Dynamics of Non-conventional Intraepithelial Lymphocytes—NK, NKT, and γδ T—in Celiac Disease: Relationship with Age, Diet, and Histopathology
Abstract
Background Intraepithelial lymphocytes (IEL) are a heterogeneous population of lymphocytes raised in celiac disease (CD), whose role in CD pathogenesis remains to be defined.Aims To investigate how the age of diagnosis, diet, and the severity of the histological lesions are related to the changes observed in unconventional IEL populations.Methods Prospective analysis of 101 confirmed celiac patients from a single center, including 66 at diagnosis (45 children, 21 adults) and 112 non-celiac controls (12 children, 100 adults). IEL from duodenal biopsies were studied by six-color flow cytometry. The results were analyzed in relationship with age, diet (gluten intake), and histopathology (Marsh type).Results In comparison with respective age controls, both children and adult patients showed duodenal intraepithelial lymphocytosis with significant differences in every single non-conventional IEL population: CD3+ TCR γδ, NK (CD3-, CD16+, CD56+), NKT (CD3+, CD161+, CD56+), and iNKT (CD3+ Vα24) (P < 0.001 for all). Gluten intake was not only directly associated with severe atrophy, but also with decreased percentages of NK (P = 0.02), NKT (P = 0.003), and iNKT (P = 0.03). Changes in iNKT and γδ IEL were more marked in celiac children compared with celiac adults (P = 0.02 and 0.01, respectively). In contrast, increased CD3+ TCR γδ were diet- and Marsh grade-independent.Conclusions The typical phenotypical profile of intraepithelial lymphocytosis in untreated pediatric and adult celiacs consists of increased CD3+ TCR γδ populations with decreased NK, NKT, and iNKT cells. NK, NKT, and iNKT IEL, but not γδ IEL, are dynamic populations associated with diet, age, and histopathology.
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The diagnostic efficacy of the assessment of iIELs by flow cytometry has been confirmed for the differentiation of active celiac disease patients, celiac disease in remission and subclinical or potential celiac disease in both pediatric and adult patients.
“The diagnostic efficacy of the assessment of iIELs by flow cytometry has been confirmed for the differentiation of active celiac disease patients, Celiac disease in remission and subclinical or potential celiac disease in both pediatric and adult patients [315-318]”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [318]
Cites
Green, P. H. R., & Jones, R. (2006) · Cited by 2,453 · see citing works
The histopathology of coeliac disease
Oberhuber, G., Granditsch, G., & Vogelsang, H. (1999) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-199910000-00019 · Cited by 1,705 · see citing works
Green, P. H. R., & Cellier, C. (2007) · New England Journal of Medicine · doi:10.1056/nejmra071600 · Cited by 1,617 · see citing works
Meresse, B., Chen, Z., Ciszewski, C., Tretiakova, M., Bhagat, G., Krausz, T. N., Raulet, D. H., Lanier, L. L., Groh, V., Spies, T. A., et al. (2004) · Immunity · doi:10.1016/j.immuni.2004.06.020 · Cited by 853 · see citing works
A Direct Role for NKG2D/MICA Interaction in Villous Atrophy during Celiac Disease
Hüe, S., Mention, J., Monteiro, R. C., Zhang, S., Cellier, C., Schmitz, J., Verkarre, V., Fodil, N., Bahram, S., Cerf–Bensussan, N., et al. (2004) · Immunity · doi:10.1016/j.immuni.2004.06.018 · Cited by 758 · see citing works
Maiuri, L., Ciacci, C., Ricciardelli, I., Vacca, L., Raia, V., Auricchio, S., PICARD, J. K., Osman, M., Quaratino, S., & Londei, M. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13803-2 · Cited by 611 · see citing works
