Contribution of the Leukocyte Adherence Inhibition Test to the Diagnosis of Non–IgE-mediated Immunoreactivity against Candida albicans in Patients with Atopic Dermatitis
Published: 2023-11-14
Page: 268-276
Issue: 2023 - Volume 6 [Issue 1]
Celso Eduardo Olivier *
Instituto Alergoimuno de Americana, Brazil.
Daiana Guedes Pinto
Instituto Alergoimuno de Americana, Brazil.
Ana Paula Monezzi Teixeira
Instituto Alergoimuno de Americana, Brazil.
Jhéssica Letícia Santos Santana
Instituto Alergoimuno de Americana, Brazil.
Raquel Acácia Pereira Gonçalves Santos
Instituto Alergoimuno de Americana, Brazil.
Regiane Patussi Santos Lima
Lavoisier’s Laboratories, São Paulo, Brazil.
Everton Salgado Monteiro
Department of Allergy and Immunopathology, Faculty of Medicine, São Paulo University, Brazil.
*Author to whom correspondence should be addressed.
Abstract
Aims: To evaluate the potential of the Leukocyte Adherence Inhibition Test (LAIT) to discriminate Non–IgE-mediated immunoreactivity against Candida albicans in Atopic Dermatitis () patients with clinical suspicion of hypersensitivity reactions to fungal allergens.
Study Design: We retrospectively examined the medical charts of 100 patients diagnosed with with clinical suspicion of Non–IgE-mediated fungal hypersensitivity who were investigated with an ex vivo challenge monitored by LAIT against an extract of Candida albicans.
Place and Duration of Study: Instituto Alergoimuno de Americana – São Paulo – Brazil – between January 2018 and October 2023.
Methodology: The percentage of Leukocyte Adherence Inhibition (LAI) promoted by the ex vivo challenges with C. albicans extract was distributed in ranges through a cascade distribution chart to outline the variability of the results.
Results: The mean LAI was 41.5%; SD 29.7%, ranging from 0% to 100%; mode = 0% (appeared 17 times). A wide distribution of LAI results suggested that some patients had immunoreactivity against the Candida albicans allergens while tolerant ones did not.
Conclusion: Our preliminary results support that the LAIT performed with Candida albicans may differentiate diverse degrees of ex vivo immunoreactivity against this airborne allergen in allergic patients.
Keywords: Allergy, Candida albicans, atopic dermatitis, diagnosis, hypersensitivity, leukocyte adherence inhibition test, non–IgE-mediated immunoreactivity
How to Cite
Downloads
References
Shen XX, Zhou X, Kominek J, Kurtzman CP, Hittinger CT, Rokas A. Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data. G3 (Genes, Genomes, Genetis). 2016;6(12):3927-3939.
Spatafora JW, Aime MC, Grigoriev IV, Martin F, Stajich JE, Blackwell M. The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies. Microbiol Spectr. 2017;5(5).
Ruggiero MA, Gordon DP, Orrell TM, Bailly N, Bourgoin T, Brusca RC, et al. A Higher Level Classification of All Living Organisms. PLOS ONE. 2015;10(4): e0119248.
Hittinger CT, Rokas A, Bai FY, Boekhout T, Gonçalves P, Jeffries TW, et al. Genomics and the making of yeast biodiversity. Curr Opin Genet Dev 2015; 35:100-9.
Soll DR, Pujol C. Candida albicans clades. FEMS Immunol Med Microbiol. 2003;39(1): 1-7.
Legrand M, Jaitly P, Feri A, d’Enfert C, Sanyal K. Candida albicans: An Emerging Yeast Model to Study Eukaryotic Genome Plasticity. Trends in Genetics. 2019;35(4): 292-307.
Arkowitz RA, Bassilana M. Recent advances in understanding Candida albicans hyphal growth. F1000Research. 2019;8.
Moyes DL, Shen C, Murciano C, Runglall M, Richardson JP, Arno M. et al. Protection against epithelial damage during Candida albicans infection is mediated by PI3K/Akt and mammalian target of rapamycin signaling. J Infect Dis. 2014;209(11):1816-26.
