional treatment. J Med Food. 2014;17:1159–64.PubMedCrossRef
71.
go back to reference Abenavoli L, Delibasic M, Peta V, Turkulov V, De Lorenzo A, Medić-Stojanoska M. Nutritional profile of adult patients with celiac disease. Eur Rev Med Pharmacol Sci. 2015;19:4285–92.PubMed Abenavoli L, Delibasic M, Peta V, Turkulov V, De Lorenzo A, Medić-Stojanoska M. Nutritional profile of adult patients with celiac disease. Eur Rev Med Pharmacol Sci. 2015;19:4285–92.PubMed
72.
go back to reference Bernini P, Bertini I, Calabrò A, et al. Are patients with potential celiac disease really potential? The answer of metabonomics. J Proteome Res. 2011;10:714–21.PubMedCrossRef Bernini P, Bertini I, Calabrò A, et al. Are patients with potential celiac disease really potential? The answer of metabonomics. J Proteome Res. 2011;10:714–21.PubMedCrossRef
73.
go back to reference Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol. 2011;11:219.PubMedPubMedCentralCrossRef Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol. 2011;11:219.PubMedPubMedCentralCrossRef
74.
go back to reference Kirchberg FF, Werkstetter KJ, Uhl O, et al. Investigating the early metabolic fingerprint of celiac disease—a prospective approach. J Autoimmun. 2016;72:95–101.PubMedCrossRef Kirchberg FF, Werkstetter KJ, Uhl O, et al. Investigating the early metabolic fingerprint of celiac disease—a prospective approach. J Autoimmun. 2016;72:95–101.PubMedCrossRef
75.
go back to reference Sen P, Carlsson C, Virtanen SM, et al. Persistent alterations in plasma lipid profiles before introduction of gluten in the diet associated with progression to celiac disease. Clin Transl Gastroenterol. 2019;10:1–10.PubMedCrossRef Sen P, Carlsson C, Virtanen SM, et al. Persistent alterations in plasma lipid profiles before introduction of gluten in the diet associated with progression to celiac disease. Clin Transl Gastroenterol. 2019;10:1–10.PubMedCrossRef
76.
go back to reference Di Stefano M, Miceli E, Mengoli C, Corazza GR, Di Sabatino A. The effect of a gluten-free diet on vitamin D metabolism in celiac disease: the state of the art. Metabolites. 2023;13. Di Stefano M, Miceli E, Mengoli C, Corazza GR, Di Sabatino A. The effect of a gluten-free diet on vitamin D metabolism in celiac disease: the state of the art. Metabolites. 2023;13.
77.
go back to reference Upadhyay D, Singh A, Das P, et al. Abnormalities in metabolic pathways in celiac disease investigated by the metabolic profiling of small intestinal mucosa, blood plasma and urine by NMR spectroscopy. NMR Biomed. 2020;33: e4305.PubMedCrossRef Upadhyay D, Singh A, Das P, et al. Abnormalities in metabolic pathways in celiac disease investigated by the metabolic profiling of small intestinal mucosa, blood plasma and urine by NMR spectroscopy. NMR Biomed. 2020;33: e4305.PubMedCrossRef
78.
go back to reference Bertini I, Calabro A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–7.PubMedCrossRef Bertini I, Calabro A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–7.PubMedCrossRef
79.
go back to reference Tracey TJ, Kirk SE, Steyn FJ, Ngo ST. The role of lipids in the central nervous system and their pathological implications in amyotrophic lateral sclerosis. Semin Cell Dev Biol. 2021;112:69–81.PubMedCrossRef Tracey TJ, Kirk SE, Steyn FJ, Ngo ST. The role of lipids in the central nervous system and their pathological implications in amyotrophic lateral sclerosis. Semin Cell Dev Biol. 2021;112:69–81.PubMedCrossRef
80.
go back to reference Ademowo OS, Dias H, Burton DG, Griffiths HR. Lipid (per) oxidation in mitochondria: an emerging target in the ageing process? Biogerontology. 2017;18:859–79.PubMedPubMedCentralCrossRef Ademowo OS, Dias H, Burton DG, Griffiths HR. Lipid (per) oxidation in mitochondria: an emerging target in the ageing process? Biogerontology. 2017;18:859–79.PubMedPubMedCentralCrossRef
81.
go back to reference Das UN. “Cell membrane theory of senescence” and the role of bioactive lipids in aging, and aging associated diseases and their therapeutic implications. Biomolecules. 2021;11. Das UN. “Cell membrane theory of senescence” and the role of bioactive lipids in aging, and aging associated diseases and their therapeutic implications. Biomolecules. 2021;11.
