Considering Intestinal Hyperpermeability and Immune-Inflammatory Metabolism in the Treatment of Food Allergy
##plugins.themes.bootstrap3.article.main##
Food Allergy is a chronic systemic immuno-inflammatory condition that depends on several factors, but, above all, the gastrointestinal epithelial barrier. The rupture of this intestinal barrier results in a deleterious increase in intestinal permeability allowing the paracellular permeation of molecules greater than 150 Da into the bloodstream, producing an equivalent immune response, decreasing the immune tolerance. Intestinal Hyperpermeability has been linked not only to food allergy but also to Metabolic Syndrome and Non-Alcoholic Fat Liver Disease. Here we review the factors that contribute to producing Intestinal Hyperpermeability, as well the factors that contribute to the restoration of the epithelial barrier, improving the clinical outcome of food-allergic patients. The main factors that increase the Intestinal Hyperpermeability are A) Immune-Inflammatory (food allergy itself and autoimmune conditions); B) Iatrogenic (steroids, non-steroidal anti-inflammatories, antacids, antibiotics, and gastric-bypass surgeries); C) Infectious (rotavirus, HIV, SARS-CO2, Helicobacter pylori, Candida albicans, etc.); and D) Lifestyle-related (alcoholic beverages, food addiction, food overconsumption, consumption of industrialized food with high-fructose content and emulsifiers). The main factors that restore the intestinal barrier and immune tolerances are the intestinal microbiota and functional nutrients such as Vitamin A and vegetal fibers. Mucoprotectants agents, such as gelatin tannate and xyloglucan, are in study to become part of the medical arsenal to treat Intestinal Hyperpermeability conditions.
References
-
Olivier CE. Food Allergy. J Allergy Ther. 2013; S3: 004:1-7.
Google Scholar
1
-
Kiela PR, Ghishan FK. Physiology of Intestinal Absorption and Secretion. Best Pract Res Clin Gastroenterol. 2016; 30(2): 145-59.
Google Scholar
2
-
Sensoy I. A review on the food digestion in the digestive tract and the used in vitro models. Curr Res Food Sci. 2021; 4: 308-19.
Google Scholar
3
-
Boland M. Human digestion – a processing perspective. J Sci Food Agric. 2016; 96(7): 2275-83.
Google Scholar
4
-
Brône B, Eggermont J. PDZ proteins retain and regulate membrane transporters in polarized epithelial cell membranes. Am J Physiol Cell Physiol. 2005; 288(1): C20-9.
Google Scholar
5
-
Shitara Y, Maeda K, Ikejiri K, Yoshida K, Horie T, Sugiyama Y. Clinical significance of organic anion transporting polypeptides (OATPs) in drug disposition: their roles in hepatic clearance and intestinal absorption. Biopharm Drug Dispos. 2013; 34(1): 45-78.
Google Scholar
6
-
Yu J, Zhou Z, Tay-Sontheimer J, Levy RH, Ragueneau-Majlessi I. Intestinal Drug Interactions Mediated by OATPs: A Systematic Review of Preclinical and Clinical Findings. J Pharm Sci. 2017; 106(9): 2312-25.
Google Scholar
7
-
Imanaga J, Kotegawa T, Imai H, Tsutsumi K, Yoshizato T, Ohyama T, et al. The effects of the SLCO2B1 c.1457C>T polymorphism and apple juice on the pharmacokinetics of fexofenadine and midazolam in humans. Pharmacogen Genom. 2011; 21(2).
Google Scholar
8
-
Dresser GK, Bailey DG, Leake BF, Schwarz UI, Dawson PA, Freeman DJ, et al. Fruit juices inhibit organic anion transporting polypeptide–mediated drug uptake to decrease the oral availability of fexofenadine. Clin Pharmacol Ther. 2002; 71(1): 11-20.
Google Scholar
9
-
Mougey EB, Lang JE, Wen X, Lima JJ. Effect of Citrus Juice and SLCO2B1 Genotype on the Pharmacokinetics of Montelukast. J Clin Pharmacol. 2011; 51(5): 751-60.
