Severe cutaneous adverse reactions induced by targeted anticancer therapies and immunotherapies

Figures & data

Figure 1 Fatal toxic epidermal necrolysis after cetuximab treatment for 8 weeks.

Notes: A 74-year-old man who had moderately differentiated metastatic colon adenocarcinoma presented diffuse erythematous plaques with dusky red centers on trunk and extremities after treatment with cetuximab for 8 weeks. The skin rashes were confluent and formed large blisters or skin detachments involving more than 70% of the body surface area.

Figure 2 Drug rash with eosinophilia and systemic symptoms after erlotinib treatment for 4 weeks.

Notes: A 60-year-old woman with EGFR-mutant metastatic lung adenocarcinoma treated with erlotinib for 4 weeks. She developed generalized infiltrative exanthema on trunk and limbs accompanied by fever, acute liver failure, coagulopathy, and leukocytosis with eosinophilia. Further lymphocyte activation testing confirmed a hypersensitivity reaction to erlotinib.

Table 1 Targeted anticancer therapies and immunotherapies-induced severe cutaneous adverse reactions (n=73)

Drug class	Agent	Classification	SJS (n=29)	SJS/TEN (n=4)	TEN (n=21)	DRESS/DIHS* (n=9)	AGEP* (n=11)	Total (n=73)	Latency, median (range)	Biopsy proved	DIF/IIF	Mortality	Tumor response	References
EGFR inhibitor	Afatinib	Monoclonal antibody to EGFR	2	0	0	0	0	2	62 (60–64)	2	1	0	PR:1, U:1	^Citation30, ^Citation110
	Cetuximab	Monoclonal antibody to EGFR	1	1	2	0	0	4	16 (5–45)	1	1	1	R:1, U:3	^Citation6, ^Citation104, ^Citation111, ^Citation112
	Erlotinib	TKI specific to EGFR	1	0	0	0	0	1	8 (8)	0	0	0	U:1	^Citation26
	Gefitinib	TKI specific to EGFR	0	0	2	0	2	4	8 (7–10)	2	0	1	PR:1, U:3	^Citation92, ^Citation113, ^Citation114
	Panitumumab	Monoclonal antibody to EGFR	1	0	0	0	0	1	8 (8)	0	0	0	U:1	^Citation112
	Vandetanib	Less specific multikinase inhibitors	0	1	1	0	0	2	21 (21)	2	0	0	U:2	^Citation115, ^Citation116
KIT and BCR-ABL inhibitors	Imatinib	KIT, BCR-ABL, PDGFR inhibitors	12	0	0	4	4	20	46 (8–240)	12	2	1	CR:1, PD:1, Rev:2, U:16	^Citation40^–^Citation44, ^Citation88^–^Citation91, ^Citation117^–^Citation126
Antiangiogenic agents	Sorafenib	Nonselective antiangiogenesis multikinase agents	2	0	1	0	3	6	17 (2–30)	4	0	0	U:6	^Citation51, ^Citation55, ^Citation127^–^Citation130
Proteasome	Bortezomib	—	1	0	1	1	0	3	49 (42–56)	1	0	1	CR:1, PR:1, U:1	^Citation131^–^Citation133
CD20	Rituximab	Monoclonal antibody to CD20	2	2	1	0	0	5	14 (14–56)	2	1	2	PD:1, U:4	^Citation63, ^Citation134^–^Citation136
CD30	Brentuximab vedotin	CD30	1	0	1	0	0	2	7 (7)	1	0	1	U:2	^Citation137, ^Citation138
RAF inhibitors	Vemurafenib	BRAF (V600E) inhibitors	1	0	6	3*	1*	10	23 (8–42)	9	1	3	CR:1, PR:1, PD:1, U:7	^Citation12, ^Citation14, ^Citation68, ^Citation70, ^Citation139^–^Citation144
Immunomodulators	Aldesleukin	Recombinant IL2	0	0	2	0	0	2	5.5 (4–7)	1	0	1	U:2	^Citation76, ^Citation77
	Denileukin	Recombinant IL2 and diphtheria toxin	0	0	1	0	0	1	91 (91)	1	0	1	U:1	^Citation75
	Ipilimumab	CTLA4 inhibitors	1	0	1	1	1	4	22.8 (14–35)	3	0	0	PR:1, U:3	^Citation82^–^Citation84, ^145
	Nivolumab	PD1 inhibitors	0	0	2	0	0	2	64.5 (39–90)	2	2	2	U:2	^Citation16, ^Citation79
	Pembrolizumab	PD1 inhibitors	4	0	0	0	0	4	83.5 (7–140)	2	0	0	U:2, SD:1, PD:1	^Citation80, ^Citation81, ^Citation85

Note:

* One patient presented as DRESS and AGEP overlapping.