82.
go back to reference Desai AJ, Miller LJ. Changes in the plasma membrane in metabolic disease: impact of the membrane environment on G protein-coupled receptor structure and function. Br J Pharmacol. 2018;175(21):4009–25.PubMedCrossRef Desai AJ, Miller LJ. Changes in the plasma membrane in metabolic disease: impact of the membrane environment on G protein-coupled receptor structure and function. Br J Pharmacol. 2018;175(21):4009–25.PubMedCrossRef
83.
go back to reference O’Donnell VB, Ekroos K, Liebisch G, Wakelam M. Lipidomics: current state of the art in a fast moving field. Wiley Interdiscip Rev Syst Biol Med. 2020;12: e1466.PubMedCrossRef O’Donnell VB, Ekroos K, Liebisch G, Wakelam M. Lipidomics: current state of the art in a fast moving field. Wiley Interdiscip Rev Syst Biol Med. 2020;12: e1466.PubMedCrossRef
84.
go back to reference Torres M, Parets S, Fernández-Díaz J, et al. Lipids in pathophysiology and development of the membrane lipid therapy: new bioactive lipids. Membranes (Basel). 2021;11. Torres M, Parets S, Fernández-Díaz J, et al. Lipids in pathophysiology and development of the membrane lipid therapy: new bioactive lipids. Membranes (Basel). 2021;11.
85.
go back to reference Züllig T, Trötzmüller M, Köfeler HC. Lipidomics from sample preparation to data analysis: a primer. Anal Bioanal Chem. 2020;412:2191–209.PubMedCrossRef Züllig T, Trötzmüller M, Köfeler HC. Lipidomics from sample preparation to data analysis: a primer. Anal Bioanal Chem. 2020;412:2191–209.PubMedCrossRef
86.
go back to reference Fahy E, Cotter D, Sud M, Subramaniam S. Lipid classification, structures and tools. Biochim Biophys Acta Mol Cell Biol Lipids. 2011;1811:637–47.CrossRef Fahy E, Cotter D, Sud M, Subramaniam S. Lipid classification, structures and tools. Biochim Biophys Acta Mol Cell Biol Lipids. 2011;1811:637–47.CrossRef
88.
go back to reference Lam SM, Tian H, Shui G. Lipidomics, en route to accurate quantitation. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862:752–61.PubMedCrossRef Lam SM, Tian H, Shui G. Lipidomics, en route to accurate quantitation. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862:752–61.PubMedCrossRef
89.
90.
go back to reference Titz B, Gadaleta RM, Lo Sasso G, et al. Proteomics and lipidomics in inflammatory bowel disease research: from mechanistic insights to biomarker identification. Int J Mol Sci. 2018;19:2775.PubMedPubMedCentralCrossRef Titz B, Gadaleta RM, Lo Sasso G, et al. Proteomics and lipidomics in inflammatory bowel disease research: from mechanistic insights to biomarker identification. Int J Mol Sci. 2018;19:2775.PubMedPubMedCentralCrossRef
91.
go back to reference Diab J, Hansen T, Goll R, et al. Lipidomics in ulcerative colitis reveal alteration in mucosal lipid composition associated with the disease state. Inflamm Bowel Dis. 2019;25:1780–7.PubMedCrossRef Diab J, Hansen T, Goll R, et al. Lipidomics in ulcerative colitis reveal alteration in mucosal lipid composition associated with the disease state. Inflamm Bowel Dis. 2019;25:1780–7.PubMedCrossRef
92.
93.
go back to reference Lin P-Y, Stern A, Peng H-H, Chen J-H, Yang H-C. Redox and metabolic regulation of intestinal barrier function and associated disorders. Int J Mol Sci. 2022;23:14463.PubMedPubMedCentralCrossRef Lin P-Y, Stern A, Peng H-H, Chen J-H, Yang H-C. Redox and metabolic regulation of intestinal barrier function and associated disorders. Int J Mol Sci. 2022;23:14463.PubMedPubMedCentralCrossRef
94.