Moyes DL, Runglall M, Murciano C, Shen C, Nayar D, Thavaraj, et al. A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe. 2010; 8(3):225-35.
de Koning HD, Rodijk-Olthuis D, van Vlijmen-Willems IM, Joosten LA, Netea MG, et al. A comprehensive analysis of pattern recognition receptors in normal and inflamed human epidermis: upregulation of dectin-1 in psoriasis. J Invest Dermatol. 2010;130(11):2611-20.
Staab JF, Bradway SD, Fidel PL, Sundstrom P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science. 1999; 283(5407):1535-8.
Hoyer LL, Payne TL, Bell M, Myers AM, Scherer S. Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet. 1998:33(6);451-9.
Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA, Yeater K, et al. ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiol (Reading, England). 2004; 150(7):2415-2428.
Naglik JR. Fostira F, Ruprai J, Staab JF, Challacombe SJ, Sundstrom P. Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J Med Microbiol. 2006;55(10): 1323-1327.
Sundstrom P, Balish E, Allen C. Essential role of the Candida albicans transglutaminase substrate, hyphal wall protein 1, in lethal oroesophageal candidiasis in immunodeficient mice. J Infect Dis. 2002;185(4):521-30.
Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, et al. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 2007;5(3):e64.
Sun JN, Solis NV, Phan QT, Bajwa JS, Kashleva H, Thompson A, et al. Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog. 20106(11):e1001181.
Liu Y, Shetty AC, Schwartz JA, Bradford LL, Xu W, Phan QT, et al. New signaling pathways govern the host response to C. albicans infection in various niches. Genome Res. 2015;25(5):679-89.
Wächtler B, Citiulo F, Jablonowski N, Förster S, Dalle F, Schaller M. et al. Candida albicans-epithelial interactions: dissecting the roles of active penetration, induced endocytosis and host factors on the infection process. PLoS One. 2012; 7(5):e36952.
Naglik JR, König A, Hube B, Gaffen SL. Candida albicans-epithelial interactions and induction of mucosal innate Immunity. Curr Opin Microbiol. 2017;40: 104-112.
Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 2016; 532(7597):64-8.
Maeda K, Caldez MJ, Akira S. Innate immunity in allergy. Allergy. 2018;74(9): 1660-1674.
Wang Y, Zou Y, Chen X, Li H, Yin Z, Zhang B, et al. Innate immune responses against the fungal pathogen Candida auris. Nature communicat. 2022;13(1):3553.
Gazendam RP, van de Geer A, Roos D, van den Berg TK, Kuijpers TW. How neutrophils kill fungi. Immunol Rev. 2016; 273(1):299-311.
He Y, Liu J, Chen Y, Yan L, Wu J. Neutrophil Extracellular Traps in Candida albicans Infection. Front Immunol. 2022; 13:913028.
Eichelberger KR, Cassat JE. Metabolic adaptations during Staphylococcus aureus and Candida albicans co-Infection. Front Immunol. 2021;12:797550.
Wang Y. Looking into Candida albicans infection, host response, and antifungal strategies. Virulence. 2015:6(4): 307-8.
Poulain D. Candida albicans, plasticity and pathogenesis. Crit Rev Microbiol. 2015; 41(2):208-17.
Bonifazi P, Zelante T, D'Angelo C, De Luca A, Moretti S, Bozza, S, et al. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol. 2009;2(4): 362-74.
Koivikko A, Kalimo K, Nieminen E, Viander M. Relationship of immediate and delayed hypersensitivity to nasopharyngeal and intestinal growth of Candida albicans in allergic subjects. Allergy. 1988;43(3): 201-5.
Horner WE, Helbling A, Salvaggio JE, Lehrer SB. Fungal allergens. Clin Microbiol Rev. 1995;8(2):161-79.
Ishiguro A, Homma M, Torii S, Tanaka K. Identification of Candida albicans antigens reactive with immunoglobulin E antibody of human sera. Infect Immun. 1992;60(4): 1550-7.