Intraepithelial lymphocytes: exploring the Third Way in immunology
Hayday, A., Theodoridis, E., Ramsburg, E., & Shires, J. (2001) · Nature Immunology · doi:10.1038/ni1101-997 · Cited by 491 · see citing works
Quantitation of intraepithelial lymphocytes in human jejunum
Ferguson, A., & Murray, D. J. (1971) · Gut · doi:10.1136/gut.12.12.988 · Cited by 399 · see citing works
Celiac disease–like abnormalities in a subgroup of patients with irritable bowel syndrome
Wahnschaffe, U., Ullrich, R., Riecken, E. O., & Schulzke, J. D. (2001) · Gastroenterology · doi:10.1053/gast.2001.29572 · Cited by 280 · see citing works
van der Vliet, H. J., Blomberg, B. M. E. V., Nishi, N., Reijm, M., Voskuyl, A. E., Bodegraven, A. A. V., Polman, C. H., Rustemeyer, T., Lips, P. T. A. M., van den Eertwegh, A. J. M., et al. (2001) · Clinical Immunology · doi:10.1006/clim.2001.5060 · Cited by 267 · see citing works
Montoya, C. J., Pollard, D. J., Martinson, J., Kumari, K., Wasserfall, C. H., Mulder, C. B., Rugeles, M. T., Atkinson, M. A., LANDAY, A. L., & Wilson, S. B. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02647.x · Cited by 245 · see citing works
Testing the NKT cell hypothesis of human IDDM pathogenesis
Lee, P. T., Putnam, A. L., Benlagha, K., Teyton, L., Gottlieb, P. A., & Bendelac, A. S. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15832 · Cited by 234 · see citing works
Testing the NKT cell hypothesis of human IDDM pathogenesis
Lee, P. T., Putnam, A. L., Benlagha, K., Teyton, L., Gottlieb, P. A., & Bendelac, A. S. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215832 · Cited by 213 · see citing works
Celiac Disease-like Abnormalities in a Subgroup of Patients With Irritable Bowel Syndrome
&NA; (2002) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200201000-00020 · Cited by 210 · see citing works
Bhagat, G., Naiyer, A. J., Shah, J. G., Harper, J., Jabri, B., Wang, T. C., Green, P. H. R., & Manavalan, J. S. (2008) · Journal of Clinical Investigation · doi:10.1172/jci30989 · Cited by 188 · see citing works
Mechanisms of Disease: immunopathogenesis of celiac disease
Jabrì, B., & Sollid, L. M. (2006) · Nature Clinical Practice Gastroenterology & Hepatology · doi:10.1038/ncpgasthep0582 · Cited by 187 · see citing works
Kutlu, T., Brousse, N., Rambaud, C., Le Deist, F., Schmitz, J., & Cerf-Bensussan, N. (1993) · Gut · doi:10.1136/gut.34.2.208 · Cited by 178 · see citing works
Mäki, M., Holm, K., Collin, P., & Savilahti, E. (1991) · Gut · doi:10.1136/gut.32.11.1412 · Cited by 177 · see citing works
Spencer, J., MacDonald, T. T., Diss, T. C., Walker‐Smith, J. A., Ciclitira, P. J., & Isaacson, P. G. (1989) · Gut · doi:10.1136/gut.30.3.339 · Cited by 169 · see citing works
Intraepithelial lymphocytes in celiac disease
Järvinen, T. T. (2003) · The American Journal of Gastroenterology · doi:10.1016/s0002-9270(03)00230-2 · Cited by 145 · see citing works
Age-Related Clinical, Serological, and Histopathological Features of Celiac Disease
Vivas, S., Morales, J., Fernandez, M. L., Hernando, M., Herrero, B., Casqueiro, J., & Gutiérrez, S. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2008.01977.x · Cited by 141 · see citing works
Self-citationIntraepithelial Lymphocytes in Celiac Disease
Järvinen, T. T., Kaukinen, K., Laurila, K., et al. (2003) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2003.07456.x · Cited by 136 · see citing works
Intraepithelial γδ T-cell-receptor lymphocytes and genetic susceptibility to coeliac disease
