Delayed Skin Testing for Systemic Medications: Helpful or Not?

Abstract

Cutaneous adverse drug reactions collectively are delayed drug reactions such as morbilliform drug eruption and severe cutaneous adverse reactions (SCARs). Morbilliform drug eruption may wane over time, be the result of drug viral interactions, and be amenable to slow reintroduction or rechallenge, whereas SCARs are HLA class I restricted, T-cell–mediated reactions that demonstrate durable immunity and warrant lifelong avoidance. SCARs such as drug reaction with eosinophilia and systemic symptoms, Stevens-Johnson syndrome and toxic epidermal necrolysis, acute generalized exanthematous pustulosis, and generalized bullous fixed drug eruption often occur in the setting of multiple drugs dosed together. Collectively, they lead to significant morbidity, mortality, and drug safety concerns that could severely limit future treatment options. Currently, no single or combination of diagnostic tests for SCARs such as ex vivo or in vitro testing, in vivo (skin) testing, or other adjunctive tests such as HLA typing have 100% negative predictive value. In this “Controversies in Allergy Review” article, we review the current literature on delayed skin testing (patch and delayed prick/intradermal test) and critically assess the evidence base of its utility across different drugs and clinical phenotypes of delayed hypersensitivity reactions. Cutaneous adverse drug reactions collectively are delayed drug reactions such as morbilliform drug eruption and severe cutaneous adverse reactions (SCARs). Morbilliform drug eruption may wane over time, be the result of drug viral interactions, and be amenable to slow reintroduction or rechallenge, whereas SCARs are HLA class I restricted, T-cell–mediated reactions that demonstrate durable immunity and warrant lifelong avoidance. SCARs such as drug reaction with eosinophilia and systemic symptoms, Stevens-Johnson syndrome and toxic epidermal necrolysis, acute generalized exanthematous pustulosis, and generalized bullous fixed drug eruption often occur in the setting of multiple drugs dosed together. Collectively, they lead to significant morbidity, mortality, and drug safety concerns that could severely limit future treatment options. Currently, no single or combination of diagnostic tests for SCARs such as ex vivo or in vitro testing, in vivo (skin) testing, or other adjunctive tests such as HLA typing have 100% negative predictive value. In this “Controversies in Allergy Review” article, we review the current literature on delayed skin testing (patch and delayed prick/intradermal test) and critically assess the evidence base of its utility across different drugs and clinical phenotypes of delayed hypersensitivity reactions. According to a recently published classification of hypersensitivity, many cutaneous adverse drug reactions (CADRs) involve delayed hypersensitivity mechanisms.1Jutel M. Agache I. Zemelka-Wiacek M. Akdis M. Chivato T. Del Giacco S. et al.Nomenclature of allergic diseases and hypersensitivity reactions: adapted to modern needs: an EAACI position paper.Allergy. 2023; 78: 2851-2874Crossref PubMed Scopus (44) Google Scholar Delayed hypersensitivity is associated with both nonsevere CADRs and severe cutaneous adverse reactions (SCARs).2Peter J.G. Lehloenya R. Dlamini S. Risma K. White K.D. Konvinse K.C. et al.Severe delayed cutaneous and systemic reactions to drugs: a global perspective on the science and art of current practice.J Allergy Clin Immunol Pract. 2017; 5: 547-563Abstract Full Text Full Text PDF PubMed Scopus (109) Google Scholar,3Hung S.I. Mockenhaupt M. Blumenthal K.G. Abe R. Ueta M. Ingen-Housz-Oro S. et al.Severe cutaneous adverse reactions.Nat Rev Dis Primers. 2024; 10: 30Crossref PubMed Scopus (3) Google Scholar Skin tests (STs), sometimes referred to as in vivo testing, include patch tests (PTs), skin prick tests (SPTs), and intradermal tests (IDTs) with delayed readings. These are valuable tools for diagnosing delayed drug hypersensitivity. Their appearance can vary depending on an individual’s skin tone and pigment. Various examples of positive ST results are shown in Figures 1 and 2.4Lehloenya R.J. Phillips E.J. Pasieka H.B. Peter J. Recognizing drug hypersensitivity in pigmented skin.Immunol Allergy Clin North Am. 2022; 42: 219-238Abstract Full Text Full Text PDF Scopus (10) Google Scholar STs with delayed readings can help establish the causal relationship between a drug and a delayed CADR, as well as assess cross-reactivity between drugs and identify safe alternatives.5Phillips E.J. Bigliardi P. Bircher A.J. Broyles A. Chang Y.S. Chung W.H. et al.Controversies in drug allergy: testing for delayed reactions.J Allergy Clin Immunol. 