Baldo BA, Baker RS. Inhalant allergies to fungi: reactions to bakers' yeast (Saccharomyces cerevisiae) and identification of bakers' yeast enolase as an important allergen. Int Arch Allergy Appl Immunol. 1988;86(2):201-8.
Savolainen J, Viander M, Einarsson R, Koivikko A. Allergenic variability of different strains of Candida albicans. Int Arch Allergy Appl Immunol. 1989:90(1):61-6.
Savolainen J, Viander M, Koivikko A. IgE-, IgA- and IgG-antibody responses to carbohydrate and protein antigens of Candida albicans in asthmatic children. Allergy. 1990;45(1):54-63.
Doekes G, Kaal MJ, van Ieperen-van Dijk AG. Allergens of Pityrosporum ovale and Candida albicans. II. Physicochemical characterization. Allergy. 1993;48(6):401-8.
Savolainen J, Lammintausta K, Kalimo K, Viander M. Candida albicans and Atopic Dermatitis. Clin Exp Allergy. 1993;23(4): 332-9.
Morita E, Hide M, Yoneya Y, Kannbe M, Tanaka A, Yamamoto S. An assessment of the role of Candida albicans antigen in Atopic Dermatitis. J Dermatol. 1999;26(5): 282-7.
Wächtler B, Wilson D, Haedicke K, Dalle F, Hube B. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One. 2011;6(2):e17046.
Kuratsuji T. Studies on leukocyte adherence inhibition test. Part II. Clinical applications of LAI test to detect delayed type hypersensitivity in infants and children. Keio J Med. 1981;30(2):65-9.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS, et al. Evaluating Non-IgE-mediated Allergens' Immunoreactivity in Patients with "Intrinsic" Persistent Rhinitis with Help of the Leukocyte Adherence Inhibition Test. Eur J Med Health Sci. 2023;5(1):17-22.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS, et al. Evaluating Non-IgE-Mediated Allergens' Immunoreactivity in Patients Formerly Classified as "Intrinsic" Asthmatics with Help of the Leukocyte Adherence Inhibition Test. Eur J Clin Med. 2023;4(2):1-7.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS, et al. Contribution of the Leukocyte Adherence Inhibition Test to the Diagnosis of Innate Non–IgE-mediated Immunoreactivity against Alternaria alternata. Asian J Immunol 2002;36(1): 243-251.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. Contribution of the Leukocyte Adherence Inhibition Test to the Diagnosis of Innate Non–IgE-mediated Immunoreactivity against Saccharomyces cerevisiae. Asian J Immunol 2023;6(1):234-241.
Olivier CE, Argentão DGP, Santos RAPG, Silva MD, Lima RPS, Zollner RL. Skin scrape test: an inexpensive and painless skin test for recognition of immediate hypersensitivity in children and adults. Open Allergy J. 2013;6:9-17.
Olivier CE, Lima RPS, Pinto DG, Santos RAPG, Silva GKM, Lorena SLS, et al. In search of a tolerance-induction strategy for cow's milk allergies: significant reduction of beta-lactoglobulin allergenicity via transglutaminase/cysteine polymerization. Clinics. 2012;67(10):1171-1179.
Olivier CE, Santos RAPG, Lima RPS, Argentão DGP, Silva GKM, Silva MD. A Novel Utility for an Old Method: The Leukocyte Adherence Inhibition Test Is an Easy Way to Detect the Immunoreactive Interference of the Collection Tube Anticoagulant on Cellular Immunoassays. J of Cell Adhesion 2014;1-6. Article ID 860427.
Available:http://dx.doi.org/10.1155/2014/860427.
Olivier CE, Pinto DG, Lima RPS, Silva MD, Santos RAPG, Teixeira APM, et al. Assessment of Immunoreactivity against Therapeutic Options Employing the Leukocyte Adherence Inhibition Test as a Tool for Precision Medicine. Eur J Clin Med. 2021;2(3):40-45.
