Reclassifying anaphylaxis to neuromuscular blocking agents based on the presumed Patho-Mechanism: IgE-Mediated, pharmacological adverse reaction or “innate hypersensitivity”?

International Journal of Molecular Sciences

Volumn 18, Issue 6, 2017, Pages

  Spoerl, David ^a   Nigolian, Haig ^a   Czarnetzki, Christoph ^a   Harr, Thomas ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Adverse drug reaction; Drug allergy; Histamine; Mas related G protein coupled receptor member X2; Mast cell; Perioperative anaphylaxis; Pseudo allergy

Indexed keywords

ABACAVIR; ALLOPURINOL; BENZYLISOQUINOLINE DERIVATIVE; CARBAMAZEPINE; IMMUNOGLOBULIN E; LEUKOCYTE ANTIGEN; NEUROMUSCULAR BLOCKING AGENT; PROTEINASE ACTIVATED RECEPTOR; SUXAMETHONIUM; TOLL LIKE RECEPTOR; VANCOMYCIN; G PROTEIN COUPLED RECEPTOR; MRGPRX2 PROTEIN, HUMAN; NERVE PROTEIN; NEUROPEPTIDE RECEPTOR;

ALLERGY; DEGRANULATION; GENE; HYPERSENSITIVITY; INNATE IMMUNITY; MAST CELL; MRGPRX2 GENE; REVIEW; SKIN TEST; ADVERSE DRUG REACTION; ANAPHYLAXIS; COMPLICATION; CROSS REACTION; DRUG HYPERSENSITIVITY; HUMAN; IMMEDIATE TYPE HYPERSENSITIVITY; IMMUNOLOGY; METABOLISM; PROCEDURES;

ANAPHYLAXIS; CROSS REACTIONS; DRUG HYPERSENSITIVITY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; HUMANS; HYPERSENSITIVITY, IMMEDIATE; IMMUNITY, INNATE; IMMUNOGLOBULIN E; MAST CELLS; NERVE TISSUE PROTEINS; NEUROMUSCULAR BLOCKING AGENTS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; SKIN TESTS;

EID: 85020401121     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18061223     Document Type: Review

References (71)