Holm, K., Mäki, M., Savilahti, E., Laippala, P. J., Lipsanen, V., & Koskimies, S. (1992) · The Lancet · doi:10.1016/0140-6736(92)91262-7 · Cited by 127 · see citing works
Human small-intestinal epithelium contains functional natural killer lymphocytes
León, F., Roldán, E., Sánchez‐Muñoz, L., Camarero, C., Bootello, A., & Roy, G. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00886-2 · Cited by 109 · see citing works
Exley, M. A., Hou, R., Shaulov, A., Tonti, E., Dellabona, P., Casorati, G., Akbari, O., Akman, H. O., Greenfield, E. A., Gumperz, J. E., et al. (2008) · European Journal of Immunology · doi:10.1002/eji.200737389 · Cited by 98 · see citing works
Lymphocytic Duodenosis and the Spectrum of Celiac Disease
Voort, J. L. V., Murray, J. A., Lahr, B. D., Dyke, C. T. V., Kroning, C. M., Moore, S. B., & Wu, T. (2008) · The American Journal of Gastroenterology · doi:10.1038/ajg.2008.7 · Cited by 77 · see citing works
Diagnostic methods beyond conventional histology in coeliac disease diagnosis
Salmi, T. T., Collin, P., Reunala, T. L., Mäki, M., & Kaukinen, K. (2009) · Digestive and Liver Disease · doi:10.1016/j.dld.2009.04.004 · Cited by 67 · see citing works
Intraepithelial lymphocytes and coeliac disease
Collin, P., Wahab, P. J., & Murray, J. A. (2005) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2005.01.005 · Cited by 43 · see citing works
Cytokine Production by Intestinal Intraepithelial Lymphocyte Subsets in Celiac Disease
Le�n, F., S�nchez, L., Camarero, C., & Roy, G. (2005) · Digestive Diseases and Sciences · doi:10.1007/s10620-005-2480-5 · Cited by 37 · see citing works
Deficiency of invariant natural killer T cells in coeliac disease
Grose, R., Cummins, A. G., & Thompson, F. M. (2006) · Gut · doi:10.1136/gut.2006.095307 · Cited by 36 · see citing works
Intraepithelial Lymphocytes in Celiac Disease
Sollid, L. M. (2004) · Immunity · doi:10.1016/j.immuni.2004.08.002 · Cited by 33 · see citing works
Verkasalo, M., Arató, A., Savilahti, E., & Tainio, V.-M. (1990) · Gut · doi:10.1136/gut.31.4.422 · Cited by 29 · see citing works
Age-Related Variation of Intraepithelial Lymphocytes Subsets in Normal Human Duodenal Mucosa
Camarero, C., Leon, F., Sanchez, L., Asensio, A., & Roy, G. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9176-3 · Cited by 25 · see citing works
Immune Phenotype of Children with Newly Diagnosed and Gluten-Free Diet-Treated Celiac Disease
Cseh, Á., Vásárhelyi, B., Szalay, B., Molnár, K., Nagy‐Szakal, D., Treszl, A., Vannay, Á., Arató, A., Tulassay, T., & Veres, G. (2010) · Digestive Diseases and Sciences · doi:10.1007/s10620-010-1363-6 · Cited by 24 · see citing works
Decreased circulating iNKT cell numbers in refractory coeliac disease
Bernardo, D., van Hoogstraten, I. M. W., Verbeek, W. H. M., Peña, A. S., Mearin, M. L., Arranz, E. M., Garrote, J. A., Scheper, R. J., Schreurs, M. W. J., Bontkes, H. J., et al. (2007) · Clinical Immunology · doi:10.1016/j.clim.2007.09.005 · Cited by 24 · see citing works
Deficiency of 6B11+ Invariant NK T-Cells in Celiac Disease
Grose, R., Thompson, F. M., & Cummins, A. G. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-007-0093-x · Cited by 22 · see citing works
Hadžiselimović, F., Emmons, L. R., Schaub, U., Signer, E., Bürgin-Wolff, A., & Krstic, R. (1992) · Gut · doi:10.1136/gut.33.6.767 · Cited by 13 · see citing works
Specificity of IEL Profiling in the Diagnosis of Celiac Disease
León, F., Camarero, C., Eiras, P., & Roy, G. (2004) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2004.40075.x · Cited by 8 · see citing works