Abbreviations: AGEP, acute generalized exanthematous pustulosis; CR, complete remission; DIF, direct immunofluorescence; DIHS, drug-induced hypersensitivity syndrome; DRESS, drug rash with eosinophilia and systemic symptoms; IIF, indirect immunofluorescence; IL-2, interleukin-2; PD, progressive disease; PR, partial remission; R, recurrence; Rev, reversion to second chronic-phase chronic myelogenous leukemia; SCAR, severe cutaneous adverse reaction; SD, stable disease; SJS, Stevens–Johnson syndrome; TEN, toxic epidermal necrolysis; U, unknown.

Table 2 Tolerability follow-up for rechallenge or alternatives in patients with targeted anticancer therapies and immunotherapyinduced severe cutaneous adverse reactions (n=25)

Agent	Phenotype	Rechallenge	Tolerability to other drugs	Reference
Afatinib	SJS	Not reported	Erlotinib (liver damage); gefitinib (liver damage)	^Citation30
Aldesleukin	TEN	Recurrent with diffuse erythema and punctuated lesions over left forearm		^Citation76
Cetuximab	SJS	Not reported	Panitumumab (SJS/TEN)	^Citation112
Denileukin	TEN	Recurrent with extensive erythema and edema with flaccid bulla, and denudation was apparent on flanks, thighs, and arms		^Citation75
Erlotinib	SJS	Recurrent with continued erythematous and congested eruption on the face		^Citation26
Gefitinib	TEN	Not reported	Icotinib (tolerance)	^Citation114
Gefitinib	AGEP	Recurrent with few pustules on previous skin lesion, but tolerated with continuation		^Citation92
Imatinib	SJS	Not reported	Dasatinib (possible cross-reactivity, but taking sulfamethoxazole–trimethoprim at the same time); nilotinib (tolerance)	^Citation117
Imatinib	SJS	Recurrent with lesions flared up at lower doses	Dasatinib (tolerance)	^Citation118
Imatinib	SJS	Recurrent with perioral pruritic eruption after reinitiation at a lower dose of 200 mg/day, but then tolerated with slow titration (100–300 mg/day) with 100 mg together with prednisolone (1 mg/kg)	Not reported	^Citation40
Imatinib	SJS	Tolerance with slow titration from 100 mg/day gradually escalated to 400 mg/day	Not reported	^Citation41
Imatinib	SJS	Tolerance with slow titration from 100 mg/day and prednisolone 30–400 mg/day, with continuation of prednisolone at 10 mg/day	Not reported	^Citation42
Imatinib	SJS	Recurrent with pruritic eruption at a lower dose of 300 mg/day, then tolerated after adding prednisolone at 30 mg/day with gradual tapering		^Citation43
Imatinib	SJS	Recurrent with multiple pruritic vesicles and bullae suddenly appeared after single-dose 600 mg/day	Not reported	^Citation89
Imatinib	SJS	Recurrent with palpebral and labial edema with generalized body rash after 1-day rechallenge	Not reported	^Citation123
Imatinib	DRESS	Recurrent erythematous skin rashes developed in 12 hours		^Citation124
Imatinib	DRESS	Recurrent with periorbital edema, itching over face, and eosinophilia after taking 50% dose (200 mg); however, tolerated with combination of low-dose imatinib and oral steroid		^Citation44
Imatinib	DRESS		Nilotinib (tolerance)	^Citation88
Imatinib	AGEP	Recurrent with urticaria		^Citation90
Ipilimumab	AGEP	Skin rashes got worse after second infusion		^Citation83
Sorafenib	SJS	Recurrent with pruritic erythematous eruptions and high fever	Not reported	^Citation127
Sorafenib	AGEP	Recurrent grouped pustules over the site close to previous skin lesion		^Citation129
Vemurafenib	SJS	Recurrent with rash and fever after taking 50% dose (480 mg) once, but tolerated with a program of desensitization with dexamethasone	Not reported	^Citation13
Vemurafenib	TEN	Not reported	Lymphocyte transformation test positive for vemurafenib with cross-reactivity to dabrafenib and sulfamethoxazole, but negative for trametinib	^Citation14
Vemurafenib	TEN	Not reported	Dabrafenib (tolerance) with gradual escalation	^Citation70

Abbreviations: AGEP, acute generalized exanthematous pustulosis; DRESS, drug rash with eosinophilia and systemic symptoms; SJS, Stevens–Johnson syndrome; TEN, toxic epidermal necrolysis.