1. Ewan, P.W., Dugué, P., Mirakian, R., Dixon, T.A., Harper, J.N., Nasser, S.M. BSACI BSACI guidelines for the investigation of suspected anaphylaxis during general anaesthesia. Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 2010, 40, 15-31.
2. Mertes, P.M., Laxenaire, M.-C., Alla, F. Groupe d’Etudes des Réactions Anaphylactoïdes Peranesthésiques Anaphylactic and anaphylactoid reactions occurring during anesthesia in France in 1999-2000. Anesthesiology 2003, 99, 536-545.
3. Farnam, K., Chang, C., Teuber, S., Gershwin, M.E. Nonallergic drug hypersensitivity reactions. Int. Arch. Allergy Immunol. 2012, 159, 327-345.
4. Czech, W., Schöpf, E., Kapp, A. Release of sulfidoleukotrienes in vitro: Its relevance in the diagnosis of pseudoallergy to acetylsalicylic acid. Inflamm. Res. Off. J. Eur. Histamine Res. Soc. 1995, 44, 291-295.
5. Mali, S. Anaphylaxis during the perioperative period. Anesth. Essays Res. 2012, 6, 124-133.
6. Johansson, S.G., Hourihane, J.O., Bousquet, J., Bruijnzeel-Koomen, C., Dreborg, S., Haahtela, T., Kowalski, M.L., Mygind, N., Ring, J., van Cauwenberge, P., et al. EAACI (the European Academy of Allergology and Cinical Immunology) nomenclature task force A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 2001, 56, 813-824.
7. De Pater, G.H., Florvaag, E., Johansson, S.G.O., Irgens, Å., Petersen, M.N.H., Guttormsen, A.B. Six years without pholcodine, Norwegians are significantly less IgE-sensitized and clinically more tolerant to neuromuscular blocking agents. Allergy 2016, doi:10.1111/all.13081.
8. Brusch, A.M., Clarke, R.C., Platt, P.R., Phillips, E.J. Exploring the link between pholcodine exposure and neuromuscular blocking agent anaphylaxis. Br. J. Clin. Pharmacol. 2014, 78, 14-23.
9. Krøigaard, M., Garvey, L.H., Menné, T., Husum, B. Allergic reactions in anaesthesia: Are suspected causes confirmed on subsequent testing? Br. J. Anaesth. 2005, 95, 468-471.
10. Celik, G., Pichler, W., Adkinson, N.F. Drug Allergy. In Middleton’s Allergy: Principles & Practice, Adkinson, N.F., Middleton, E., Eds., Mosby/Elsevier: Philadelphia, PA, USA, 2009.
11. McNeil, B.D., Pundir, P., Meeker, S., Han, L., Undem, B.J., Kulka, M., Dong, X. Identification of a mast-cellspecific receptor crucial for pseudo-allergic drug reactions. Nature 2015, 519, 237-241.
12. Ebo, D.G., Fisher, M.M., Hagendorens, M.M., Bridts, C.H., Stevens, W.J. Anaphylaxis during anaesthesia: Diagnostic approach. Allergy 2007, 62, 471-487.
13. Dewachter, P., Mouton-Faivre, C., Emala, C.W. Anaphylaxis and anesthesia: Controversies and new insights. Anesthesiology 2009, 111, 1141-1150.
14. Rawlins, M., Thompson, J. Pathogenesis of adverse drug reactions. In Textbook of Adverse Drug Reactions, Davies, D.M., Ed., Oxford University Press: Oxford, UK, New York, NY, USA, 1977.
15. Waller, D.G. Allergy, pseudo-allergy and non-allergy. Br. J. Clin. Pharmacol. 2011, 71, 637-638.
16. Edwards, I.R., Aronson, J.K. Adverse drug reactions: Definitions, diagnosis, and management. Lancet Lond. Engl. 2000, 356, 1255-1259.
17. Pichler, W. Drug allergy: Classification and clinical features. In UpToDate, Adkinson, N.F., Feldweg, A.M., Eds., UpToDate: Waltham, MA, USA, 2016.
18. Yun, J., Mattsson, J., Schnyder, K., Fontana, S., Largiadèr, C.R., Pichler, W.J., Yerly, D. Allopurinol hypersensitivity is primarily mediated by dose-dependent oxypurinol-specific T cell response. Clin. Exp. Allergy 2013, 43, 1246-1255.
19. Stamp, L.K., Taylor, W.J., Jones, P.B., Dockerty, J.L., Drake, J., Frampton, C., Dalbeth, N. Starting dose is a risk factor for allopurinol hypersensitivity syndrome: A proposed safe starting dose of allopurinol. Arthritis Rheum. 2012, 64, 2529-2536.