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Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · see citing works
Diverse developmental pathways of intestinal intraepithelial lymphocytes
McDonald, B. D., Jabri, B., & Bendelac, A. (2018) · Nature Reviews Immunology · doi:10.1038/s41577-018-0013-7 · Cited by 190 · see citing works
Intraepithelial lymphocytes in celiac disease immunopathology
Abadie, V., Discepolo, V., & Jabri, B. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-012-0316-x · Cited by 183 · see citing works
Ilus, T., Lähdeaho, M., Salmi, T. T., Haimila, K., Partanen, J., Saavalainen, P., Heini, H., Mäki, M., Collin, P., & Kaukinen, K. (2012) · The American Journal of Gastroenterology · doi:10.1038/ajg.2012.220 · Cited by 129 · see citing works
Dunne, M. R., Elliott, L., Hussey, S., Mahmud, N. U., Kelly, J., Doherty, D. G., & Feighery, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076008 · Cited by 125 · see citing works
Håkansson, Å., Aronsson, C. A., Brundin, C., Oscarsson, E., Molin, G., & Agardh, D. (2019) · Nutrients · doi:10.3390/nu11081925 · Cited by 90 · see citing works
Montalban‐Arques, A., Chaparro, M., Gisbert, J. P., & Bernardo, D. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy177 · Cited by 61 · see citing works
Age-related differences in celiac disease: Specific characteristics of adult presentation
Vivas, S. (2015) · World Journal of Gastrointestinal Pharmacology and Therapeutics · doi:10.4292/wjgpt.v6.i4.207 · Cited by 56 · see citing works
Self-citationPathogenesis of Enteropathy-Associated T Cell Lymphoma
Chander, U., Leeman‐Neill, R. J., & Bhagat, G. (2018) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-018-0459-5 · Cited by 56 · see citing works
Sagebiel, A. F., Steinert, F. L., Lunemann, S., Körner, C., Schreurs, R., Altfeld, M. A., Perez, D. R., Reinshagen, K., & Bunders, M. J. (2019) · Nature Communications · doi:10.1038/s41467-018-08267-7 · Cited by 57 · see citing works
Fernández-Bañares, F., Carrasco, A., García-Puig, R., Rosinach, M., González, C., Alsina, M., Loras, C., Salas, A., Viver, J. M., & Esteve, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101249 · Cited by 49 · see citing works
Natural Killer Cell Integrins and Their Functions in Tissue Residency
Shannon, M. J., & Mace, E. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.647358 · Cited by 49 · see citing works
Gamma-Delta T Lymphocytes in the Diagnostic Approach of Coeliac Disease
Nijeboer, P., Gils, T. V., Reijm, M., Ooijevaar, R. E., Lissenberg-Witte, B. I., Bontkes, H. J., Mulder, C. J. J., & Bouma, G. (2018) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001060 · Cited by 43 · see citing works
Immunomodulation at epithelial sites by obesity and metabolic disease
Cheung, K. P., Taylor, K. R., & Jameson, J. (2011) · Immunologic Research · doi:10.1007/s12026-011-8261-7 · Cited by 39 · see citing works
Eggesbø, L. M., Risnes, L. F., Neumann, R. S., Lundin, K. E. A., Christophersen, A. O., & Sollid, L. M. (2019) · Mucosal Immunology · doi:10.1038/s41385-019-0222-9 · Cited by 38 · see citing works
Costes, L. M. M., Lindenbergh-Kortleve, D. J., van Berkel, L. A., Veenbergen, S., Raatgeep, H. C., Simons-Oosterhuis, Y., van Haaften, D. H., Karrich, J. J., Escher, J. C., Groeneweg, M., et al. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0118-0 · Cited by 33 · see citing works
Fernández‐Bañares, F., Carrasco, A., Martín‐Cardona, A., & Esteve, M. (2019) · Nutrients · doi:10.3390/nu11091992 · Cited by 33 · see citing works
