Electrochemotherapy with intravenous bleomycin for patients with cutaneous malignancies, across tumour histology: a systematic review

Figures & data

Table 1. Studies performing ECT with standard dose of intravenous bleomycin performed from 1993 to 2021 for treatment of cutaneous malignancies. Studies written in italics are from the InspECT network.

	Study	Patients/nodules	Tumour histology	Bleomycin administration (1000 IU = 0.66mg)	Electrodes	Size mm (median)	Response rates (%)	Objective response rate (%)
1	Belehradek 1993 [14]	8/40	HNSCC	IV 10mg/m^2 ($\sim$15.000IU/m^2) 15 mg/m^2 (1 pt) ($\sim$22.700IU/m^2)	Hex	16–17	CR 57 PR 15 NC 7.5	72
2	Domenge 1996 [28]	7/53	HNSCC, BC	IV 10mg/m^2 ($\sim$15.000IU/m^2) 15 mg/m^2 ($\sim$22.700IU/m^2) Patients received in some cases additional bleomycin.	Hex	10–200	CR 11 PR 11 NC 56 PD 22	22
3	Mir 1998 [26]	50 (15 incl in previuos)/291	BCC, MM, BC, HNSCC	IT or IV 10mg/m^2 ($\sim$15.000IU/m^2), 15 mg/m^2 ($\sim$22.700IU/m^2), 10.000 IU/m^2 (6 pt’s)	Plate, needle	2–125 (11)	CR 56.4 PR 28.9	85.3
4	Rols 2000 [31]	4/55	MM	IV 10mg/m^2 ($\sim$15.000IU/m^2)	Plate	2–35	CR 9 PR 84 NC 7	93
5	Marty 2006 [5]	62/290	MM, carcinom, sarcoma	IT or IV 15.000 IU/m^2	Hex, lin or plate	Not described	CR 73.7 PR 11.1	84.8
6	Larkin 2007 [32]	30/111	SCC, BC	IT or IV 15.000 IU/m^2	Plate, lin	90/111 < 3 cm	CR 60 PR 22 NC 18	82
7	Quaglino 2008 [33]	14/233	MM	IV 15 mg/m^2 ($\sim$22.700IU/m^2)		Not described	CR 58 PR 34 NC 8	92
8	Campana 2009 [34]	52/608	MM, BC, SCC, HNc	IT or IV 15.000 IU/m^2	Plate/ hex	1–30	CR 58 PR 34 NC 7	93
9	Kis 2011 [35]	9/158	MM	15 mg/m^2 ($\sim$22.700IU/m^2)	Lin, hex	5–56 (14.7)	CR 23 PR 39 NC 30 PD 8	62
10	Matthiessen 2011 [36]	52/196	MM, BC	IT or IV 15.000 IU/m^2	Plate/ hex	1–200 (10)	CR 60 PR 19 SD 11 PD 7	58.5 <3 cm: 86 >3 cm: 31
11	Skarlatos 2011 [37]	51/52	MM, KS, HNc + solid	IT or IV 15.000 IU/m^2	Lin, hex or plate	Not described	CR 63.8 PR 31.9	95.7
12	Matthiessen 2012 [38]	17/25	BC	IT or IV 15.000 IU/m^2	Plate, hex	32–250 (65)	CR 8.3 PR 8.3	23.6
13	Curatolo 2012 [39]	23/25	KS	IV 15 mg/m^2 ($\sim$22.700IU/m^2)	Plate, hex	Not described	CR 60.9 PR 39.1 SD 75	100
14	Latini 2012 [40]	18/29	KS	IV 15.000 IU/m^2			CR 86 PR 14	100
15	Campana 2012 [41]	85/894	MM	IT or IV 15.000 IU/m^2 or in combination	Needle	3–73 (24)	CR 48 PR 46 NC 4 PD 2	94
16	Campana 2012 [42]	35/516	BC	IV 15.000 IU/m^2	Hex	10–220 (20)	CR 54.3 PR 37.1 SD 8.6	92.3
17	Benevento 2012 [43]	12/142	BC	IV 15.000 IU/m^2	Hex	5–30	CR 75.3 PR 17 NC 7.7	91.4
18	Gargiulo 2012 [44]	25/25	SCC, BCC, adenocarcinoma	IV 15.000 IU/m^2	Hex, finger	Not described	CR 72 PR 28	100
19	Caraco 2013 [45]	60	MM	IV 15.000 IU/m^2 10% received reduced dose	Lin, hex	0.8–20 (5)	CR 48.4 PR 38.3 PD 13.3	86.7
20	Di Monta 2014 [46]	19	KS	IV 15.000 IU/m^2	Plate, lin	Not described	CR 73.6	100
21	Campana 2014 [47]	34/210	soft tissue sarcoma	IV 15.000 IU/m^2	Hex	20–120 (40)	CR 32.3 PR 52.9 SD 14.7	85.2
22	Campana 2014 [48]	55	Metastatic BC	IT or IV 15.000 IU/m^2	Needle	10–320 (20)	CR 40 PR 47.3 SD 12.7	87.3