Google Scholar
10
-
Luo J, Imai H, Ohyama T, Hashimoto S, Hasunuma T, Inoue Y, et al. The Pharmacokinetic Exposure to Fexofenadine is Volume-Dependently Reduced in Healthy Subjects Following Oral Administration With Apple Juice. Clin Trans Sci. 2016; 9(4): 201-6.
Google Scholar
11
-
Bjarnason I, MacPherson A, Hollander D. Intestinal permeability: an overview. Gastroenterol. 1995; 108(5): 1566-81.
Google Scholar
12
-
Khoshbin K, Camilleri M. Effects of dietary components on intestinal permeability in health and disease. Am J Physiol Gastrointest Liver Physiol. 2020; 319(5): G589-g608.
Google Scholar
13
-
Camilleri M, Lyle BJ, Madsen KL, Sonnenburg J, Verbeke K, Wu GD. Role for diet in normal gut barrier function: developing guidance within the framework of food-labeling regulations. Am J Physiol Gastrointest Liver Physiol. 2019; 317(1): G17-G39.
Google Scholar
14
-
Chassaing B, Raja SM, Lewis JD, Srinivasan S, Gewirtz AT. Colonic Microbiota Encroachment Correlates With Dysglycemia in Humans. Cel Mol Gastroenterol Hepatol. 2017; 4(2): 205-21.
Google Scholar
15
-
Corthësy B. Secretory immunoglobulin A: well beyond immune exclusion at mucosal surfaces. Immunopharmacol Immunotoxicol. 2009; 31(2): 174-9.
Google Scholar
16
-
Frossard CP, Hauser C, Eigenmann PA. Antigen-specific secretory IgA antibodies in the gut are decreased in a mouse model of food allergy. J Allergy Clin Immunol. 2004; 114(2): 377-82.
Google Scholar
17
-
Cunningham-Rundles C, Brandeis WE, Good RA, Day NK. Milk precipitins, circulating immune complexes, and IgA deficiency. Proc Nat Acad Sci U S A. 1978; 75(7): 3387-9.
Google Scholar
18
-
Samadi N, Klems M, Untersmayr E. The role of gastrointestinal permeability in food allergy. Ann Allergy Asthma Immunol. 2018; 121(2): 168-73.
Google Scholar
19
-
Johansson MEV, Hansson GC. Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol. 2016;16(10):639-49.
Google Scholar
20
-
Shan M, Gentile M, Yeiser John R, Walland AC, Bornstein Victor U, Chen K, et al. Mucus Enhances Gut Homeostasis and Oral Tolerance by Delivering Immunoregulatory Signals. Science. 2013; 342(6157): 447-53.
Google Scholar
21
-
Bernard C. [Internet] Lessons of Experimental Physiology Applied to Medicine Available from: http://books.google.com/books?id=tgIAAAAAQAAJ&printsec=frontcover&hl=pt-BR&source=gbs_similarbooks_r&cad=2_2#PPR3,M1. First ed. Paris: Bailliere; 1855. 510 p.
Google Scholar
22
-
Travis S, Menzies I. Intestinal permeability: functional assessment and significance. Clin Sci. 1992; 82(5): 471-88.
Google Scholar
23
-
Asha M, Govind KM, lt, sup, gt, lt, et al. Techniques of Functional and Motility Test: How to Perform and Interpret Intestinal Permeability. J Neurogastroenterol Motil. 2012; 18(4): 443-7.
Google Scholar
24
-
Camilleri M. Leaky gut: mechanisms, measurement and clinical implications in humans. Gut. 2019;6 8(8): 1516-26.
Google Scholar
25
-
Binienda A, Twardowska A, Makaro A, Salaga M. Dietary Carbohydrates and Lipids in the Pathogenesis of Leaky Gut Syndrome: An Overview. Int J Mol Sci. 2020; 21(21): 8368.