Schmitz, F., Kooy–Winkelaar, Y., Wiekmeijer, A., Brugman, M. H., Mearin, M. L., Mulder, C. J. J., Lopes, S. M. C. D. S., Mummery, C. L., Staal, F. J. T., van Bergen, J., et al. (2015) · Gut · doi:10.1136/gutjnl-2014-308153 · Cited by 31 · see citing works
Bank, I., & Marcu‐Malina, V. (2013) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-013-8391-x · Cited by 27 · see citing works
Ong, M. L. D. M., Yeruva, S., Sailer, A., Nilsen, S. P., & Turner, J. R. (2019) · Laboratory Investigation · doi:10.1038/s41374-019-0324-8 · Cited by 26 · see citing works
The composition of T cell subtypes in duodenal biopsies are altered in coeliac disease patients
Steenholt, J. V., Nielsen, C., Leen, B., Staal, A., Rasmussen, K. S., Sabir, H. J., Barington, T., Husby, S., & Toft‐Hansen, H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170270 · Cited by 25 · see citing works
Non-celiac gluten sensitivity: Clinical presentation, etiology and differential diagnosis
Miranda, M. E., Garcia-Valdes, L., Espigares, E., Leno‐Durán, E., & Requena, P. (2023) · Gastroenterología y Hepatología (English Edition) · doi:10.1016/j.gastre.2022.10.010 · Cited by 24 · see citing works
Mandile, R., Maglio, M., Mosca, C., Marano, A., Discepolo, V., Troncone, R., & Auricchio, R. (2022) · Nutrients · doi:10.3390/nu14183696 · Cited by 26 · see citing works
Intraepithelial lymphocytes subsets in different forms of celiac disease
Sánchez-Castañon, M., Castro, B. G., Toca, M., Santacruz, C., Arias-Loste, M., Iruzubieta, P., Crespo, J., & López-Hoyos, M. (2016) · Autoimmunity Highlights · doi:10.1007/s13317-016-0085-y · Cited by 23 · see citing works
Intestinal and blood lymphograms as new diagnostic tests for celiac disease
Roy, G., Fernández‐Bañares, F., Corzo, M., Gómez-Aguililla, S., García‐Hoz, C., & Núñez, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1081955 · Cited by 22 · see citing works
A gluten-free diet lowers NKG2D and ligand expression in BALB/c and non-obese diabetic (NOD) mice
Adlercreutz, E. H., Weile, C., Larsen, J., Engkilde, K., Agardh, D., Buschard, K., & Antvorskov, J. C. (2014) · Clinical & Experimental Immunology · doi:10.1111/cei.12340 · Cited by 22 · see citing works
Cellular and molecular bases of refractory celiac disease
Soderquist, C. R., & Bhagat, G. (2021) · International review of cytology · doi:10.1016/bs.ircmb.2020.12.001 · Cited by 22 · see citing works
Popp, A., Taavela, J., Graziano, P., Parente, P., Covelli, C., Lamacchia, C., Andriulli, A., Mäki, M., & Isola, J. J. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06680-x · Cited by 19 · see citing works
Martín‐Cardona, A., Carrasco, A., Arau, B., Vidal, J., Tristán, E., Ferrer, C., González-Puglia, G., Pallarés, N., Tebé, C., Farráis, S., et al. (2024) · Nutrients · doi:10.3390/nu16142294 · Cited by 18 · see citing works
Epithelial cell dysfunction in coeliac disease
Escudero‐Hernández, C. (2020) · International review of cytology · doi:10.1016/bs.ircmb.2020.09.007 · Cited by 17 · see citing works
Foers, A. D., Shoukat, M. S., Welsh, O. E., Donovan, K., Petry, R., Evans, S. C., FitzPatrick, M. E. B., Collins, N., Klenerman, P., Fowler, A., et al. (2020) · The Journal of Pathology · doi:10.1002/path.5592 · Cited by 17 · see citing works
Ruiz-Ramírez, P., Carreras, G., Fajardo, I., Tristán, E., Carrasco, A., Salvador, I., Zabana, Y., Andújar, X., Ferrer, C., Horta, D., et al. (2021) · Nutrients · doi:10.3390/nu13051684 · Cited by 16 · see citing works
Innate lymphoid cells and natural killer T cells in the gastrointestinal tract immune system.
