The study evaluating the effect of probiotic supplementation on the mental status, inflammation, and intestinal barrier in major depressive disorder patients using gluten-free or gluten-containing diet (SANGUT study): a 12-week, randomized, double-blind, and placebo-controlled clinical study protocol

Hanna Karakula-Juchnowicz, Joanna Rog, Dariusz Juchnowicz, Igor Łoniewski, Karolina Skonieczna-Żydecka, Paweł Krukow, Malgorzata Futyma-Jedrzejewska, Mariusz Kaczmarczyk, Hanna Karakula-Juchnowicz, Joanna Rog, Dariusz Juchnowicz, Igor Łoniewski, Karolina Skonieczna-Żydecka, Paweł Krukow, Malgorzata Futyma-Jedrzejewska, Mariusz Kaczmarczyk

Abstract

Background: Current treatment of major depressive disorder (MDD) often does not achieve full remission of symptoms. Therefore, new forms of treatment and/or adjunct therapy are needed. Evidence has confirmed the modulation of the gut-brain-microbiota axis as a promising approach in MDD patients. The overall purpose of the SANGUT study-a 12-week, randomized, double-blind, and placebo-controlled Study Evaluating the Effect of Probiotic Supplementation on the Mental Status, Inflammation, and Intestinal Barrier in Major Depressive Disorder Patients Using Gluten-free or Gluten-containing Diet - is to determine the effect of interventions focused on the gut-brain-microbiota axis in a group of MDD patients.

Methods: A total of 120 outpatients will be equally allocated into one of four groups: (1) probiotic supplementation+gluten-free diet group (PRO-GFD), (2) placebo supplementation+ gluten-free diet group (PLA-GFD), (3) probiotic supplementation+ gluten containing diet group (PRO-GD), and (4) placebo supplementation+gluten containing diet group (PLA-GD). PRO groups will receive a mixture of psychobiotics (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175), and GFD groups will follow a gluten-free diet. The intervention will last 12 weeks. The primary outcome measure is change in wellbeing, whereas the secondary outcome measures include physiological parameters.

Discussion: Microbiota and its metabolites have the potential to influence CNS function. Probiotics may restore the eubiosis within the gut while a gluten-free diet, via changes in the microbiota profile and modulation of intestinal permeability, may alter the activity of microbiota-gut-brain axis previously found to be associated with the pathophysiology of depression. It is also noteworthy that microbiota being able to digest gluten may play a role in formation of peptides with different immunogenic capacities. Thus, the combination of a gluten-free diet and probiotic supplementation may inhibit the immune-inflammatory cascade in MDD course and improve both psychiatric and gut barrier-associated traits.

Trial registration: NCT03877393 .

Keywords: Depression; EEG functional connectivity; Gluten-free diet; Gut microbiota; Gut permeability; Gut-brain axis; Inflammation; Intervention study; Probiotics; Study protocol.

Conflict of interest statement

I.Ł. is a foundation shareholder in Sanprobi, a probiotics distributor. K.S-Ż and H.K-J received remuneration from Sanprobi. However, the content of this study was not constrained by this fact. Moreover, our adherence to Nutrition Journal policies on sharing of data and materials was unaffected. The other authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Timeline of SANGUT STUDY visits. V0 – Screening visit; V1 – Baseline Visit; V2 – Visit 2; V3 – End of Study Visit