20. Hennino, A., Bérard, F., Guillot, I., Saad, N., Rozières, A., Nicolas, J.-F. Pathophysiology of urticaria. Clin. Rev. Allergy Immunol. 2006, 30, 3-11.
21. D’Andrea, M.R., Rogahn, C.J., Andrade-Gordon, P. Localization of protease-activated receptors-1 and-2 in human mast cells: Indications for an amplified mast cell degranulation cascade. Biotech. Histochem. 2000, 75, 85-90.
22. Subramanian, H., Gupta, K., Ali, H. Roles of Mas-related G protein-coupled receptor X2 on mast cellmediated host defense, pseudoallergic drug reactions, and chronic inflammatory diseases. J. Allergy Clin. Immunol. 2016, 138, 700-710.
23. Marshall, J.S. Mast-cell responses to pathogens. Nat. Rev. Immunol. 2004, 4, 787-799.
24. Zuberbier, T., Pfrommer, C., Specht, K., Vieths, S., Bastl-Borrmann, R., Worm, M., Henz, B.M. Aromatic components of food as novel eliciting factors of pseudoallergic reactions in chronic urticaria. J. Allergy Clin. Immunol. 2002, 109, 343-348.
25. Bonadonna, P., Pagani, M., Aberer, W., Bilò, M.B., Brockow, K., Oude Elberink, H., Garvey, L., Mosbech, H., Romano, A., Zanotti, R., et al. Drug hypersensitivity in clonal mast cell disorders: ENDA/EAACI position paper. Allergy 2015, 70, 755-763.
26. Zuberbier, T., Asero, R., Bindslev-Jensen, C., Walter Canonica, G., Church, M.K., Giménez-Arnau, A.M., Grattan, C.E.H., Kapp, A., Maurer, M., Merk, H.F., et al. Dermatology Section of the European Academy of Allergology and Clinical Immunology, Global Allergy and Asthma European Network, European Dermatology Forum, World Allergy Organization EAACI/GA (2) LEN/EDF/WAO guideline: Management of urticaria. Allergy 2009, 64, 1427-1443.
27. Zuberbier, T., Chantraine-Hess, S., Hartmann, K., Czarnetzki, B.M. Pseudoallergen-free diet in the treatment of chronic urticaria. A prospective study. Acta Derm. Venereol. 1995, 75, 484-487.
28. Dewachter, P., Castells, M.C., Hepner, D.L., Mouton-Faivre, C. Perioperative management of patients with mastocytosis. Anesthesiology 2014, 120, 753-759.
29. Baldo, B.A., Fisher, M.M., Pham, N.H. On the origin and specificity of antibodies to neuromuscular blocking (muscle relaxant) drugs: An immunochemical perspective. Clin. Exp. Allergy 2009, 39, 325-344.
30. Moss, J. Muscle relaxants and histamine release. Acta Anaesthesiol. Scand. Suppl. 1995, 106, 7-12.
31. Claudius, C., Garvey, L.H., Viby-Mogensen, J. The undesirable effects of neuromuscular blocking drugs. Anaesthesia 2009, 64 (Suppl. S1), 10-21.
32. Florvaag, E., Johansson, S.G.O., Irgens, Å., de Pater, G.H. IgE-sensitization to the cough suppressant pholcodine and the effects of its withdrawal from the Norwegian market. Allergy 2011, 66, 955-960.
33. Florvaag, E., Johansson, S.G.O., Oman, H., Harboe, T., Nopp, A. Pholcodine stimulates a dramatic increase of IgE in IgE-sensitized individuals. A pilot study. Allergy 2006, 61, 49-55.
34. Kaminsky, E.B., Kaul, V., Paschall, J., Church, D.M., Bunke, B., Kunig, D., Moreno-De-Luca, D., Moreno-De-Luca, A., Mulle, J.G., Warren, S.T., et al. An evidence-based approach to establish the functional and clinical significance of copy number variants in intellectual and developmental disabilities. Genet. Med. 2011, 13, 777-784.
35. Miller, D.T., Adam, M.P., Aradhya, S., Biesecker, L.G., Brothman, A.R., Carter, N.P., Church, D.M., Crolla, J.A., Eichler, E.E., Epstein, C.J., et al. Consensus statement: Chromosomal microarray is a first-tier clinical diagnostic test for individuals with developmental disabilities or congenital anomalies. Am. J. Hum. Genet. 2010, 86, 749-764.
36. Yang, S., Liu, Y., Lin, A.A., Cavalli-Sforza, L.L., Zhao, Z., Su, B. Adaptive evolution of MRGX2, a human sensory neuron specific gene involved in nociception. Gene 2005, 352, 30-35.
37. Nel, L., Eren, E. Peri-operative anaphylaxis. Br. J. Clin. Pharmacol. 2011, 71, 647-658.