Google Scholar
26
-
Moreno FJ. Gastrointestinal digestion of food allergens: Effect on their allergenicity. Biomed Pharmacother. 2007; 61(1): 50-60.
Google Scholar
27
-
Gocki J, Bartuzi Z. Role of immunoglobulin G antibodies in diagnosis of food allergy. Postepy dermatologii i alergologii. 2016; 33(4): 253-6.
Google Scholar
28
-
Saba TM. Physiology and Physiopathology of the Reticuloendothelial System. Arch Intern Med. 1970; 126(6): 1031-52.
Google Scholar
29
-
Lefvert AK. Recurrent angioedema caused by circulating immune complexes containing antibodies against bovine proteins. Int Arch Allergy Immunol. 1993; 102(1): 112-6.
Google Scholar
30
-
Gell PGH, Harington CR, Rivers RP. The antigenic function of simple chemical compounds; production of precipitins in rabbits. Br J Exp Pathol. 1946; 27(5): 267-86.
Google Scholar
31
-
Ishizaka K, Ishizaka T, Campbell DH. The biological activity of soluble antigen-antibody complexes. J Exp Med. 1959; 109(2): 127-43.
Google Scholar
32
-
Wells HG. Studies on the chemistry of anaphylaxis (III). Experiments with isolated proteins, especially those of the hen's egg. J Inf Dis. 1911; 9: 147-71.
Google Scholar
33
-
Olivier CE, Pinto DG, Lima RPdS, Teixeira APM, Santana JLS. Self-imposed food restriction and oral food challenges are correlated with precipitin's accuracy in the diagnosis of non-IgE-mediated food-related adulthood acute episodes of urticaria. J Allergy Ther. 2021; 12(8): 1-8.
Google Scholar
34
-
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. Intrinsic Atopic Dermatitis: Titration of Precipitins in the Screening of Food Allergens for Prescription of Elimination Diets and Desensitization Strategies. Eur J Clin Med. 2021; 2(6): 1-9.
Google Scholar
35
-
Tran CD, Grice DM, Wade B, Kerr CA, Bauer DC, Li D, et al. Gut permeability, its interaction with gut microflora and effects on metabolic health are mediated by the lymphatics system, liver and bile acid. Future Microbiol. 2015; 10(8): 1339-53.
Google Scholar
36
-
Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatol. 2009; 49(6): 1877-87.
Google Scholar
37
-
Goretzki A, Lin Y-J, Schülke S. Immune metabolism in allergies, does it matter?—A review of immune metabolic basics and adaptations associated with the activation of innate immune cells in allergy. Allergy. 2021; 76(11): 3314-31.
Google Scholar
38
-
Nakagawa T, Lanaspa MA, Millan IS, Fini M, Rivard CJ, Sanchez-Lozada LG, et al. Fructose contributes to the Warburg effect for cancer growth. Cancer Metab. 2020; 8(1): 16.
Google Scholar
39
-
Warburg O. On the origin of cancer cells. Science. 1956; 123(3191): 309-14.
Google Scholar
40
-
Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature. 2017; 542(7640): 177-85.
Google Scholar
41
-
Kuryłowicz A, Koźniewski K. Anti-Inflammatory Strategies Targeting Metaflammation in Type 2 Diabetes. Molecules (Basel, Switzerland). 2020; 25(9): 2224.
Google Scholar
42
-
Perrier C, Corthésy B. Gut permeability and food allergies. Clin Exp Allergy. 2011; 41(1): 20-8.
Google Scholar
43
-
Grozdanovic MM, Čavić M, Nešić A, Andjelković U, Akbari P, Smit JJ, et al. Kiwifruit cysteine protease actinidin compromises the intestinal barrier by disrupting tight junctions. Biochim Biophys Acta. 2016; 1860(3): 516-26.
Google Scholar
44
-
Lee SHJIr. Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res. 2015; 13(1): 11.