References

    1. Depression in Europe: facts and figures. 2019 Cited 2019 Mar 7. Available from:
    1. Depression in Europe. 2012 Cited 2019 Mar 7. Available from:
    1. Mrazek DA, Hornberger JC, Altar CA, Degtiar I. A review of the clinical, economic, and societal burden of treatment-resistant depression: 1996-2013. Psychiatr Serv. 2014;65:977–987. doi: 10.1176/appi.ps.201300059.
    1. Rantala MJ, Luoto S, Krams I, Karlsson H. Depression subtyping based on evolutionary psychiatry: proximate mechanisms and ultimate functions. Brain Behav Immun. 2018;69:603–617. doi: 10.1016/j.bbi.2017.10.012.
    1. Miller AH, Raison CL. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat Rev Immunol. 2016;16:22–34. doi: 10.1038/nri.2015.5.
    1. Al-Hakeim H, Twayej AJ, Al-Dujaili AH, Maes M. Ketoprofen as an add-on treatment to sertraline for drug-Naïve major depressed patients: normalization of plasma levels of Indoleamine-2, 3-dioxygenase in association with pro-inflammatory and immune regulatory cytokines. 2018.
    1. Dooley LN, Kuhlman KR, Robles TF, Eisenberger NI, Craske MG, Bower JE. The role of inflammation in core features of depression: insights from paradigms using exogenously-induced inflammation. Neurosci Biobehav Rev. 2018;94:219–237. doi: 10.1016/j.neubiorev.2018.09.006.
    1. Kipnis J, Filiano AJ. Neuroimmunology in 2017: the central nervous system: privileged by immune connections. Nat Rev Immunol. 2018;18:83–84. doi: 10.1038/nri.2017.152.
    1. Fenster RJ, Eisen JL. Checking the Brain’s immune privilege: evolving theories of brain–immune interactions. Biol Psychiatry. 2017;81:e7–e9. doi: 10.1016/j.biopsych.2016.10.027.
    1. Smith RS. The macrophage theory of depression. Med Hypotheses. 1991;35:298–306. doi: 10.1016/0306-9877(91)90272-Z.
    1. Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 2015;28:203–209.
    1. Chinthrajah RS, Hernandez JD, Boyd SD, Galli SJ, Nadeau KC. Molecular and cellular mechanisms of food allergy and food tolerance. J Allergy Clin Immunol. 2016;137:984–997. doi: 10.1016/j.jaci.2016.02.004.
    1. Karakuła-Juchnowicz H, Szachta P, Opolska A, Morylowska-Topolska J, Gałęcka M, Juchnowicz D, et al. The role of IgG hypersensitivity in the pathogenesis and therapy of depressive disorders. Nutr Neurosci. 2017;20:110–118. doi: 10.1179/1476830514Y.0000000158.
    1. Karakula-Juchnowicz Hanna, Gałęcka Mirosława, Rog Joanna, Bartnicka Anna, Łukaszewicz Zuzanna, Krukow Pawel, Morylowska-Topolska Justyna, Skonieczna-Zydecka Karolina, Krajka Tomasz, Jonak Kamil, Juchnowicz Dariusz. The Food-Specific Serum IgG Reactivity in Major Depressive Disorder Patients, Irritable Bowel Syndrome Patients and Healthy Controls. Nutrients. 2018;10(5):548. doi: 10.3390/nu10050548.
    1. Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, et al. Targeting the microbiota-gut-brain Axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry. 2017;82:472–487. doi: 10.1016/j.biopsych.2016.12.031.
    1. Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF. Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Transl Res. 2017;179:223–244. doi: 10.1016/j.trsl.2016.10.002.
    1. Severance EG, Yolken RH. Deciphering microbiome and neuroactive immune gene interactions in schizophrenia. Neurobiol Dis. 2018; Available from: .
    1. Mahmoodpoor F, Saadat YR, Barzegari A, Ardalan M, Vahed SZ. The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharmacother. 2017;93:412–419. doi: 10.1016/j.biopha.2017.06.066.