go back to reference Wit M, Trujillo-Viera J, Strohmeyer A, Klingenspor M, Hankir M, Sumara G. When fat meets the gut—focus on intestinal lipid handling in metabolic health and disease. EMBO Mol Med. 2022;14: e14742.PubMedPubMedCentralCrossRef Wit M, Trujillo-Viera J, Strohmeyer A, Klingenspor M, Hankir M, Sumara G. When fat meets the gut—focus on intestinal lipid handling in metabolic health and disease. EMBO Mol Med. 2022;14: e14742.PubMedPubMedCentralCrossRef
95.
go back to reference Ko C-W, Qu J, Black DD, Tso P. Regulation of intestinal lipid metabolism: current concepts and relevance to disease. Nat Rev Gastroenterol. 2020;17:169–83.CrossRef Ko C-W, Qu J, Black DD, Tso P. Regulation of intestinal lipid metabolism: current concepts and relevance to disease. Nat Rev Gastroenterol. 2020;17:169–83.CrossRef
96.
go back to reference Pan X, Hussain MM. Gut triglyceride production. Biochim Biophys Acta. 1821;2012:727–35. Pan X, Hussain MM. Gut triglyceride production. Biochim Biophys Acta. 1821;2012:727–35.
97.
go back to reference D'Aquila T, Hung Y-H, Carreiro A, Buhman KK. Recent discoveries on absorption of dietary fat: presence, synthesis, and metabolism of cytoplasmic lipid droplets within enterocytes. Biochim Biophys Acta Mol Cell Biol Lipids. 2016;1861(8, Part A):730–47. D'Aquila T, Hung Y-H, Carreiro A, Buhman KK. Recent discoveries on absorption of dietary fat: presence, synthesis, and metabolism of cytoplasmic lipid droplets within enterocytes. Biochim Biophys Acta Mol Cell Biol Lipids. 2016;1861(8, Part A):730–47.
98.
go back to reference Monson EA, Trenerry AM, Laws JL, Mackenzie JM, Helbig KJ. Lipid droplets and lipid mediators in viral infection and immunity. FEMS Microbiol Rev. 2021;45:fuaa066. Monson EA, Trenerry AM, Laws JL, Mackenzie JM, Helbig KJ. Lipid droplets and lipid mediators in viral infection and immunity. FEMS Microbiol Rev. 2021;45:fuaa066.
99.
go back to reference Steel DM, Ryd W, Ascher H, Strandvik B. Abnormal fatty acid pattern in intestinal mucosa of children with celiac disease is not reflected in serum phospholipids. J Pediatr Gastroenterol Nutr. 2006;43:318–23.PubMedCrossRef Steel DM, Ryd W, Ascher H, Strandvik B. Abnormal fatty acid pattern in intestinal mucosa of children with celiac disease is not reflected in serum phospholipids. J Pediatr Gastroenterol Nutr. 2006;43:318–23.PubMedCrossRef
100.
go back to reference Bene J, Komlósi K, Gasztonyi B, Juhász M, Tulassay Z, Melegh B. Plasma carnitine ester profile in adult celiac disease patients maintained on long-term gluten free diet. World J Gastroenterol. 2005;11:6671.PubMedPubMedCentralCrossRef Bene J, Komlósi K, Gasztonyi B, Juhász M, Tulassay Z, Melegh B. Plasma carnitine ester profile in adult celiac disease patients maintained on long-term gluten free diet. World J Gastroenterol. 2005;11:6671.PubMedPubMedCentralCrossRef
101.
go back to reference Solakivi T, Kaukinen K, Kunnas T, Lehtimäki T, Mäki M, Nikkari ST. Serum fatty acid profile in celiac disease patients before and after a gluten-free diet. Scand J Gastroenterol. 2009;44:826–30.PubMedCrossRef Solakivi T, Kaukinen K, Kunnas T, Lehtimäki T, Mäki M, Nikkari ST. Serum fatty acid profile in celiac disease patients before and after a gluten-free diet. Scand J Gastroenterol. 2009;44:826–30.PubMedCrossRef
102.
go back to reference Sen P, Carlsson C, Virtanen SM, et al. Persistent alterations in plasma lipid profiles before introduction of gluten in the diet associated with progression to celiac disease. Clin Transl Gastroenterol. 2019;10. Sen P, Carlsson C, Virtanen SM, et al. Persistent alterations in plasma lipid profiles before introduction of gluten in the diet associated with progression to celiac disease. Clin Transl Gastroenterol. 2019;10.