Google Scholar
45
-
Hollander D, Vadheim CM, Brettholz E, Petersen GM, Delahunty T, Rotter JI. Increased Intestinal Permeability in Patients with Crohn's Disease and Their Relatives. Ann Int Med. 1986; 105(6): 883-5.
Google Scholar
46
-
Dunlop SP, Hebden J, Campbell E, Naesdal J, Olbe L, Perkins AC, et al. Abnormal Intestinal Permeability in Subgroups of Diarrhea-Predominant Irritable Bowel Syndromes. Am J Gastroenterol. 2006; 101(6): 1288-94.
Google Scholar
47
-
Bjarnason I, Hayllar J, MacPherson AJ, Russell AS. Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterol. 1993; 104(6): 1832-47.
Google Scholar
48
-
Olivier CE, Santos RAPG, Argentão DGP, MD S, RPS L. Food-dependent drug-induced angioedema: a case report. J Allergy Immunol. 2017.
Google Scholar
49
-
Sánchez-López J, Araujo G, Cardona V, García-Moral A, Casas-Saucedo R, Guilarte M, et al. Food-dependent NSAID-induced hypersensitivity (FDNIH) reactions: Unraveling the clinical features and risk factors. Allergy. 2020: 14689.
Google Scholar
50
-
Taylor SL, Gendel SM, Houben GF, Julien E. The Key Events Dose-Response Framework: a foundation for examining variability in elicitation thresholds for food allergens. Crit Rev Food Sci Nutr. 2009; 49(8): 729-39.
Google Scholar
51
-
Izumi K, Aihara M, Ikezawa Z. [Effects of non steroidal antiinflammatory drugs (NSAIDs) on immediate-type food allergy analysis of Japanese cases from 1998 to 2009]. Arerugi. 2009; 58(12): 1629-39.
Google Scholar
52
-
Untersmayr E, Scholl I, Swoboda I, Beil WJ, Forster-Waldl E, Walter F, et al. Antacid medication inhibits digestion of dietary proteins and causes food allergy: a fish allergy model in BALB/c mice. J Allergy Clin Immunol. 2003; 112(3): 616-23.
Google Scholar
53
-
Untersmayr E, Jensen-Jarolim E. The role of protein digestibility and antacids on food allergy outcomes. J Allergy Clin Immunol. 2008; 121(6): 1301-8; quiz 9-10.
Google Scholar
54
-
Untersmayr E, Bakos N, Schöll I, Kundi M, Roth-Walter F, Szalai K, et al. Anti-ulcer drugs promote IgE formation toward dietary antigens in adult patients. FASEB J. 2005; 19(6): 1-16.
Google Scholar
55
-
DeMuth K, Stecenko A, Sullivan K, Fitzpatrick A. Relationship between treatment with antacid medication and the prevalence of food allergy in children. Allergy Asthma Proc. 2013; 34(3): 227-32.
Google Scholar
56
-
Black HE. The effects of steroids upon the gastrointestinal tract. Toxicol Pathol. 1988 ;16(2): 213-22.
Google Scholar
57
-
Gaudier E, Jarry A, Blottière HM, de Coppet P, Buisine MP, Aubert JP, et al. Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol. 2004; 287(6): G1168-74.
Google Scholar
58
-
Blaser M. Antibiotic overuse: Stop the killing of beneficial bacteria. Nature. 2011; 476(7361): 393-4.
Google Scholar
59
-
Bai J, Moran C, Martinez C, Niveloni S, Crosetti E, Sambuelli A, et al. Celiac Sprue After Surgery of the Upper Gastrointestinal Tract. Report of 10 Patients with Special Attention to Diagnosis, Clinical Behavior, and Follow-up. J Clin Gastroenterol. 1991; 13(5).
Google Scholar
60
-
Kamau J, Kearny S, Jaworek A, Snyder R, Chaar ME. Anaphylactic Food Allergy After Roux-en-Y Gastric Bypass. Cureus. 2021; 9(13).