    1. Nagpal R, Newman TM, Wang S, Jain S, Lovato JF, Yadav H. Obesity-linked gut microbiome Dysbiosis associated with derangements in gut permeability and intestinal cellular homeostasis independent of diet. J Diabetes Res. 2018;2018:3462092. doi: 10.1155/2018/3462092.
    1. Jang SE, Lim SM, Jeong JJ, Jang HM, Lee HJ, Han MJ, et al. Gastrointestinal inflammation by gut microbiota disturbance induces memory impairment in mice. Mucosal Immunol. 2018;11:369–379. doi: 10.1038/mi.2017.49.
    1. Jalanka-Tuovinen J, Salojärvi J, Salonen A, Immonen O, Garsed K, Kelly FM, et al. Faecal microbiota composition and host–microbe cross-talk following gastroenteritis and in postinfectious irritable bowel syndrome. Gut. 2014; Cited 2019 Jun 20. Available from: .
    1. Chen P, Stärkel P, Turner JR, Ho SB, Schnabl B. Dysbiosis-induced intestinal inflammation activates tumor necrosis factor receptor I and mediates alcoholic liver disease in mice. Hepatology. 2015;61:883–894. doi: 10.1002/hep.27489.
    1. Hu J, Luo H, Wang J, Tang W, Lu J, Wu S, et al. Enteric dysbiosis-linked gut barrier disruption triggers early renal injury induced by chronic high salt feeding in mice. Exp Mol Med. 2017;49:e370. doi: 10.1038/emm.2017.122.
    1. Pellegrini C, Antonioli L, Colucci R, Blandizzi C, Fornai M. Interplay among gut microbiota, intestinal mucosal barrier and enteric neuro-immune system: a common path to neurodegenerative diseases? Acta Neuropathol. 2018;136:345–361. doi: 10.1007/s00401-018-1856-5.
    1. Huang Ruixue, Wang Ke, Hu Jianan. Effect of Probiotics on Depression: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients. 2016;8(8):483. doi: 10.3390/nu8080483.
    1. Ng QX, Peters C, Ho CYX, Lim DY, Yeo WS. A meta-analysis of the use of probiotics to alleviate depressive symptoms. J Affect Disord. 2018;228:13–19. doi: 10.1016/j.jad.2017.11.063.
    1. Liang S, Wu X, Hu X, Wang T, Jin F. Recognizing depression from the microbiota–gut–brain axis. Int J Mol Sci. 2018;19:1592. doi: 10.3390/ijms19061592.
    1. Dinan TG, Cryan JF. Melancholic microbes: a link between gut microbiota and depression? Neurogastroenterol Motil. 2013;25:713–719. doi: 10.1111/nmo.12198.
    1. Huo R, Zeng B, Zeng L, Cheng K, Li B, Luo Y, et al. Microbiota modulate anxiety-like behavior and endocrine abnormalities in hypothalamic-pituitary-adrenal axis. Front Cell Infect Microbiol. 2017;7:489. doi: 10.3389/fcimb.2017.00489.
    1. Zingone F, Swift GL, Card TR, Sanders DS, Ludvigsson JF, Bai JC. Psychological morbidity of celiac disease: a review of the literature. United European Gastroenterol J. 2015;3:136–145. doi: 10.1177/2050640614560786.
    1. Fasano A. Celiac Disease, Gut-Brain Axis, and Behavior: Cause, Consequence, or Merely Epiphenomenon? Pediatrics. 2017;139:e20164323. doi: 10.1542/peds.2016-4323.
    1. Sander GR, Cummins AG, Henshall T, Powell BC. Rapid disruption of intestinal barrier function by gliadin involves altered expression of apical junctional proteins. FEBS Lett. 2005;579:4851–4855. doi: 10.1016/j.febslet.2005.07.066.
    1. Vazquez-Roque MI, Camilleri M, Smyrk T, Murray JA, Marietta E, O’Neill J, et al. A controlled trial of gluten-free diet in patients with irritable bowel syndrome-diarrhea: effects on bowel frequency and intestinal function. Gastroenterology. 2013;144:903–911.e3. doi: 10.1053/j.gastro.2013.01.049.
    1. Gutiérrez S, Pérez-Andrés J, Martínez-Blanco H, Ferrero MA, Vaquero L, Vivas S, et al. The human digestive tract has proteases capable of gluten hydrolysis. Mol Metab. 2017;6:693–702. doi: 10.1016/j.molmet.2017.05.008.
