Intestinal Barrier Permeability in Allergic Diseases
Abstract
:1. Introduction
2. Intestinal Barrier
2.1. Characteristics of the Intestinal Barrier Structure
2.2. Mucus Layer
2.3. Outer Mucus Layer
2.4. The Intestinal Microbiome
2.5. Inner Mucus Layer
2.6. Cells of the Blood, Lymphoid, Immune and Nervous Systems
3. Intestinal Epithelium and the Structure of Tight Junctions
4. Laboratory Diagnosis of the Intestinal Barrier Permeability Disorders
5. Allergic Diseases
6. Pathomechanisms of Atopic Diseases and the Intestinal Barrier
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Renz, H.; Holt, P.G.; Inouye, M.; Logan, A.C.; Prescott, S.L.; Sly, P.D. An exposome perspective: Early-life events and immune development in a changing world. J. Allergy Clin. Immunol. 2017, 140, 24–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Noverr, M.C.; Huffnagle, G.B. The ‘microflora hypothesis’ of allergic diseases. Clin. Exp. Allergy 2005, 35, 1511–1520. [Google Scholar] [CrossRef] [PubMed]
- Fasano, A.; Shea-Donohue, T. Mechanisms of disease: The role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pr. Gastroenterol. Hepatol. 2005, 2, 416–422. [Google Scholar] [CrossRef] [PubMed]
- Takiishi, T.; Fenero, C.I.M.; Câmara, N.O.S. Intestinal barrier and gut microbiota: Shaping our immune responses throughout life. Tissue Barriers 2017, 5, e1373208. [Google Scholar] [CrossRef] [PubMed]
- Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207–214. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mischke, M.; Plösch, T. The Gut Microbiota and their Metabolites: Potential Implications for the Host Epigenome. Adv. Exp. Med. Biol. 2016, 902, 33–44. [Google Scholar] [CrossRef]
- Krajewska-Włodarczyk, M. The gastrointestinal tract microbiom in connective tissue diseases. Prz. Lek. 2017, 74, 84–88. [Google Scholar]
- McGarr, S.E.; Ridlon, J.M.; Hylemon, P.B. Diet, anaerobic bacterial metabolism, and colon cancer: A review of the literature. J. Clin. Gastroenterol. 2005, 39, 98–109. [Google Scholar]
- Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022–1023. [Google Scholar] [CrossRef]
- Frank, D.N.; St Amand, A.L.; Feldman, R.A.; Boedeker, E.C.; Harpaz, N.; Pace, N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007, 104, 13780–13785. [Google Scholar] [CrossRef] [Green Version]
- Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971–11975. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collado, M.C.; Cernada, M.; Baüerl, C.; Vento, M.; Pérez-Martínez, G. Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes 2012, 3, 352–365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, R.; Makino, H.; Cetinyurek Yavuz, A.; Ben-Amor, K.; Roelofs, M.; Ishikawa, E.; Kubota, H.; Swinkels, S.; Sakai, T.; Oishi, K.; et al. Early-Life Events, Including Mode of Delivery and Type of Feeding, Siblings and Gender, Shape the Developing Gut Microbiota. PLoS ONE 2016, 11, e0158498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wlasiuk, G.; Vercelli, D. The farm effect, or: When, what and how a farming environment protects from asthma and allergic disease. Curr. Opin. Allergy Clin. Immunol. 2012, 12, 461–466. [Google Scholar] [CrossRef] [PubMed]