2019; 143: 66-73Abstract Full Text Full Text PDF PubMed Scopus (150) Google Scholar Moreover, because they have a very high reproducibility in the long-term, they can contribute to identifying the culprit drug of the CADR.6Pinho A. Marta A. Coutinho I. Goncalo M. Long-term reproducibility of positive patch test reactions in patients with non-immediate cutaneous adverse drug reactions to antibiotics.Contact Dermatitis. 2017; 76: 204-209Crossref PubMed Scopus (29) Google Scholar In nonsevere CADRs such as morbilliform drug eruption (MDE), negative ST result (PT and/or SPT/IDT) in conjunction with shared patient decision making, drug challenge (DC) or drug provocation tests (DPTs) with the suspected drug, or a structurally similar (potentially cross-reactive) drug, may be offered if equally safe and efficacious alternatives are A. M. A. P. et position on drug provocation 2024; PubMed Scopus Google Scholar in severe drugs a be for reintroduction and if the of the the of drug provocation test the drug or a structurally drug be is a the of skin testing in and with A. M. A. P. et position on drug provocation 2024; PubMed Scopus Google A. Blumenthal K.G. Phillips E.J. R. White et allergy: a Allergy Clin Immunol. 2022; Full Text Full Text PDF PubMed Scopus Google Scholar to of in patients with a of SCARs patients with reactions to drugs in the setting of or of is with of published patients that challenge with to reactions is a safe to identify culprit and the R.J. Peter J.G. A. Phillips E.J. delayed drug can Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google R.J. T. T. A. S. et syndrome and drug reaction with eosinophilia and systemic on drug Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google for the the is the for treatment and of on this an decision can be the for lifelong and or of of drug and a drug to in allergic for are to the on and skin with in for and are on the test and between and with readings to 1 for tests or in patients for multiple readings in patch testing is that drugs a positive reaction and readings may to an of readings. of results to for to as et K. T. Bircher A. M. et of for diagnostic patch testing on Dermatitis. PubMed Scopus Google Scholar for drugs have in et S. J. A. and of in drug patch Dermatitis. PubMed Scopus Google Scholar and et A. J. A. Skin tests in the of cutaneous adverse drug reactions: a review and Dermatitis. 2022; PubMed Scopus Google Scholar and are in I. for of or are drugs to a in in the test be drugs patients because a of drugs are in of and/or in or delayed drug E.J. Bigliardi P. Bircher A.J. Broyles A. Chang Y.S. Chung W.H. et al.Controversies in drug allergy: testing for delayed reactions.J Allergy Clin Immunol. 2019; 143: 66-73Abstract Full Text Full Text PDF PubMed Scopus (150) Google intradermal negative ST results with delayed a challenge test can be A. M. A. P. et position on drug provocation 2024; PubMed Scopus Google of with negative delayed ST result with delayed and in negative ST results with delayed if on the of eruption if negative a drug in A. et patch test and test for fixed drug a Allergy Clin Immunol Pract. 2024; Full Text Full Text PDF Scopus Google in or in test results are bullous fixed drug if in can be A. et patch test and test for fixed drug a Allergy Clin Immunol Pract. 2024; Full Text Full Text PDF Scopus Google to A. M. et to the and safety of drug patch tests for the of severe cutaneous adverse drug PubMed Scopus Google P. M. et testing in severe cutaneous adverse drug Stevens-Johnson syndrome and toxic epidermal Dermatitis. PubMed Scopus Google with suspected drugs and depending on the A. M. et to the and safety of drug patch tests for the of severe cutaneous adverse drug PubMed Scopus Google Goncalo M. to in drug reaction with eosinophilia and systemic other Dermatitis. PubMed Scopus Google of A. M. et to the and safety of drug patch tests for the of severe cutaneous adverse drug PubMed Scopus Google A. A. T. A. drug intradermal tests to cross-reactivity and in 2019; PubMed Scopus Google with suspected drug and with drugs can be A. M. A. P. et position on drug provocation 2024; PubMed Scopus Google R.J. Peter J.G. A. Phillips E.J. delayed drug can Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google R.J. T. T. A. S. et syndrome and drug reaction with eosinophilia and systemic on drug Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google T. J. S. A. we a of drugs suspected as in drug reaction with eosinophilia and systemic of 2019; PubMed Scopus Google to the with the suspected to have a et testing and drug provocation tests in epidermal a Allergy Clin Immunol Pract. 