38. Galvão, V.R., Giavina-Bianchi, P., Castells, M. Perioperative anaphylaxis. Curr. Allergy Asthma Rep. 2014, 14, 452.
39. Laxenaire, M.C., Mertes, P.M. Groupe d’Etudes des Réactions Anaphylactoïdes Peranesthésiques Anaphylaxis during anaesthesia. Results of a two-year survey in France. Br. J. Anaesth. 2001, 87, 549-558.
40. Fisher, M.M., Munro, I. Life-threatening anaphylactoid reactions to muscle relaxants. Anesth. Anal. 1983, 62, 559-564.
41. Spoerl, D., D’Incau, S., Roux-Lombard, P., Harr, T., Czarnetzki, C. Non-IgE-Dependent Hypersensitivity to Rocuronium Reversed by Sugammadex: Report of Three Cases and Hypothesis on the Underlying Mechanism. Int. Arch. Allergy Immunol. 2016, 169, 256-262.
42. Fisher, M.M., Merefield, D., Baldo, B. Failure to prevent an anaphylactic reaction to a second neuromuscular blocking drug during anaesthesia. Br. J. Anaesth. 1999, 82, 770-773.
43. Leysen, J., Uyttebroek, A., Sabato, V., Bridts, C.H., de Clerck, L.S., Ebo, D.G. Predictive value of allergy tests for neuromuscular blocking agents: Tackling an unmet need. Clin. Exp. Allergy 2014, 44, 1069-1075.
44. Hagau, N., Gherman-Ionica, N., Sfichi, M., Petrisor, C. Threshold for basophil activation test positivity in neuromuscular blocking agents hypersensitivity reactions. Allergy Asthma Clin. Immunol. 2013, 9, 42.
45. Dong, S.W., Mertes, P.M., Petitpain, N., Hasdenteufel, F., Malinovsky, J.M., GERAP Hypersensitivity reactions during anesthesia. Results from the ninth French survey (2005-2007). Minerva Anestesiol. 2012, 78, 868-878.
46. Mertes, P.-M., Laxenaire, M.-C. GERAP (Anaphylactic and anaphylactoid reactions occurring during anaesthesia in France. Seventh epidemiologic survey (January 2001-December 2002)). Ann. Fr. Anesth. Reanim. 2004, 23, 1133-1143.
47. Harboe, T., Guttormsen, A.B., Irgens, A., Dybendal, T., Florvaag, E. Anaphylaxis during anesthesia in Norway: A 6-year single-center follow-up study. Anesthesiology 2005, 102, 897-903.
48. Karila, C., Brunet-Langot, D., Labbez, F., Jacqmarcq, O., Ponvert, C., Paupe, J., Scheinmann, P., de Blic, J. Anaphylaxis during anesthesia: Results of a 12-year survey at a French pediatric center. Allergy 2005, 60, 828-834.
49. Kvedariene, V., Kamey, S., Ryckwaert, Y., Rongier, M., Bousquet, J., Demoly, P., Arnoux, B. Diagnosis of neuromuscular blocking agent hypersensitivity reactions using cytofluorimetric analysis of basophils. Allergy 2006, 61, 311-315.
50. Chong, Y.Y., Caballero, M.R., Lukawska, J., Dugué, P. Anaphylaxis during general anaesthesia: One-year survey from a British allergy clinic. Singap. Med. J. 2008, 49, 483-487.
51. Laroche, D., Chollet-Martin, S., Léturgie, P., Malzac, L., Vergnaud, M.-C., Neukirch, C., Venemalm, L., Guéant, J.-L., Roland, P.N. Evaluation of a new routine diagnostic test for immunoglobulin E sensitization to neuromuscular blocking agents. Anesthesiology 2011, 114, 91-97.
52. Aalberse, R.C., Kleine Budde, I., Mulder, M., Stapel, S.O., Paulij, W., Leynadier, F., Hollmann, M.W. Differentiating the cellular and humoral components of neuromuscular blocking agent-induced anaphylactic reactions in patients undergoing anaesthesia. Br. J. Anaesth. 2011, 106, 665-674.
53. Ramirez, L.F., Pereira, A., Chiriac, A.M., Bonnet-Boyer, M.-C., Demoly, P. Negative predictive value of skin tests to neuromuscular blocking agents. Allergy 2012, 67, 439-441.
54. Antunes, J., Kochuyt, A.-M., Ceuppens, J.L. Perioperative allergic reactions: Experience in a Flemish referral centre. Allergol. Immunopathol. Madr. 2014, 42, 348-354.
55. Krishna, M.T., York, M., Chin, T., Gnanakumaran, G., Heslegrave, J., Derbridge, C., Huissoon, A., Diwakar, L., Eren, E., Crossman, R.J., et al. Multi-centre retrospective analysis of anaphylaxis during general anaesthesia in the United Kingdom: Aetiology and diagnostic performance of acute serum tryptase. Clin. Exp. Immunol. 2014, 178, 399-404.