- Neuman, H.; Forsythe, P.; Uzan, A.; Avni, O.; Koren, O. Antibiotics in early life: Dysbiosis and the damage done. FEMS Microbiol. Rev. 2018, 42, 489–499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rogers, M.A.M.; Aronoff, D.M. The influence of non-steroidal anti-inflammatory drugs on the gut microbiome. Clin. Microbiol. Infect. 2016, 22, 178.e1–178.e9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weersma, R.K.; Zhernakova, A.; Fu, J. Interaction between drugs and the gut microbiome. Gut 2020, 69, 1510–1519. [Google Scholar] [CrossRef]
- Musilova, S.; Rada, V.; Vlkova, E.; Bunesova, V. Beneficial effects of human milk oligosaccharides on gut microbiota. Benef. Microbes 2014, 5, 273–283. [Google Scholar] [CrossRef]
- Fernández, L.; Langa, S.; Martín, V.; Jiménez, E.; Martín, R.; Rodríguez, J.M. The microbiota of human milk in healthy women. Cell. Mol. Biol. (Noisy-Le-Grand) 2013, 59, 31–42. [Google Scholar]
- Gómez-Gallego, C.; Morales, J.M.; Monleón, D.; du Toit, E.; Kumar, H.; Linderborg, K.M.; Zhang, Y.; Yang, B.; Isolauri, E.; Salminen, S.; et al. Human Breast Milk NMR Metabolomic Profile across Specific Geographical Locations and Its Association with the Milk Microbiota. Nutrients 2018, 10, 1355. [Google Scholar] [CrossRef] [Green Version]
- Knol, J.; Scholtens, P.; Kafka, C.; Steenbakkers, J.; Gro, S.; Helm, K.; Klarczyk, M.; Schöpfer, H.; Böckler, H.M.; Wells, J. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: More like breast-fed infants. J. Pediatr. Gastroenterol. Nutr. 2005, 40, 36–42. [Google Scholar] [CrossRef] [PubMed]
- Salvini, F.; Riva, E.; Salvatici, E.; Boehm, G.; Jelinek, J.; Banderali, G.; Giovannini, M. A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. J. Nutr. 2011, 141, 1335–1339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moro, G.; Arslanoglu, S.; Stahl, B.; Jelinek, J.; Wahn, U.; Boehm, G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch. Dis. Child. 2006, 91, 814–819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arslanoglu, S.; Moro, G.E.; Schmitt, J.; Tandoi, L.; Rizzardi, S.; Boehm, G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr. 2008, 138, 1091–1095. [Google Scholar] [CrossRef] [PubMed]
- Arslanoglu, S.; Moro, G.E.; Boehm, G.; Wienz, F.; Stahl, B.; Bertino, E. Early neutral prebiotic oligosaccharide supplementation reduces the incidence of some allergic manifestations in the first 5 years of life. J. Biol. Regul. Homeost. Agents 2012, 26 (Suppl. 3), 49–59. [Google Scholar]
- Kozakova, H.; Schwarzer, M.; Tuckova, L.; Srutkova, D.; Czarnowska, E.; Rosiak, I.; Hudcovic, T.; Schabussova, I.; Hermanova, P.; Zakostelska, Z. Colonization of germ-free mice with a mixture of three lactobacillus strains enhances the integrity of gut mucosa and ameliorates allergic sensitization. Cell. Mol. Immunol. 2016, 13, 251–262. [Google Scholar] [CrossRef]
- Tlaskalová-Hogenová, H.; Stepánková, R.; Hudcovic, T.; Tucková, L.; Cukrowska, B.; Lodinová-Zádníková, R.; Kozáková, H.; Rossmann, P.; Bártová, J.; Sokol, D.; et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol. Lett. 2004, 93, 97–108. [Google Scholar] [CrossRef]
- Purchiaroni, F.; Tortora, A.; Gabrielli, M.; Bertucci, F.; Gigante, G.; Ianiro, G.; Ojetti, V.; Scarpellini, E.; Gasbarrini, A. The role of intestinal microbiota and the immune system. Eur. Rev. Med. Pharm. Sci. 2013, 17, 323–333. [Google Scholar]