23	Campana 2014 [49]	42/81	SCC, BCC, adenocarcinoma	IT or IV 15.000 IU/m^2	Plate, lin, hex, finger	10–100 (35)	CR 41 PR 18	59
24	Solari 2014 [50]	39	MM, BC, KS, BCC, SCC	IV 15.000 IU/m^2	Hex	Not described	For MM: CR 10 PR 45 For others: CR 36.8 PR 42.1	67 For MM: 55 For others: 78.9
25	Ricotti 2014 [51]	30/654	MM	IV 15.000 IU/m^2		0.2–10cm^2	CR 20 PR 80	100
26	Cabula 2015 [52]	125/239	BC	IT or IV 15.000 IU/m^2	Plate, lin or hex	15–45 (21)	CR 68.5 PR 23.5 SD 6.6 PD 0.9	92
27	Kreuter 2015 [53]	56	MM, BC, SCC + others	IV 15 mg/m^2 ($\sim$22.700IU/m^2)	Plate, lin of hex	Not described	CR 10.7 PR 33.9 SD 12.5 PD 42.9	44.6
28	Mir-Bonafe 2015 [54]	31	MM	IV 15.000 IU/m^2	Hex	0.8–15 (4.4)	CR 23 PR 49 PD 28	72
29	Quaglino 2015 [55]	121	MM, SCC, BC, BCC	IT or IV 15.000 IU/m^2	Plate, lin, hex	3–400 (23)	CR 34 PR 32	66
30	Bertino 2016 [8]	105/105	SCC, BCC, MM and others.	IT or IV 15.000 IU/m^2	Plate, hex or finger	2–145 (20)	CR 48 PR 26 SD 19 PD 6	74
31	Campana 2016 [56]	376/1304	MM, SCC, KS, BC, BCC and others	IT or IV 15.000 IU/m^2 – (251 pt)	Hex, lin, plate, multiple	6–20 (10)	CR 30.1 PR 45.5 SD 21	82.7
32	Guida 2016 [57]	19	AS	IV 15.000 IU/m^2	Lin	15–35 (20)	CR 66.7 PR 18.5 SD 9.3 PD 5.6	85.5
33	Groselj 2016 [58]	24/47	BCC, SCC, BC	IV 15.000 IU/m^2	Plate, hex	<50	CR 82.6 PR 15.2 SD 2.2	97.8
34	Bourke 2017 [59]	24/161	BC	IT or IV 15.000 IU/m^2	Plate, lin or hex	Not described	CR 64.4 PR 15.3 NC 19.3	79.7
35	Di Monta 2017 [60]	22/22	SCC	IV 15.000 IU/m^2	Lin, hex	Not described	CR 22.7 PR 59 SD 13.6 PD 4.5	81.7
36	Campana 2017 [61]	84/185	BCC	IT or IV 15.000 IU/m^2	Lin, hex	5–267 (20)	CR 50 PR 35.7	85.7
37	Kunte 2017 [62]	151/394	MM	IT or IV 15.000 IU/m^2	Plate, lin, hex	5–20 (9)	CR 58 PR 20 SD 20 PD 2	78
38	Matthiessen 2018 [63]	90/207	BC	IT or IV 15.000 IU/m^2	Plate, hex	1–550 (25)	CR 50 PR 21 SD 18 PD 8	71
39	Gargiulo 2018 [64]	21/21	Lower lip SCC	IV 15.000 IU/m^2	Lin	Not described	CR 71.4 PR 28.6	100
40	Al-Hadithy 2018 [65]	48	MM, BC, AS, SCC	IV 15.000 IU/m^2	Lin, hex or finger	1.33–2.1 m^2	CR 74 PR 14 NR 8.5	88
41	Wichtowski 2019 [66]	38	BC	IV 15.000 IU/m^2	Hex	Not described	CR 42 PR 29 NR 11 PD 18	71
42	Bonadies 2019 [67]	33	HNSC	IV 15.000 IU/m^2	Plate, lin, hex, finger	Not described	CR 82 PR 18	100
43	Kis 2019 [68]	12/12	Eyelid-periocular BCC	IT or IV 15.000 IU/m^2 (9 pts)	Lin, hex	1–108	CR 58.3 (100 after several treatments)	58.3
44	Longo 2019 [69]	93	HNSC	IV 15.000 IU/m^2	Lin, hex, finger	>30 or <30	CR 5 PR 40 PD 20 SD 34	45
45	Campana 2019 [70]	20/20	cAS	IT or IV 15.000 IU/m^2	Lin, hex	10–200 (23)	CR 61 PR 22 SD 18 PD 2	83
46	Pirc 2020 [71]	23	MM	IT or IV 15.000 IU/m^2	Hex, plate, lin	Not described	Not described
47	Fabrizio 2020 [72]	41	SCC, KS, BCC, MM, BC	IT or IV 15.000 IU/m^2	Lin, hex	17–350 (60)	CR 61 PR 39	100
48	Clover 2020 [13]	987/2482	MM, BC, SCC, BCC and KS	IT or IV 15.000 IU/m^2	Lin, hex	5–500 (23)	CR 61 PR 22 SD 12 ND 2	83
49	Borgognoni 2020 [73]	68/699	MM, NMSC	IT or IV 15.000 IU/m^2	Plate, lin or hex	Not described	CR 54.4 PR 35.3	89.7
50	Groselj 2021 [16]	25	BCC, SCC, MM and others	IV 15.000 IU/m^2	Lin	Not described	CR 71.9 PR 24.6 SD 1.8 PD 1.8	96.5