2022; Full Text Full Text PDF PubMed Scopus (10) Google tests with a to negative predictive value. in a negative predictive value. of and they be drugs in can be the of the a of A. Goncalo M. Bircher A. of Dermatitis. for skin tests with drugs in the of cutaneous adverse drug Dermatitis. PubMed Scopus Google Scholar or K. A. M. J. P. for skin test in the of drug PubMed Scopus Google Scholar in A. A. Skin testing for and delayed hypersensitivity Allergy Clin North Am. 2022; 42: Full Text Full Text PDF PubMed Scopus Google Scholar and of the or drug and are often because a a T-cell–mediated In a drug may be to have skin to for and a may have a Phillips E.J. review of drug patch testing and for PubMed Scopus Google Scholar et S. J. A. and of in drug patch Dermatitis. PubMed Scopus Google Scholar that the of in drug in with of of the is that with drugs the of the to the of results across different drugs for or in the drug can be in to very high K. T. Bircher A. M. et of for diagnostic patch testing on Dermatitis. PubMed Scopus Google Goncalo M. to in drug reaction with eosinophilia and systemic other Dermatitis. PubMed Scopus Google Scholar the is in is to to a of in A. Goncalo M. Bircher A. of Dermatitis. for skin tests with drugs in the of cutaneous adverse drug Dermatitis. PubMed Scopus Google K. A. M. J. P. for skin test in the of drug PubMed Scopus Google Scholar In a be the and to the drug for drugs testing, a of negative is to result because many drugs have for patch testing, and is to be to and test the of a in patch testing for drugs of the and for and and for have in other A. J. A. Skin tests in the of cutaneous adverse drug reactions: a review and Dermatitis. 2022; PubMed Scopus Google Scholar in the the of the is to for a of to drug in the can be Skin testing for drug Scholar can be of a drug, in such as in or E.J. Bigliardi P. Bircher A.J. Broyles A. Chang Y.S. Chung W.H. et al.Controversies in drug allergy: testing for delayed reactions.J Allergy Clin Immunol. 2019; 143: 66-73Abstract Full Text Full Text PDF PubMed Scopus (150) Google A. Goncalo M. Bircher A. of Dermatitis. for skin tests with drugs in the of cutaneous adverse drug Dermatitis. PubMed Scopus Google K. A. M. J. P. for skin test in the of drug PubMed Scopus Google Scholar are for hypersensitivity reactions to delayed positive to have in such as drug reaction with eosinophilia and systemic and acute generalized exanthematous A. M. et to the and safety of drug patch tests for the of severe cutaneous adverse drug PubMed Scopus Google A. A. Skin testing for and delayed hypersensitivity Allergy Clin North Am. 2022; 42: Full Text Full Text PDF PubMed Scopus Google Scholar delayed positive reaction in an is and the 1 or the A. Goncalo M. Bircher A. of Dermatitis. for skin tests with drugs in the of cutaneous adverse drug Dermatitis. PubMed Scopus Google K. A. M. J. P. for skin test in the of drug PubMed Scopus Google Scholar have of delayed reactions in drug prick tests with drugs for hypersensitivity testing A. M. et to the and safety of drug patch tests for the of severe cutaneous adverse drug PubMed Scopus Google A. A. Skin testing for and delayed hypersensitivity Allergy Clin North Am. 2022; 42: Full Text Full Text PDF PubMed Scopus Google Scholar for delayed prick and intradermal testing are in the delayed testing, the utility and of prick testing have with utility for clinical phenotypes for delayed drug prick and intradermal A. Blumenthal K.G. Phillips E.J. R. White et allergy: a Allergy Clin Immunol. 2022; Full Text Full Text PDF PubMed Scopus Google A. A. Skin testing for and delayed hypersensitivity Allergy Clin North Am. 2022; 42: Full Text Full Text PDF PubMed Scopus Google A. M. S. S. et tests with drugs: an to PubMed Scopus Google K. M. A. et test for drugs an Allergy position paper.Allergy. PubMed Scopus Google drugs can be and other other and K.C. R. I. et is associated with drug reaction with eosinophilia and systemic Allergy Clin Immunol. 