Google Scholar
61
-
Jalonen T, Isolauri E, Heyman M, Crain-Denoyelle AM, Sillanaukee P, Koivula T. Increased beta-lactoglobulin absorption during rotavirus enteritis in infants: relationship to sugar permeability. Pediatr Res. 1991; 30(3): 290-3.
Google Scholar
62
-
Giron LB, Dweep H, Yin X, Wang H, Damra M, Goldman AR, et al. Plasma Markers of Disrupted Gut Permeability in Severe COVID-19 Patients. Front Immunol. 2021; 12.
Google Scholar
63
-
Hensley-McBain T, Berard AR, Manuzak JA, Miller CJ, Zevin AS, Polacino P, et al. Intestinal damage precedes mucosal immune dysfunction in SIV infection. Mucosal Immunol. 2018; 11(5): 1429-40.
Google Scholar
64
-
Corrado G, Luzzi I, Lucarelli S, Frediani T, Pacchiarotti C, Cavaliere M, et al. Positive Association between Helicobacter pylori Infection and Food Allergy in Children. Scand J Gastroenterol. 1998; 33(11): 1135-9.
Google Scholar
65
-
Vera JF, Gotteland M, Chavez E, Vial MT, Kakarieka E, Brunser O. Sucrose Permeability in Children with Gastric Damage and Helicobacter pylori Infection. J Pediatr Gastroenterol Nutr. 1997; 24(5): 506-11.
Google Scholar
66
-
Kim JM, Eckmann L, Savidge TC, Lowe DC, Witthöft T, Kagnoff MF. Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Invest. 1998; 102(10): 1815-23.
Google Scholar
67
-
Allert S, Förster TM, Svensson CM, Richardson JP, Pawlik T, Hebecker B, et al. Candida albicans-Induced Epithelial Damage Mediates Translocation through Intestinal Barriers. mBio. 2018; 9(3).
Google Scholar
68
-
de Moraes RCS, Sawaya AL, Vieira ACA, Pereira JKG, de Brito Alves JL, de Luna Freire MO, et al. Food addiction symptoms and metabolic changes in children and adolescents with the double burden of malnutrition. Br J Nutr. 2021; 126(12): 1911-8.
Google Scholar
69
-
Blumenthal DM, Gold MS. Neurobiology of food addiction. Curr Opin Clin Nutr Metab Care. 2010; 13(4).
Google Scholar
70
-
Mattson MP. An Evolutionary Perspective on Why Food Overconsumption Impairs Cognition. Trends in Cogn Sci. 2019; 23(3): 200-12.
Google Scholar
71
-
Spruss A, Bergheim I. Dietary fructose and intestinal barrier: potential risk factor in the pathogenesis of nonalcoholic fatty liver disease. J Nutr Biochem. 2009; 20(9): 657-62.
Google Scholar
72
-
Bergheim I, Weber S, Vos M, Krämer S, Volynets V, Kaserouni S, et al. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol. 2008; 48(6): 983-92.
Google Scholar
73
-
Mock K, Lateef S, Benedito VA, Tou JC. High-fructose corn syrup-55 consumption alters hepatic lipid metabolism and promotes triglyceride accumulation. J Nutr Bioch. 2017; 39: 32-9.
Google Scholar
74
-
Spruss A, Kanuri G, Stahl C, Bischoff SC, Bergheim I. Metformin protects against the development of fructose-induced steatosis in mice: role of the intestinal barrier function. Lab Invest. 2012; 92(7): 1020-32.
Google Scholar
75
-
Parrish A, Boudaud M, Kuehn A, Ollert M, Desai MS. Intestinal mucus barrier: a missing piece of the puzzle in food allergy. Trends Mol Med. 2022; 28(1): 36-50.
Google Scholar
76
-
Csáki KF. Synthetic surfactant food additives can cause intestinal barrier dysfunction. Med Hypotheses. 2011; 76(5): 676-81.
Google Scholar
77
-
Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature. 2015; 519(7541): 92-6.