Tumour histology: BCC: Basal cell carcinoma; SCC: Squamous cell carcinoma; MM: Malignant melanoma; BC: Breast cancer; HNSCC: Head and neck SCC; KS: Kaposi’s sarcoma; AS: Angiosarcoma; NMSC: Non-melanoma skin cancer.

Drug administration: IV: Intravenous; IT: Intratumoural.

Response: ORR: Objective response rate, CR: Complete response, PR: Partial response, SD: Stable disease, PD: Progressive disease, NC: No change, ND: Not determined.

Electrodes: Hex: Hexagonal needle electrodes; Lin: Linear needle electrodes; Needle: Other types of needle electrodes; Plate: Surface electrode with opposing plates [9].

Table 2. Studies performing ECT with a reduced dose of intravenous bleomycin for treatment of cutaneous malignancies.

	Study	Patients/nodules	Tumour histology	Bleomycin administration	Electrodes	Size mm (median)	Response rates (%)	Objective response rate (%)
51	Heller 1996 [74]	6/18	MM, BCC, BC	IV 10 U/m^2 ($\sim$10.000 IU/m^2)	Plate	4–16	CR 33 PR 39	72
52	Rotunno 2018 [29]	57/147	MM, SCC, BCC, BC, KS and others	Three groups: 50% reduction − 7.500 IU/m^2 33% reduction − 10.000 IU/m^2 10% reduction − 13.500 IU/m^2	Plate, lin, hex	5–190 (10)	CR 82 PR 9 CR 64 PR 20 CR 74 PR 15	90 84 89
53 + 54	Groselj 2018; Jamsek 2020 [17,19]	28 (>65yo)	NMSC	IV two groups: 10.000 IU/m^2 (12 pt’s)	Hex, lin, plate	6–80 (21)	CR 96–100	100
				15.000 IU/m^2 (16 pt’s)		4–50 (17)		96
55	Sersa 2021 [18]	61 (>90yo)	SCC, BCC, MM, BC + others	IT or IV 2 × 10.000 IU/m^2 15.000 IU/m^2	Hex, lin, plate	5–450 (15)	CR 64.7 PR 23	87.7
		122 (<90yo)					CR 57.4 PR 30	87.4

Tumour histology: BCC: Basal cell carcinoma; SCC: Squamous cell carcinoma; MM: Malignant melanoma; BC: Breast cancer; KS: Kaposi’s sarcoma; NMSC: Non-melanoma skin cancer.

Drug administration: IV: Intravenous; IT: Intratumoural.

Response: ORR: Objective response rate; CR: Complete response; PR: Partial response; SD: Stable disease; PD: Progressive disease; NC: No change; ND: Not determined.

Electrodes: Hex: Hexagonal needle electrodes; Lin: Linear needle electrodes; Plate: Surface electrode with opposing plates [9].

Figure 1. PRISMA flowchart depicting the search and screening process.

Figure 2. Forest plot of the objective response rates reported in the 55 studies mentioned in Tables 1 and 2, including the pooled mean with confidence intervals (CI). Squares indicate studies with standard dose of bleomycin and triangles indicate studies with reduced dose of bleomycin. The size of square/triangle is dependent on study size. Studies written in italics are from the InspECT network.

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Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article.