- Akdis, C.A.; Akdis, M. Mechanisms of immune tolerance to allergens: Role of IL-10 and Tregs. J. Clin. Investig. 2014, 124, 4678–4680. [Google Scholar] [CrossRef] [Green Version]
- Sjögren, Y.M.; Jenmalm, M.C.; Böttcher, M.F.; Björkstén, B.; Sverremark-Ekström, E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin. Exp. Allergy 2009, 39, 518–526. [Google Scholar] [CrossRef] [Green Version]
- Björkstén, B.; Naaber, P.; Sepp, E.; Mikelsaar, M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin. Exp. Allergy 1999, 29, 342–346. [Google Scholar] [CrossRef] [PubMed]
- Bisgaard, H.; Li, N.; Bonnelykke, K.; Chawes, B.L.; Skov, T.; Paludan-Müller, G.; Stokholm, J.; Smith, B.; Krogfelt, K.A. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Allergy Clin. Immunol. 2011, 128, 646–652.e1-5. [Google Scholar] [CrossRef] [PubMed]
- Kalliomäki, M.; Kirjavainen, P.; Eerola, E.; Kero, P.; Salminen, S.; Isolauri, E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 2001, 107, 129–134. [Google Scholar] [CrossRef]
- Turner, J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 2009, 9, 799–809. [Google Scholar] [CrossRef] [PubMed]
- Gill, N.; Wlodarska, M.; Finlay, B.B. Roadblocks in the gut: Barriers to enteric infection. Cell. Microbiol. 2011, 13, 660–669. [Google Scholar] [CrossRef]
- Pott, J.; Hornef, M. Innate immune signalling at the intestinal epithelium in homeostasis and disease. EMBO Rep. 2012, 13, 684–698. [Google Scholar] [CrossRef] [Green Version]
- Lee, S.H. Intestinal permeability regulation by tight junction: Implication on inflammatory bowel diseases. Intest. Res. 2015, 13, 11–18. [Google Scholar] [CrossRef] [Green Version]
- Higashi, T.; Tokuda, S.; Kitajiri, S.; Masuda, S.; Nakamura, H.; Oda, Y.; Furuse, M. Analysis of the ‘angulin’ proteins LSR, ILDR1 and ILDR2--tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J. Cell Sci. 2013, 126 Pt 4, 966–977. [Google Scholar] [CrossRef] [Green Version]
- Umeda, K.; Matsui, T.; Nakayama, M.; Furuse, K.; Sasaki, H.; Furuse, M.; Tsukita, S. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. J. Biol. Chem. 2004, 279, 44785–44794. [Google Scholar] [CrossRef] [Green Version]
- Sicherer, S.H.; Sampson, H.A. Food allergy: Epidemiology, pathogenesis, diagnosis, and treatment. J. Allergy Clin. Immunol. 2014, 133, 291–308. [Google Scholar] [CrossRef]
- Shen, L.; Black, E.D.; Witkowski, E.D.; Lencer, W.I.; Guerriero, V.; Schneeberger, E.E.; Turner, J.R. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J. Cell Sci. 2006, 119 Pt 10, 2095–2106. [Google Scholar] [CrossRef] [Green Version]
- Bruewer, M.; Utech, M.; Ivanov, A.I.; Hopkins, A.M.; Parkos, C.A.; Nusrat, A. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J. 2005, 19, 923–933. [Google Scholar] [CrossRef] [PubMed]
- Cario, E.; Gerken, G.; Podolsky, D.K. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 2004, 127, 224–238. [Google Scholar] [CrossRef] [PubMed]
- Darmoul, D.; Marie, J.C.; Devaud, H.; Gratio, V.; Laburthe, M. Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2. Br. J. Cancer 2001, 85, 772–779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeissig, S.; Bürgel, N.; Günzel, D.; Richter, J.; Mankertz, J.; Wahnschaffe, U.; Kroesen, A.J.; Zeitz, M.; Fromm, M.; Schulzke, J.D. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn’s disease. Gut 2007, 56, 61–72. [Google Scholar] [CrossRef]