    1. 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;10:1708. doi: 10.3390/nu10111708.
    1. Rudzki L, Pawlak D, Pawlak K, Waszkiewicz N, Małus A, Konarzewska B, et al. Immune suppression of IgG response against dairy proteins in major depression. BMC Psychiatry. 2017;17:268. doi: 10.1186/s12888-017-1431-y.
    1. Lebwohl B, Cao Y, Zong G, Hu FB, Green PHR, Neugut AI, et al. Long term gluten consumption in adults without celiac disease and risk of coronary heart disease: prospective cohort study. BMJ. 2017;357:j1892. doi: 10.1136/bmj.j1892.
    1. Rivière A, Moens F, Selak M, Maes D, Weckx S, De Vuyst L. The ability of Bifidobacteria to degrade Arabinoxylan oligosaccharide constituents and derived oligosaccharides is strain dependent. Appl Environ Microbiol. 2014;80:204–217. doi: 10.1128/AEM.02853-13.
    1. Bordoni A, Danesi F, Dardevet D, Dupont D, Fernandez AS, Gille D, et al. Dairy products and inflammation: a review of the clinical evidence. Crit Rev Food Sci Nutr. 2017;57:2497–2525. doi: 10.1080/10408398.2014.967385.
    1. Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ. Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends Neurosci. 2016;39:763–781. doi: 10.1016/j.tins.2016.09.002.
    1. Messaoudi M, Violle N, Bisson J-F, Desor D, Javelot H, Rougeot C. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes. 2011;2:256–261. doi: 10.4161/gmic.2.4.16108.
    1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). Washington: American Psychiatric Pub; 2013.
    1. Pludowski P, Holick MF, Grant WB, Konstantynowicz J, Mascarenhas MR, Haq A, et al. Vitamin D supplementation guidelines. J Steroid Biochem Mol Biol. 2018;175:125–135. doi: 10.1016/j.jsbmb.2017.01.021.
    1. Urbaniak GC, Plous S. Research Randomizer (Version 4.0) 2013.
    1. Lidia Wądołowska. Cited 2019 Mar 18. Available from:
    1. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35:1381–1395. doi: 10.1249/01.MSS.0000078924.61453.FB.
    1. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382–389. doi: 10.1192/bjp.134.4.382.
    1. Beck AT. Depression: clinical, experimental, and theoretical aspects. Philadelphia: University of Pennsylvania Press; 1967.
    1. Derrogatis LR, Lipman RS, Covi I. The SCL-90: an outpatient psychiatric rating scale. Psychopharmacol Bull. 1973;9:13–28.
    1. Ware JE, Jr, Sherbourne CD. The MOS 36-item short-form health survey (SF-36): I. conceptual framework and item selection. Med Care. 1992;30:473–483. doi: 10.1097/00005650-199206000-00002.
    1. Svedlund J, Sjödin I, Dotevall G. GSRS—a clinical rating scale for gastrointestinal symptoms in patients with irritable bowel syndrome and peptic ulcer disease. Dig Dis Sci. 1988;33:129–134. doi: 10.1007/BF01535722.
    1. Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24:385–396. doi: 10.2307/2136404.
    1. Bernstein DP, Fink L. Childhood trauma questionnaire: a retrospective self-report: manual. Orlando: Psychological Corporation; 1998.
    1. Szponar L, Rychlik E, Wolnicka K. Album fotografii produktów i potraw: album of photographs of food products and dishes. Warszawa: Instytut Żywności i Żywienia; 2008.
    1. Baza produktów spożywczych i zestaw narzędzi przydatnych przy gotowaniu i dietach. Cited 2019 Mar 18. Available from:
    1. Hopman EG, Pruijn R, Tabben EH, le Cessie S, Mearin ML. Food questionnaire for the assessment of gluten intake by children 1 to 4 years old. J Pediatr Gastroenterol Nutr. 2012;54:791–796. doi: 10.1097/MPG.0b013e31825144fe.