Table 3 Mortality in severe cutaneous adverse reactions related to targeted anticancer therapies and immunotherapies (n=14)

Agent	Phenotype	Age/sex	Underlying disease	Cause of death	Latency	Reference
Cetuximab	TEN	74/male	Adenocarcinoma of the sigmoid colon with hepatic metastasis	Pneumonia with renal/respiratory failure	14 days	^Citation6
Gefitinib	TEN	U/U	Non-small-cell lung cancer with leptomeningeal metastases	Systemic lung cancer progression	21 days	^Citation113
Imatinib	SJS	52/male	Chronic myeloid leukemia	Acute graft-versus-host disease of the gut	2 months	^Citation121
Bortezomib	TEN	61/male	IgG multiple myeloma	Multiorgan failure	4 days	^Citation131
Brentuximab vedotin	TEN	22/male	Anaplastic large-cell lymphoma, stage IIIA	Disease progression of lymphoma	20 days	^Citation138
Rituximab	SJS	36/male	Follicular non-Hodgkin’s lymphoma	Disease progression of lymphoma with inferior vena cava obstruction	5 months	^Citation134
Rituximab	SJS/TEN	78/male	Diffuse large B-cell lymphoma with bone marrow involvement	Died secondary to complications of SJS/TEN	U	^Citation63
Vemurafenib	TEN	69/male	Melanoma with axillary lymph nodes and pulmonary metastasis	Sepsis	4 days	^Citation139
Vemurafenib	TEN	63/female	Melanoma with cervical lymph-node, scalp, lung, and liver metastases	Disease progression of melanoma	3 months	^Citation68
Vemurafenib	TEN	73/female	Melanoma with inguinal lymph node metastasis	Multiple-organ failure after ventilator-acquired pneumonia and melena	35 days	^Citation142
Aldesleukin	TEN	67/female	Renal cell carcinoma with lung metastasis	Septic shock and hypovolemia secondary to pancytopenia and TEN	10 days	^Citation77
Denileukin	TEN	45/male	Follicular large-cell lymphoma with widespread lymphadenopathy, splenomegaly, and bone marrow involvement	Multisystem organ failure with massive TEN and disease progression of lymphoma	18 days	^Citation75
Nivolumab	TEN	64/female	Melanoma with pulmonary and liver metastases	Disease progression of melanoma and sepsis	4 months	^Citation79
Nivolumab	TEN	50/female	Metastatic malignant melanoma	Septic shock and multisystem organ failure	6 days	^Citation81

Abbreviations: SJS, Stevens–Johnson syndrome; TEN, toxic epidermal necrolysis; U, unknown.

Table 4 Targeted anticancer therapies and immunotherapy-induced severe cutaneous adverse reaction cases with multiple concomitant medication (n=24)

Agent	Coadministered medication	Phenotype	Reference
Afatinib	Carboplatin, pemetrexed, esomeprazole, and sulfamethoxazole	SJS	^Citation30
Brentuximab vedotin	Naproxen	SJS	^Citation137
Brentuximab vedotin	Piperacillin–tazobactam, omeprazole, morphine, granisetron, pregabalin, and amisulpride	TEN	^Citation138
Cetuximab	Minocycline	TEN	^Citation111
Cetuximab	Camptothecin-II	SJS	^Citation112
Gefitinib	Pemetrexed and cisplatin	TEN	^Citation114
Imatinib	Ibuprofen	SJS	^Citation117
Imatinib	Mercaptopurine	SJS	^Citation42
Imatinib	Allopurinol and sulfamethoxazole–trimethoprim	SJS	^Citation89
Imatinib	Fludarabine, busulfan	SJS	^Citation121
Imatinib	Allopurinol	SJS	^Citation122
Imatinib	Lansoprazole	SJS	^Citation123
Imatinib	Allopurinol	DRESS	^Citation124
Pembrolizumab	Phenprocoumon, spironolactone, acetylsalicylic acid, bisoprolol, metamizole, rabeprazole, mirtazapine, lorazepam, torasemide, ramipril, oxycodone, and dalteparin	SJS	^Citation80
Pembrolizumab	Phenytoin (with whole-brain radiotherapy)	SJS	^Citation81
Rituximab	Bendamustine	SJS/TEN	^Citation135
Rituximab	Allopurinol and bendamustine	SJS/TEN	^Citation63
Sorafenib	Tosufloxacin	TEN	^Citation51
Sorafenib	Furosemide, spironolactone, and lansoprazole	AGEP	^Citation129
Vemurafenib	Ipilimumab	SJS	^Citation13
Vemurafenib	Valproate	TEN	^Citation142
Vemurafenib	Levothyroxine sodium	TEN	^Citation68
Vemurafenib	Metoprolol and hydrochlorothiazide	DRESS	^Citation144
Vandetanib	Temozolomide	TEN	^Citation116

Abbreviations: AGEP, acute generalized exanthematous pustulosis; DRESS, drug rash with eosinophilia and systemic symptoms; SJS, Stevens–Johnson syndrome; TEN, toxic epidermal necrolysis.

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