- Sander, G.R.; Cummins, A.G.; Henshall, T.; Powell, B.C. Rapid disruption of intestinal barrier function by gliadin involves altered expression of apical junctional proteins. FEBS Lett. 2005, 579, 4851–4855. [Google Scholar] [CrossRef]
- Al-Sadi, R.; Khatib, K.; Guo, S.; Ye, D.; Youssef, M.; Ma, T. Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300, G1054–G1064. [Google Scholar] [CrossRef] [Green Version]
- Rao, R. Occludin phosphorylation in regulation of epithelial tight junctions. Ann. N. Y. Acad. Sci. 2009, 1165, 62–68. [Google Scholar] [CrossRef]
- Martínez, C.; Lobo, B.; Pigrau, M.; Ramos, L.; González-Castro, A.M.; Alonso, C.; Guilarte, M.; Guilá, M.; de Torres, I.; Azpiroz, F.; et al. Diarrhoea-predominant irritable bowel syndrome: An organic disorder with structural abnormalities in the jejunal epithelial barrier. Gut 2013, 62, 1160–1168. [Google Scholar] [CrossRef]
- Granito, A.; Zauli, D.; Muratori, P.; Muratori, L.; Grassi, A.; Bortolotti, R.; Petrolini, N.; Veronesi, L.; Gionchetti, P.; Bianchi, F.B.; et al. Anti-Saccharomyces cerevisiae and perinuclear anti-neutrophil cytoplasmic antibodies in coeliac disease before and after gluten-free diet. Aliment. Pharm. Ther. 2005, 21, 881–887. [Google Scholar] [CrossRef]
- Wyatt, J.; Vogelsang, H.; Hübl, W.; Waldhöer, T.; Lochs, H. Intestinal permeability and the prediction of relapse in Crohn’s disease. Lancet 1993, 341, 1437–1439. [Google Scholar] [CrossRef]
- Järvinen, K.M.; Konstantinou, G.N.; Pilapil, M.; Arrieta, M.C.; Noone, S.; Sampson, H.A.; Meddings, J.; Nowak-Węgrzyn, A. Intestinal permeability in children with food allergy on specific elimination diets. Pediatr. Allergy Immunol. 2013, 24, 589–595. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laudat, A.; Arnaud, P.; Napoly, A.; Brion, F. The intestinal permeability test applied to the diagnosis of food allergy in paediatrics. West. Indian Med. J. 1994, 43, 87–88. [Google Scholar] [PubMed]
- Ventura, M.T.; Polimeno, L.; Amoruso, A.C.; Gatti, F.; Annoscia, E.; Marinaro, M.; Di Leo, E.; Matino, M.G.; Buquicchio, R.; Bonini, S. Intestinal permeability in patients with adverse reactions to food. Dig. Liver Dis. 2006, 38, 732–736. [Google Scholar] [CrossRef] [PubMed]
- Denno, D.M.; VanBuskirk, K.; Nelson, Z.C.; Musser, C.A.; Burgess, D.C.H.; Tarr, P.I. Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: A systematic review. Clin. Infect. Dis. 2014, 59 (Suppl. S4), S213–S219. [Google Scholar] [CrossRef] [Green Version]
- Sequeira, I.R.; Lentle, R.G.; Kruger, M.C.; Hurst, R.D. Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability. PLoS ONE 2014, 9, e99256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fasano, A.; Not, T.; Wang, W.; Uzzau, S.; Berti, I.; Tommasini, A.; Goldblum, S.E. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 2000, 355, 1518–1519. [Google Scholar] [CrossRef]
- Klatt, N.R.; Harris, L.D.; Vinton, C.L.; Sung, H.; Briant, J.A.; Tabb, B.; Morcock, D.; McGinty, J.W.; Lifson, J.D.; Lafont, B.A.; et al. Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation, immune activation, and IL-17 production in the absence of SIV infection. Mucosal Immunol. 2010, 3, 387–398. [Google Scholar] [CrossRef]