    1. Jamnik J, García-Bailo B, Borchers CH, El-Sohemy A. Gluten intake is positively associated with plasma α2-macroglobulin in young adults–3. J Nutr. 2015;145:1256–1262. doi: 10.3945/jn.115.212829.
    1. Queipo-Ortuño MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One. 2013;8:e65465. doi: 10.1371/journal.pone.0065465.
    1. Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr. 2016;13:43. doi: 10.1186/s12970-016-0155-6.
    1. Kasapis C, Thompson PD. The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol. 2005;45:1563–1569. doi: 10.1016/j.jacc.2004.12.077.
    1. Clarke SF, Murphy EF, O’Sullivan O, Lucey AJ, Humphreys M, Hogan A, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63:1913–1920. doi: 10.1136/gutjnl-2013-306541.
    1. Xiao R, Wu BG, Goldklang M, McClelland M, Segal LN, D’Armiento JM. Cigarette smoke dysregulates gut microbiome in multiple strains of mice correlating with inflammation in the lung. A13 role of dysbiosis in lung disease. Am Thorac Soc. 2017;195:A1006.
    1. Tibuakuu M, Kamimura D, Kianoush S, DeFilippis AP, Al Rifai M, Reynolds LM, et al. The association between cigarette smoking and inflammation: the genetic epidemiology network of Arteriopathy (GENOA) study. PLoS One. 2017;12:e0184914. doi: 10.1371/journal.pone.0184914.
    1. World Health Organization . Waist circumference and waist-hip ratio: report of a WHO expert consultation, Geneva, 8–11 December 2008. 2011.
    1. Aye IL, Lager S, Ramirez VI, Gaccioli F, Dudley DJ, Jansson T, et al. Increasing maternal body mass index is associated with systemic inflammation in the mother and the activation of distinct placental inflammatory pathways. Biol Reprod. 2014;90:129. doi: 10.1095/biolreprod.113.116186.
    1. Guardiola M, Solà R, Vallvé JC, Girona J, Godàs G, Heras M, et al. Body mass index correlates with atherogenic lipoprotein profile even in nonobese, normoglycemic, and normolipidemic healthy men. J Clin Lipidol. 2015;9:824–831.e1. doi: 10.1016/j.jacl.2015.08.001.
    1. Yang XY, Shao MJ, Zhou Q, Xia Y, Zou HQ. Association of waist-to-hip ratio with insulin resistance in non-diabetic normal-weight individuals: a cross-sectional study. Nan Fang Yi Ke Da Xue Xue Bao. 2017;37:1540–1544.
    1. Park S, Bae JH. Probiotics for weight loss: a systematic review and meta-analysis. Nutr Res. 2015;35:566–575. doi: 10.1016/j.nutres.2015.05.008.
    1. Jasper HH. The ten-twenty electrode system of the international federation. Electroencephalogr Clin Neurophysiol. 1958;10:370–375. doi: 10.1016/0013-4694(58)90053-1.
    1. Seeck M, Koessler L, Bast T, Leijten F, Michel C, Baumgartner C, et al. The standardized EEG electrode array of the IFCN. Clin Neurophysiol. 2017;128:2070–2077. doi: 10.1016/j.clinph.2017.06.254.
    1. Stam CJ, Nolte G, Daffertshofer A. Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum Brain Mapp. 2007;28:1178–1193. doi: 10.1002/hbm.20346.
    1. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186. doi: 10.1038/nrn2575.
    1. Tewarie P, van Dellen E, Hillebrand A, Stam CJ. The minimum spanning tree: an unbiased method for brain network analysis. Neuroimage. 2015;104:177–188. doi: 10.1016/j.neuroimage.2014.10.015.
    1. Lee T-W, Wu Y-T, Yu YWY, Chen M-C, Chen T-J. The implication of functional connectivity strength in predicting treatment response of major depressive disorder: a resting EEG study. Psychiatry Res Neuroimaging. 2011;194:372–377. doi: 10.1016/j.pscychresns.2011.02.009.
    1. Olbrich S, Arns M. EEG biomarkers in major depressive disorder: discriminative power and prediction of treatment response. Int Rev Psychiatry. 2013;25:604–618. doi: 10.3109/09540261.2013.816269.