Google Scholar
78
-
Draper LR, Gyure LA, Hall JG, Robertson D. Effect of alcohol on the integrity of the intestinal epithelium. Gut. 1983; 24(5): 399-404.
Google Scholar
79
-
Bode C, Bode JC. Effect of alcohol consumption on the gut. Best Pract Res Clin Gastroenterol. 2003; 17(4): 575-92.
Google Scholar
80
-
Wieser H. Chemistry of gluten proteins. Food Microbiol. 2007; 24(2): 115-9.
Google Scholar
81
-
Asri N, Rostami-Nejad M. Chapter 4 - Gluten-related disorders definition. In: Rostami-Nejad M, editor. Gluten-Related Disorders: Academic Press; 2022: 49-57.
Google Scholar
82
-
Menta PLR, Andrade MER, Leocádio PCL, Fraga JR, Dias MTS, Cara DC, et al. Wheat gluten intake increases the severity of experimental colitis and bacterial translocation by weakening of the proteins of the junctional complex. Br J Nutr. 2019; 121(4): 361-73.
Google Scholar
83
-
Sanz Y. Microbiome and Gluten. Ann Nutr Metab. 2015; 67(suppl 2)(Suppl. 2): 27-42.
Google Scholar
84
-
Young VB. The intestinal microbiota in health and disease. Curr Opin Gastroenterol. 2012; 28(1): 63-9.
Google Scholar
85
-
Pushpanathan P, Mathew GS, Selvarajan S, Seshadri KG, Srikanth P. Gut microbiota and its mysteries. Indian J Med Microbiol. 2019; 37(2): 268-77.
Google Scholar
86
-
Stefka AT, Feehley T, Tripathi P, Qiu J, McCoy K, Mazmanian SK, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A. 2014; 111(36): 13145-50.
Google Scholar
87
-
Huang R, Ning H, Shen M, Li J, Zhang J, Chen X. Probiotics for the Treatment of Atopic Dermatitis in Children: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Front Cell Infect Microbiol. 2017; 7: 392-.
Google Scholar
88
-
Rosenfeldt V, Benfeldt E, Valerius NH, Paerregaard A, Michaelsen KF. Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr. 2004; 145(5): 612-6.
Google Scholar
89
-
Mennini M, Arasi S, Artesani MC, Fiocchi AG. Probiotics in food allergy. Curr Opin Allergy Clin Immunol. 2021; 21(3): 309-16.
Google Scholar
90
-
Rijnierse A, Jeurink PV, van Esch BC, Garssen J, Knippels LM. Food-derived oligosaccharides exhibit pharmaceutical properties. Eur J Pharmacol. 2011; 668 Suppl 1: S117-23.
Google Scholar
91
-
Rapin JR, Wiernsperger N. Possible links between intestinal permeability and food processing: A potential therapeutic niche for glutamine. Clinics (Sao Paulo). 2010; 65(6): 635-43.
Google Scholar
92
-
De-Souza DA, Greene LJ. Intestinal permeability and systemic infections in critically ill patients: effect of glutamine. Crit Care Med. 2005; 33(5): 1125-35.
Google Scholar
93
-
Lima AA, Brito LF, Ribeiro HB, Martins MC, Lustosa AP, Rocha EM, et al. Intestinal barrier function and weight gain in malnourished children taking glutamine supplemented enteral formula. J Pediatr Gastroenterol Nutr. 2005; 40(1): 28-35.
Google Scholar
94
-
Hond ED, Hiele M, Peeters M, Ghoos Y, Rutgeerts PJJoP, Nutrition E. Effect of long‐term oral glutamine supplements on small intestinal permeability in patients with Crohn's disease. JPEN J Parenter Enteral Nutr. 1999; 23(1): 7-11.
Google Scholar
95
-
Cruzat V, Macedo Rogero M, Noel Keane K, Curi R, Newsholme P. Glutamine: Metabolism and Immune Function, Supplementation and Clinical Translation. Nutrients. 2018; 10(11): 1564.