Montalvillo, E., Garrote, J. A., Bernardo, D., & Arranz, E. M. (2014) · PubMed · Cited by 14 · see citing works
Laurikka, P., Lindfors, K., Oittinen, M., Huhtala, H., Salmi, T. T., Lähdeaho, M., Ilus, T., Mäki, M., Kaukinen, K., & Kurppa, K. (2018) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001013 · Cited by 14 · see citing works
Camarero, C., de Andrés, A., García‐Hoz, C., Roldán, B., Muriel, A., León, F., & Roy, G. (2021) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000426 · Cited by 15 · see citing works
Sensibilidad al gluten no celiaca: etiología, diagnóstico diferencial y presentación clínica
Miranda, M. E., Garcia-Valdes, L., Espigares, E., Leno‐Durán, E., & Requena, P. (2022) · Gastroenterología y Hepatología · doi:10.1016/j.gastrohep.2022.10.001 · Cited by 13 · see citing works
Mata‐Romero, P., Martín-Holgado, D., Ferreira-Nossa, H. C., Gonzalez-Cordero, P. L., Izquierdo-Martín, A., Barros-García, P., Fernandez-Gonzalez, N., Pereira, L. F., Hijón, C. C., & Molina‐Infante, J. (2022) · Gastroenterología y Hepatología · doi:10.1016/j.gastrohep.2022.03.011 · Cited by 12 · see citing works
Basu, K., Creasey, H., Bruggeman, N., Stevens, J., Bloxham, D. M., & Woodward, J. M. (2021) · Frontline Gastroenterology · doi:10.1136/flgastro-2021-101838 · Cited by 11 · see citing works
Intraepithelial Lymphogram in the Diagnosis of Celiac Disease in Adult Patients: A Validation Cohort
García‐Hoz, C., Crespo, L., Pariente, R., Andrés, A. D., Rodríguez-Ramos, R., & Roy, G. (2024) · Nutrients · doi:10.3390/nu16081117 · Cited by 13 · see citing works
Enteropathy-Associated T-Cell Lymphoma
Wong, K., & Mead, M. D. (2020) · Springer eBooks · doi:10.1007/978-3-030-56722-4_11 · Cited by 11 · see citing works
Lindeman, I., & Sollid, L. M. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00452-0 · Cited by 11 · see citing works
Increased Intraepithelial Vα24 Invariant NKT Cells in the Celiac Duodenum
Montalvillo, E., Bernardo, D., Martínez‐Abad, B., Allegretti, Y., Fernández-Salazar, L. I., Calvo, C. M., Chirdo, F. G., Garrote, J. A., & Arranz, E. M. (2015) · Nutrients · doi:10.3390/nu7115444 · Cited by 7 · see citing works
Jansen, M. A. E., van den Heuvel, D., Jaddoe, V. W. V., van Zelm, M. C., & Moll, H. A. (2017) · Clinical Immunology · doi:10.1016/j.clim.2017.04.008 · Cited by 6 · see citing works
Anti-Anisakis sp. antibodies in serum of healthy subjects. Relationship with αβ and γδ T cells
Zamora, V., García‐Ballesteros, C., Benet, C., Ballester, F., Cuéllar, C., & Andreu‐Ballester, J. C. (2016) · Acta Parasitologica · doi:10.1515/ap-2017-0011 · Cited by 5 · see citing works
Núñez, C., Carrasco, A., Corzo, M., Pariente, R., Esteve, M., & Roy, G. (2023) · Methods in cell biology · doi:10.1016/bs.mcb.2022.11.004 · Cited by 6 · see citing works
Duodenal lymphogram as a complementary tool in the diagnosis of celiac disease in adults
Gómez, B. B., Escudero‐Hernández, C., de Pedro, R., Montalvillo, E., Bernardo, D., García‐Lagarto, E., Garrote, J. A., Sanz, E. A., & Fernández-Salazar, L. I. (2020) · Revista Española de Enfermedades Digestivas · doi:10.17235/reed.2020.6391/2019 · Cited by 4 · see citing works
The Role of Invariant Natural Killer T Cells in Autoimmune Diseases
Wingender, G., & Kronenberg, M. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-384929-8.00008-3 · Cited by 3 · see citing works
New tools for the Diagnosis of Celiac Disease
Fernández‐Bañares, F., Farré, C., Carrasco, A., Mariné, M., & Esteve, M. (2015) · doi:10.3926/oms.255 · Cited by 3 · see citing works
Coeliac disease and multiple immunodeficiencies: case report of a diagnostic dilemma.