56. Soetens, F.M., Smolders, F.J., Meeuwis, H.C., Van der Donck, A.G., van der Aa, P.H., De Vel, M.A., Vanhoof, M.J., Soetens, M.A. Intradermal skin testing in the investigation of suspected anaphylactic reactions during anaesthesia—A retrospective survey. Acta Anaesthesiol. Belg. 2003, 54, 59-63.
57. Hagau, N., Gherman, N., Cocis, M., Petrisor, C. Antibiotic-induced immediate type hypersensitivity is a risk factor for positive allergy skin tests for neuromuscular blocking agents. Allergol. Int. 2016, 65, 52-55.
58. Berg, C.M., Heier, T., Wilhelmsen, V., Florvaag, E. Rocuronium and cisatracurium-positive skin tests in non-allergic volunteers: Determination of drug concentration thresholds using a dilution titration technique. Acta Anaesthesiol. Scand. 2003, 47, 576-582.
59. Reddy, J.I., Cooke, P.J., van Schalkwyk, J.M., Hannam, J.A., Fitzharris, P., Mitchell, S.J. Anaphylaxis is more common with rocuronium and succinylcholine than with atracurium. Anesthesiology 2015, 122, 39-45.
60. Veien, M., Szlam, F., Holden, J.T., Yamaguchi, K., Denson, D.D., Levy, J.H. Mechanisms of nonimmunological histamine and tryptase release from human cutaneous mast cells. Anesthesiology 2000, 92, 1074-1081.
61. Marone, G., Stellato, C., Mastronardi, P., Mazzarella, B. Mechanisms of activation of human mast cells and basophils by general anesthetic drugs. Ann. Fr. Anesth. Reanim. 1993, 12, 116-125.
62. Uyttebroek, A.P., Sabato, V., Leysen, J., Bridts, C.H., De Clerck, L.S., Ebo, D.G. Flowcytometric diagnosis of atracurium-induced anaphylaxis. Allergy 2014, 69, 1324-1332.
63. Leysen, J., de Witte, L., Sabato, V., Faber, M., Hagendorens, M., Bridts, C., de Clerck, L., Ebo, D. IgEmediated allergy to pholcodine and cross-reactivity to neuromuscular blocking agents: Lessons from flow cytometry. Cytom. B Clin. Cytom. 2013, 84, 65-70.
64. Fisher, M.M., Baldo, B.A. Immunoassays in the diagnosis of anaphylaxis to neuromuscular blocking drugs: The value of morphine for the detection of IgE antibodies in allergic subjects. Anaesth. Intensive Care 2000, 28, 167-170.
65. Decuyper, I.I., Ebo, D.G., Uyttebroek, A.P., Hagendorens, M.M., Faber, M.A., Bridts, C.H., de Clerck, L.S., Sabato, V. Quantification of specific IgE antibodies in immediate drug hypersensitivity: More shortcomings than potentials? Clin. Chim. Acta 2016, 460, 184-189.
66. Baldo, B.A., Fisher, M.M. Substituted ammonium ions as allergenic determinants in drug allergy. Nature 1983, 306, 262-264.
67. Ebo, D.G., Bridts, C.H., Hagendorens, M.M., Mertens, C.H., de Clerck, L.S., Stevens, W.J. Flow-assisted diagnostic management of anaphylaxis from rocuronium bromide. Allergy 2006, 61, 935-939.
68. Sabato, V., van Gasse, A., Cop, N., Claesen, K., Decuyper, I.I., Faber, M.A., Bridts, C., Mertens, C., Hagendorens, M., de Clerck, L., et al. The Mas-Related G Protein-Coupled Receptor MRGPRX2 Is Expressed on Human Basophils and up-Regulated upon Activation, AAAAI, Atlanta, GA, USA, 3-6 March 2017, Abstract 536.
69. Johansson, S.G.O., Oman, H., Degerbeck, F., Tunelli, J., Florvaag, E., Nopp, A. Anaphylaxis to atracurium— A non-QAI-dependent reaction? Acta Anaesthesiol. Scand. 2012, 56, 262-263.
70. Uyttebroek, A.P., Sabato, V., Bridts, C.H., De Clerck, L.S., Ebo, D.G. Immunoglobulin E antibodies to atracurium: A new diagnostic tool? Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 2015, 45, 485-487.
71. Naguib, M., Samarkandi, A.H., Bakhamees, H.S., Magboul, M.A., El-Bakry, A.K. Histamine-release haemodynamic changes produced by rocuronium, vecuronium, mivacurium, atracurium and tubocurarine. Br. J. Anaesth. 1995, 75, 588-592.