Google Scholar
96
-
Hufnagl K, Jensen-Jarolim E. Does a carrot a day keep the allergy away? Immunol Lett. 2019; 206: 54-8.
Google Scholar
97
-
Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, et al. Dietary Fiber and Bacterial SCFA Enhance Oral Tolerance and Protect against Food Allergy through Diverse Cellular Pathways. Cell Rep. 2016; 15(12): 2809-24.
Google Scholar
98
-
Eutamene H, Beaufrand C, Harkat C, Theodorou V. The role of mucoprotectants in the management of gastrointestinal disorders. Expert Rev Gastroenterol Hepatol. 2018; 12(1): 83-90.
Google Scholar
99
-
Akdis CA. The epithelial barrier hypothesis proposes a comprehensive understanding of the origins of allergic and other chronic noncommunicable diseases. J Allergy Clin Immunol 2022; 149(1): 41-4.
Google Scholar
100
Most read articles by the same author(s)
-
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana Paula M. Teixeira,
Jhéssica L. S. Santana,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Leukocyte Adherence Inhibition Test to the assessment of Immunoreactivity Against Cow’s Milk Proteins in Non—IgE-Mediated Gastrointestinal Food Allergy , European Journal of Clinical Medicine: Vol. 3 No. 2 (2022) -
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana P. M. Teixeira,
Jhéssica L. S. Santana,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Contribution of the Leukocyte Adherence Inhibition Test to the Evaluation of Cellular Immunoreactivity against Latex Extracts for Non—IgE-Mediated Latex-Fruit-Pollen Syndrome in Allergic Candidates to Exclusion Diets and Allergic Desensitization , European Journal of Clinical Medicine: Vol. 3 No. 1 (2022) -
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana P. M. Teixeira,
Jhéssica L. S. Santana,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Contribution of the Leukocyte Adherence Inhibition Test for the Evaluation of Immunoreactivity against Gluten Extracts in Non—IgE-Mediated / Non-Autoimmune Gluten-Related Disorders , European Journal of Clinical Medicine: Vol. 3 No. 2 (2022) -
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana P. M. Teixeira,
Jhéssica L. S. Santana ,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Everton S. Monteiro,
Evaluating Non-IgE-Mediated Allergens’ Immunoreactivity in Patients Formerly Classified as “Intrinsic” Asthmatics with Help of the Leukocyte Adherence Inhibition Test , European Journal of Clinical Medicine: Vol. 4 No. 2 (2023) -
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana P. M. Teixeira,
Jhéssica L. S. Santana,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Immunoreactivity against Dermatophagoides pteronyssinus Assessed by the Leukocyte Adherence Inhibition Test in Patients with Intrinsic Atopic Dermatitis and Correlated “Intrinsic” Non–IgE-mediated Allergic Conditions , European Journal of Clinical Medicine: Vol. 2 No. 6 (2021) -
Celso Eduardo Olivier,
Daiana G. Pinto,
Ana P. M. Teixeira,
Jhéssica L. S. Santana ,
Raquel A. P. G. Santos,
Regiane P. S. Lima,
Anti-Saccharomyces cerevisiae Antibodies (ASCA) Researched by Tube Precipitins are Elevated in Patients with Dermatologic and Gastrointestinal Non-Ige-Mediated Hypersensitivity , European Journal of Clinical Medicine: Vol. 4 No. 2 (2023) -
Celso Eduardo Olivier,
Daiana Guedes Pinto,
Regiane Patussi dos Santos Lima,
Mariana Dias da Silva,
Raquel Acácia Pereira Gonçalves dos Santos,
Ana Paula Monezzi Teixeira,
Patricia Ucelli Simioni,
Assessment of Immunoreactivity against Therapeutic Options Employing the Leukocyte Adherence Inhibition Test as a Tool for Precision Medicine , European Journal of Clinical Medicine: Vol. 2 No. 3 (2021)