Anis, S., Kumar, R., Abbas, Z., Hassan, S. M., Luck, N. H., & Muzaffar, R. (2012) · PubMed · Cited by 3 · see citing works
Arregui, M. V. (2016) · Annals of Gastroenterology · doi:10.20524/aog.2016.0113 · Cited by 3 · see citing works
Immunopathology of Celiac Disease
Abadie, V., & Jabrì, B. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-415847-4.00080-x · Cited by 2 · see citing works
The emerging paradigm of Unconventional T cells as a novel therapeutic target for celiac disease
Parihar, N., & Bhatt, L. K. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110666 · Cited by 2 · see citing works
Gamma-Delta T lymphocytes in the Diagnostic Approach of Celiac Disease
Fernández‐Bañares, F., & Esteve, M. (2019) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001196 · Cited by 1 · see citing works
The Role of Invariant Natural Killer T Cells in Autoimmune Diseases
Wingender, G., & Kronenberg, M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-812102-3.00007-5 · Cited by 1 · see citing works
Inmunogenética de la enfermedad celiaca: papel de la IL-15 y su receptor
Escudero‐Hernández, C. (2015) · doi:10.35376/10324/16087
Kriszta, M. (2012) · Semmelweis University Repository (Semmelweis University) · doi:10.14753/se.2012.1788
Mata‐Romero, P., Martín-Holgado, D., Ferreira-Nossa, H. C., Gonzalez-Cordero, P. L., Izquierdo-Martín, A., Barros-García, P., Fernandez-Gonzalez, N., Pereira, L. F., Hijón, C. C., & Molina‐Infante, J. (2022) · Gastroenterología y Hepatología (English Edition) · doi:10.1016/j.gastre.2022.03.002
Ultra-Short Celiac Disease: Clinical, Immunophenotypic, Morphological, and Genetic Features
Хавкин, А. И., Лошкова, Е. В., Yablokova, E. A., Yankina, G. N., Nalyotov, A. V., Желев, В. А., Владимирович, Б. А., Дмитриевна, З. К., Popova, A. D., & Федосова, М. В. (2026) · Педиатрическая фармакология · doi:10.15690/pf.v22i6.2988
Cirrhosis-associated immune dysfunction reflects impaired intestinal CD8αβ⁺ IEL compartmentalizationPreprint
Akkaya, C., van Sligtenhorst, M., Shaukat, S., Modave, E., Dumarey, A., Caxali, G. H., Verbiest, A., Meyere, L. D., Vrancken, S., Meerbeeck, L. V., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.26.713594
- Authors
- Calleja, S., Vivas, S., Santiuste, M., Arias, L., Hernando, M., Nistal, E., Casqueiro, J., & Ruiz de Morales, J. G.
- Affiliations
- Hospital Universitario de León (ES)
- Universidad de León (ES)
- Venue
- Digestive Diseases and Sciences
- Published
- 2011-01-08
- Volume
- 56
- Issue
- 7
- Pages
- 2042-2049
- ISSN
- 0163-2116 (ISSN-L)
- 1573-2568
- OpenAlex
- W2040610974
- Cited by
- 60
- References
- 37
- Citations by year
- 2026: 2 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 7 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 2 · 2016: 3 · 2015: 7 · 2014: 3 · 2013: 3 · 2012: 4
- FWCI
- 3.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Digestive Diseases and Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Junta de Castilla y León
- Instituto de Salud Carlos III
- Topics
- Health Sciences › Medicine › Gastroenterology › Celiac Disease Research and Management
- Health Sciences › Medicine › Surgery › Eosinophilic Esophagitis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Keywords
- celiac disease, intraepithelial lymphocytes, natural killer cells, NKT cells, invariant natural killer T cells, γδ T cells, intraepithelial lymphocytosis, gluten intake, duodenal histopathology, age at diagnosis, pediatric celiac disease, duodenal biopsy
- MeSH terms
- Adolescent, Adult, Age Factors, Aged, Celiac Disease, Child, Child, Preschool, Diet, Duodenum, Female, Glutens, Humans, Infant, Intestinal Mucosa, Killer Cells, Natural, Lymphocytosis, Male, Middle Aged, Receptors, Antigen, T-Cell, gamma-delta, Natural Killer T-Cells, Young Adult
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