- Kosek, M.; Haque, R.; Lima, A.; Babji, S.; Shrestha, S.; Qureshi, S.; Amidou, S.; Mduma, E.; Lee, G.; Yori, P.P.; et al. Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. Am. J. Trop. Med. Hyg. 2013, 88, 390–396. [Google Scholar] [CrossRef] [Green Version]
- Chandra, R.K.; Gill, B.; Kumari, S. Food allergy and atopic disease: Pathogenesis, diagnosis, prediction of high risk, and prevention. Ann. Allergy 1993, 71, 495–502. [Google Scholar]
- Osterballe, M.; Hansen, T.K.; Mortz, C.G.; Høst, A.; Bindslev-Jensen, C. The prevalence of food hypersensitivity in an unselected population of children and adults. Pediatr. Allergy Immunol. 2005, 16, 567–573. [Google Scholar] [CrossRef] [PubMed]
- Björkstén, B.; Crevel, R.; Hischenhuber, C.; Løvik, M.; Samuels, F.; Strobel, S.; Taylor, S.L.; Wal, J.M.; Ward, R. Criteria for identifying allergenic foods of public health importance. Regul. Toxicol. Pharmacol. 2008, 51, 42–52. [Google Scholar] [CrossRef] [PubMed]
- Rona, R.J.; Keil, T.; Summers, C.; Gislason, D.; Zuidmeer, L.; Sodergren, E.; Sigurdardottir, S.T.; Lindner, T.; Goldhahn, K.; Dahlstrom, J.; et al. The prevalence of food allergy: A meta-analysis. J. Allergy Clin. Immunol. 2007, 120, 638–646. [Google Scholar] [CrossRef] [PubMed]
- Eggesbø, M.; Botten, G.; Halvorsen, R.; Magnus, P. The prevalence of CMA/CMPI in young children: The validity of parentally perceived reactions in a population-based study. Allergy 2001, 56, 393–402. [Google Scholar] [CrossRef]
- Chafen, J.J.; Newberry, S.J.; Riedl, M.A.; Bravata, D.M.; Maglione, M.; Suttorp, M.J.; Sundaram, V.; Paige, N.M.; Towfigh, A.; Hulley, B.J.; et al. Diagnosing and managing common food allergies: A systematic review. JAMA 2010, 303, 1848–1856. [Google Scholar] [CrossRef]
- Kim, J.S.; Nowak-Węgrzyn, A.; Sicherer, S.H.; Noone, S.; Moshier, E.L.; Sampson, H.A. Dietary baked milk accelerates the resolution of cow’s milk allergy in children. J. Allergy Clin. Immunol. 2011, 128, 125–131.e2. [Google Scholar] [CrossRef] [Green Version]
- Vieira, M.C.; Morais, M.B.; Spolidoro, J.V.; Toporovski, M.S.; Cardoso, A.L.; Araujo, G.T.; Nudelman, V.; Fonseca, M.C. A survey on clinical presentation and nutritional status of infants with suspected cow’ milk allergy. BMC Pediatr. 2010, 10, 25. [Google Scholar] [CrossRef]
- Meyer, R.; Wright, K.; Vieira, M.C.; Chong, K.W.; Chatchatee, P.; Vlieg-Boerstra, B.J.; Groetch, M.; Dominguez-Ortega, G.; Heath, S.; Lang, A.; et al. International survey on growth indices and impacting factors in children with food allergies. J. Hum. Nutr. Diet. 2019, 32, 175–184. [Google Scholar] [CrossRef]
- van Elburg, R.M.; Fetter, W.P.; Bunkers, C.M.; Heymans, H.S. Intestinal permeability in relation to birth weight and gestational and postnatal age. Arch. Dis. Child Fetal. Neonatal Ed. 2003, 88, F52–F55. [Google Scholar] [CrossRef] [Green Version]
- Kuitunen, M.; Saukkonen, T.; Ilonen, J.; Akerblom, H.K.; Savilahti, E. Intestinal permeability to mannitol and lactulose in children with type 1 diabetes with the HLA-DQB1*02 allele. Autoimmunity 2002, 35, 365–368. [Google Scholar] [CrossRef]
- Reinhardt, M.C. Macromolecular absorption of food antigens in health and disease. Ann. Allergy 1984, 53 Pt 2, 597–601. [Google Scholar]