103.
go back to reference Baldi S, Menicatti M, Nannini G, et al. Free fatty acids signature in human intestinal disorders: significant association between butyric acid and celiac disease. Nutrients. 2021;13. Baldi S, Menicatti M, Nannini G, et al. Free fatty acids signature in human intestinal disorders: significant association between butyric acid and celiac disease. Nutrients. 2021;13.
104.
105.
go back to reference Kochhar GS, Singh T, Gill A, Kirby DF. Celiac disease: managing a multisystem disorder. Cleve Clin J Med. 2016;83:217–27.PubMedCrossRef Kochhar GS, Singh T, Gill A, Kirby DF. Celiac disease: managing a multisystem disorder. Cleve Clin J Med. 2016;83:217–27.PubMedCrossRef
106.
go back to reference Busby E, Bold J, Fellows L, Rostami K. Mood disorders and gluten: It's not all in your mind! A systematic review with meta-analysis. Nutrients. 2018;10. Busby E, Bold J, Fellows L, Rostami K. Mood disorders and gluten: It's not all in your mind! A systematic review with meta-analysis. Nutrients. 2018;10.
107.
go back to reference van Hees NJ, Giltay EJ, Geleijnse JM, Janssen N, van der Does W. DHA serum levels were significantly higher in celiac disease patients compared to healthy controls and were unrelated to depression. PLoS ONE. 2014;9: e97778.ADSPubMedPubMedCentralCrossRef van Hees NJ, Giltay EJ, Geleijnse JM, Janssen N, van der Does W. DHA serum levels were significantly higher in celiac disease patients compared to healthy controls and were unrelated to depression. PLoS ONE. 2014;9: e97778.ADSPubMedPubMedCentralCrossRef
108.
go back to reference Harris RB, Foote JA, Hakim IA, Bronson DL, Alberts DS. Fatty acid composition of red blood cell membranes and risk of squamous cell carcinoma of the skin. Cancer Epidemiol Biomarkers Prev. 2005;14:906–12.PubMedCrossRef Harris RB, Foote JA, Hakim IA, Bronson DL, Alberts DS. Fatty acid composition of red blood cell membranes and risk of squamous cell carcinoma of the skin. Cancer Epidemiol Biomarkers Prev. 2005;14:906–12.PubMedCrossRef
109.
go back to reference Riezzo G, Ferreri C, Orlando A, Martulli M, D’Attoma B, Russo F. Lipidomic analysis of fatty acids in erythrocytes of coeliac patients before and after a gluten-free diet intervention: a comparison with healthy subjects. Br J Nutr. 2014;112:1787–96.PubMedCrossRef Riezzo G, Ferreri C, Orlando A, Martulli M, D’Attoma B, Russo F. Lipidomic analysis of fatty acids in erythrocytes of coeliac patients before and after a gluten-free diet intervention: a comparison with healthy subjects. Br J Nutr. 2014;112:1787–96.PubMedCrossRef
110.
go back to reference Ginocchio VM, Brunetti-Pierri N. Progress toward improved therapies for inborn errors of metabolism. Hum Mol Genet. 2016;25:R27–35.PubMedCrossRef Ginocchio VM, Brunetti-Pierri N. Progress toward improved therapies for inborn errors of metabolism. Hum Mol Genet. 2016;25:R27–35.PubMedCrossRef
111.
go back to reference Agarwal A, Singh A, Mehtab W, et al. Patients with celiac disease are at high risk of developing metabolic syndrome and fatty liver. Intest Res. 2021;19:106–14.PubMedCrossRef Agarwal A, Singh A, Mehtab W, et al. Patients with celiac disease are at high risk of developing metabolic syndrome and fatty liver. Intest Res. 2021;19:106–14.PubMedCrossRef
Metadata
Title
Metabolomics and lipidomics signature in celiac disease: a narrative review
Authors
Mohammad Rostami-Nejad
Nastaran Asri
Sajjad Bakhtiari
Ensieh Khalkhal
Sepehr Maleki
Mostafa Rezaei-Tavirani
Somayeh Jahani-Sherafat
Kamran Rostami
Publication date
01-12-2024
Publisher
Springer International Publishing
Published in
Clinical and Experimental Medicine / Issue 1/2024
Print ISSN: 1591-8890
Electronic ISSN: 1591-9528
DOI
https://doi.org/10.1007/s10238-024-01295-2

Other articles of this Issue 1/2024

Clinical and Experimental Medicine 1/2024 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.