2019; Full Text Full Text PDF PubMed Scopus Google and and other A. I. K. A. S. et for diagnosing and 76: PubMed Scopus Google for delayed S. S. P. M. A. K. et reactions to EAACI position paper.Allergy. 2024; Scopus (3) Google drugs can be in a the of is with in for and the results can vary between drug et A. M. S. S. et tests with drugs: an to PubMed Scopus Google Scholar an to result across and According to this the for intradermal on the or is a in are a of or 1 of the with a A. M. S. S. et tests with drugs: an to PubMed Scopus Google Scholar of the be and result is positive if the is or to with such as for results have to be R. Phillips E.J. for intradermal skin testing and challenge in patients as Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google Scholar In delayed drug hypersensitivity can positive results on delayed readings test results have as negative or shown an is that the test results negative demonstrate a delayed 1 to Skin testing for drug Scholar delayed is and the and may be in a severe may a delayed for results on readings and negative have for many drugs associated with A. Goncalo M. Bircher A. of Dermatitis. for skin tests with drugs in the of cutaneous adverse drug Dermatitis. PubMed Scopus Google A. A. Skin testing for and delayed hypersensitivity Allergy Clin North Am. 2022; 42: Full Text Full Text PDF PubMed Scopus Google K. M. A. et test for drugs an Allergy position paper.Allergy. 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Full Text Full Text PDF PubMed Scopus Google Scholar is a and the of drug to the of clinical and of the drug to testing that be testing and delayed prick/intradermal testing are the because they can be in the setting the of or drugs for intradermal testing or drugs in a for for patch utility skin testing is that can help the culprit the for to R.J. Peter J.G. A. Phillips E.J. delayed drug can Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google Scholar alternatives the of the as well as with the to the and Skin testing may of multiple drug hypersensitivity to with the culprit drug on a clinical utility of skin testing is across clinical phenotypes or drugs or results are they have shown to be and that they are durable over E.J. Bigliardi P. Bircher A.J. Broyles A. Chang Y.S. Chung W.H. et al.Controversies in drug allergy: testing for delayed reactions.J Allergy Clin Immunol. 2019; 143: 66-73Abstract Full Text Full Text PDF PubMed Scopus (150) Google A. A. et of drug reaction with eosinophilia and systemic Allergy Clin Immunol Pract. 2024; Full Text Full Text PDF Scopus Google E.J. of patch testing in patients with hypersensitivity associated with PubMed Scopus Google Scholar we clinical phenotypes evidence that skin testing may have utility in clinical E.J. Bigliardi P. Bircher A.J. Broyles A. Chang Y.S. Chung W.H. et al.Controversies in drug allergy: testing for delayed reactions.J Allergy Clin Immunol. 2019; 143: 66-73Abstract Full Text Full Text PDF PubMed Scopus (150) Google Scholar for no clinical drug hypersensitivity or drug a negative ST result its in the delayed skin testing to drugs is and if the result is utility in identifying the culprit drug of the or a In the of an for diagnostic to and and patient According to the recently published for or A. M. A. P. et position on drug provocation 2024; PubMed Scopus Google Scholar drug STs are in of because the challenge is the is as an that is of the drug and or systemic treatment to include of the bullous pustulosis, generalized generalized in and or severe of to skin or patch testing for drug provocation or the negative predictive of such testing is the decision to challenge a shared with the patient the of the treatment in the of a reaction testing for in severe are the results are negative and the drug in with delayed readings are are associated with adverse have as for across drug such as A. M. A. Bircher A.J. K. et a of hypersensitivity to an EAACI position paper.Allergy. PubMed Scopus Google Scholar A. I. K. A. S. et for diagnosing and 76: PubMed Scopus Google Scholar A. S. Blumenthal K. et for the and of drug Allergy Clin Immunol Pract. Full Text Full Text PDF PubMed Scopus Google Scholar A. S. Blumenthal K. et for the and of drug Allergy Clin Immunol Pract. 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