- Van Elburg, R.M.; Heymans, H.S.; De Monchy, J.G. Effect of disodiumcromoglycate on intestinal permeability changes and clinical response during cow’s milk challenge. Pediatr. Allergy Immunol. 1993, 4, 79–85. [Google Scholar] [CrossRef] [PubMed]
- Schrander, J.J.; Unsalan-Hooyen, R.W.; Forget, P.P.; Jansen, J. [51Cr]EDTA intestinal permeability in children with cow’s milk intolerance. J. Pediatr. Gastroenterol. Nutr. 1990, 10, 189–192. [Google Scholar] [CrossRef] [PubMed]
- Paganelli, R.; Levinsky, R.J.; Brostoff, J.; Wraith, D.G. Immune complexes containing food proteins in normal and atopic subjects after oral challenge and effect of sodium cromoglycate on antigen absorption. Lancet 1979, 1, 1270–1272. [Google Scholar] [CrossRef]
- Paganelli, R.; Atherton, D.J.; Levinsky, R.J. Differences between normal and milk allergic subjects in their immune responses after milk ingestion. Arch. Dis. Child. 1983, 58, 201–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heyman, M.; Desjeux, J.F. Cytokine-induced alteration of the epithelial barrier to food antigens in disease. Ann. N. Y. Acad. Sci. 2000, 915, 304–311. [Google Scholar] [CrossRef]
- Salinas, E.; Reyes-Pavón, D.; Cortes-Perez, N.G.; Torres-Maravilla, E.; Bitzer-Quintero, O.K.; Langella, P.; Bermúdez-Humarán, L.G. Bioactive Compounds in Food as a Current Therapeutic Approach to Maintain a Healthy Intestinal Epithelium. Microorganisms. 2021, 9, 1634. [Google Scholar] [CrossRef]
- Jackson, P.G.; Lessof, M.H.; Baker, R.W.; Ferrett, J.; MacDonald, D.M. Intestinal permeability in patients with eczema and food allergy. Lancet 1981, 1, 1285–1286. [Google Scholar] [CrossRef]
- Benard, A.; Desreumeaux, P.; Huglo, D.; Hoorelbeke, A.; Tonnel, A.B.; Wallaert, B. Increased intestinal permeability in bronchial asthma. J. Allergy Clin. Immunol. 1996, 97, 1173–1178. [Google Scholar] [CrossRef]
- Zauli, D.; Grassi, A.; Granito, A.; Foderaro, S.; De Franceschi, L.; Ballardini, G.; Bianchi, F.B.; Volta, U. Prevalence of silent coeliac disease in atopics. Dig. Liver Dis. 2000, 32, 775–779. [Google Scholar] [CrossRef]
- Bottaro, G.; Cataldo, F.; Rotolo, N.; Spina, M.; Corazza, G.R. The clinical pattern of subclinical/silent celiac disease: An analysis on 1026 consecutive cases. Am. J. Gastroenterol. 1999, 94, 691–696. [Google Scholar] [CrossRef]
- Liu, Z.; Li, N.; Neu, J. Tight junctions, leaky intestines, and pediatric diseases. Acta Paediatr. 2005, 94, 386–393. [Google Scholar] [CrossRef] [PubMed]
- Sheen, Y.H.; Jee, H.M.; Kim, D.H.; Ha, E.K.; Jeong, I.J.; Lee, S.J.; Baek, H.S.; Lee, S.W.; Lee, K.J.; Lee, K. Serum zonulin is associated with presence and severity of atopic dermatitis in children, independent of total IgE and eosinophil. Clin. Exp. Allergy 2018, 48, 1059–1062. [Google Scholar] [CrossRef] [PubMed]
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Niewiem, M.; Grzybowska-Chlebowczyk, U. Intestinal Barrier Permeability in Allergic Diseases. Nutrients 2022, 14, 1893. https://doi.org/10.3390/nu14091893
Niewiem M, Grzybowska-Chlebowczyk U. Intestinal Barrier Permeability in Allergic Diseases. Nutrients. 2022; 14(9):1893. https://doi.org/10.3390/nu14091893
Chicago/Turabian StyleNiewiem, Monika, and Urszula Grzybowska-Chlebowczyk. 2022. "Intestinal Barrier Permeability in Allergic Diseases" Nutrients 14, no. 9: 1893. https://doi.org/10.3390/nu14091893