Olivier CE, Pinto DG, Santos RAPG, Lima RPS. Dextran's interference over the Leukocyte Adherence Inhibition Test. Academia Letter. 2021;3792.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. 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. Eur J Clin Med. 2021;2(6):45-50.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. 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. Eur J Clin Med. 2022;3(1): 11-17.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. Contribution of the Leukocyte Adherence Inhibition Test for the evaluation of immunoreactivity against gluten extracts in non—IgE-mediated / non-autoimmune Gluten-Related Disorders. Eur J Clin Med. 2022;3(2):1-7.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. Leukocyte Adherence Inhibition Test to the assessment of Immunoreactivity Against Cow's Milk Proteins in Non—IgE-Mediated Gastrointestinal Food Allergy. Eur J Clin Med. 2022;3(2):38-43.
Olivier CE, Pinto DG, Teixeira APM, Santana JLS, Santos RAPGS, Lima RPS. Contribution of the Leukocyte Adherence Inhibition Test to the Diagnosis of Immunoreactivity against Cobalt. Asian J Immunol. 2023;6(1):174-184.
Tao R, Li R, Wang R. Dysbiosis of skin mycobiome in Atopic Dermatitis. Mycoses. 2022;65(3):285-293.
Ashman RB, Papadimitriou JM, Ott AK, Warmington JR. Antigens and immune responses in Candida albicans infection. Immunol Cell Biol. 1990;68(1):1-13.
Javad G, Taheri-Sarvtin M, Hedayati MT, Hajheydari Z, Yazdani J, Shokohi T. Evaluation of Candida Colonization and Specific Humoral Responses against Candida albicans in Patients with Atopic Dermatitis. BioMed Res Int. 2015:849206.
Faergemann J. Atopic Dermatitis and fungi. Clin Microbiol Rev. 2002;15(4):545-63.
Akiyama K., Yui Y, Shida T, Miyamoto T. Relationship between the results of skin, conjunctival and bronchial tests and RAST with Candida albicans in patients with asthma. Clin Allergy. 1981;11(4):343-51.
Qin Y, Zhang L, Xu Z, Zhang J, Jiang YY, Cao Y, et al. Innate immune cell response upon Candida albicans infection. Virulence. 2016;7(5):512-26.
Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity. 2001;15(6):985-95.
Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med. 2006; 203(6):1435-46.
Shirakawa T; Kusaka Y, Fujimura N, Goto S, Morimoto K. The existence of specific antibodies to cobalt in hard metal asthma. Clin Exp Allergy. 1988;18(5):451-460.Jutel M, Agache I, Zemelka-Wiacek M, Akdis M, Chivato T, Del Giacco S, Gajdanowicz P, et al. Nomenclature of allergic diseases and hypersensitivity reactions: Adapted to modern needs: An EAACI position paper. Allergy; 2023 Available:https://onlinelibrary.wiley.com/doi/epdf/10.1111/all.158
Olivier CE, Lima RPS, Pinto DG, Santos RAPG. The Plasma Preincubation with Papain Before the Assay Suggests that a Gell and Coombs Type II Reaction is Been Demonstrated by the Leukocyte Adherence Inhibition Test. Biomed J Sci. TechRes. 2021;36(3):28647-28655.
Thomson DMP. Assessment of immune status by the leukocyte adherence inhibition test. Academic Press: New York. 1982;p xvii:380.
Tong AW, Burger DR, Finke P, Barney C, Vandenbark AA, Vetto RM. Assessment of the mechanism of the leukocyte adherence inhibition test. Cancer Res. 1979;39(2): 597-603.
Fink A, Heller L, Eliraz A, Weisman Z, Miskin A, Schlezinger M, et al. Allergen-specific leukocyte adherence inhibition (LAI) assay: Sensitivity, specificity and mechanism. Immunol Lett. 1987;16(1): 65-70.
Halliday WJ, Maluish A, Miller S. Blocking and unblocking of cell-mediated anti-tumor Immunity in mice, as detected by the leucocyte adherence inhibition test. Cell Immunol. 1974;10(3): 467-475.
World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-4.