    1. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–7541. doi: 10.1128/AEM.01541-09.
    1. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–D596. doi: 10.1093/nar/gks1219.
    1. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814. doi: 10.1038/nbt.2676.
    1. What is Physiological Measurement? Cited 2019 Mar 18. Available from
    1. Food and Drug A . Guidance for industry: E9 statistical principles for clinical trials. Rockville: Food and Drug Administration; 1998.
    1. The Comprehensive R Archive Network. Cited 2019 Mar 18. Available from:
    1. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–3124. doi: 10.1093/bioinformatics/btu494.
    1. Slyepchenko A, Maes M, Jacka FN, Köhler CA, Barichello T, McIntyre RS, et al. Gut microbiota, bacterial translocation, and interactions with diet: pathophysiological links between major depressive disorder and non-communicable medical comorbidities. Psychother Psychosom. 2017;86:31–46. doi: 10.1159/000448957.
    1. Kazemi A, Noorbala AA, Azam K, Djafarian K. Effect of prebiotic and probiotic supplementation on circulating pro-inflammatory cytokines and urinary cortisol levels in patients with major depressive disorder: a double-blind, placebo-controlled randomized clinical trial. J Funct Foods. 2019;52:596–602. doi: 10.1016/j.jff.2018.11.041.
    1. Bonder MJ, Tigchelaar EF, Cai X, Trynka G, Cenit MC, Hrdlickova B, et al. The influence of a short-term gluten-free diet on the human gut microbiome. Genome Med. 2016;8:45. doi: 10.1186/s13073-016-0295-y.
    1. Mohan Mahesh, Chow Cheryl-Emiliane, Ryan Caitlin, Chan Luisa, Dufour Jason, Aye Pyone, Blanchard James, Moehs Charles, Sestak Karol. Dietary Gluten-Induced Gut Dysbiosis Is Accompanied by Selective Upregulation of microRNAs with Intestinal Tight Junction and Bacteria-Binding Motifs in Rhesus Macaque Model of Celiac Disease. Nutrients. 2016;8(11):684. doi: 10.3390/nu8110684.
    1. Phromraksa P, Nagano H, Boonmars T, Kamboonruang C. Identification of proteolytic bacteria from thai traditional fermented foods and their allergenic reducing potentials. J Food Sci. 2008;73:M189–M195. doi: 10.1111/j.1750-3841.2008.00721.x.
    1. Caminero Alberto, Nistal Esther, Herrán Alexandra R., Pérez-Andrés Jenifer, Vaquero Luis, Vivas Santiago, Ruíz de Morales José María, Casqueiro Javier. Wheat and Rice in Disease Prevention and Health. 2014. Gluten Metabolism in Humans; pp. 157–170.
    1. Caminero A, Meisel M, Jabri B, Verdu EF. Mechanisms by which gut microorganisms influence food sensitivities. Nat Rev Gastroenterol Hepatol. 2019;16:7–18. doi: 10.1038/s41575-018-0064-z.
    1. Verdu EF, Galipeau HJ, Jabri B. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat Rev Gastroenterol Hepatol. 2015;12:497–506. doi: 10.1038/nrgastro.2015.90.
    1. Garcia-Mazcorro Jose, Rivera-Gutierrez Xaira, Cobos-Quevedo Orestes, Grube-Pagola Peter, Meixueiro-Daza Arturo, Hernandez-Flores Karina, Cabrera-Jorge Francisco, Vivanco-Cid Hector, Dowd Scot, Remes-Troche Jose. First Insights into the Gut Microbiota of Mexican Patients with Celiac Disease and Non-Celiac Gluten Sensitivity. Nutrients. 2018;10(11):1641. doi: 10.3390/nu10111641.
    1. Sturgeon C, Fasano A. Zonulin, a regulator of epithelial and endothelial barrier functions, and its involvement in chronic inflammatory diseases. Tissue barriers. 2016;4:e1251384. doi: 10.1080/21688370.2016.1251384.

Source: PubMed

3
Sottoscrivi