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Irreversible Electroporation (IRE)
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This entry is adapted from the peer-reviewed paper 10.3390/jcm10081609

Electroporation (IRE) is a novel cancer treatment that may improve survival and quality of life in LAPC. 

irreversible electroporation locally advanced pancreatic cancer immunotherapy

1. Introduction

Irreversible electroporation (IRE) is a novel, non-thermal ablative therapy used to treat solid cancers [1]. IRE treatment destroys cancer cells using electricity [2]. It is applied by placing two or more electrodes in and around the cancer. Electrodes can be inserted percutaneously under image guidance, laparoscopically, or through an open approach following a midline laparotomy.

Multiple short pulses of high-voltage electrical current are applied between electrode pairs. The application of an electric field across cell membranes is thought to initiate the formation of nanopores in the lipid bilayer of the tumour cell’s plasma membrane, leading to homeostatic disruption and cell death [3][4]. The mechanism of action of IRE remains controversial. Initial studies reported apoptosis as the main mechanism of cellular death [5], however there is increasing evidence that necrosis also contributes [6]. Apoptotic cell death involves a number of complex intracellular signalling pathways involving mitochondria [7]. The exact mechanism through which IRE induces apoptosis, and whether this is through mitochondrial-mediated pathways, remains to be established.

Unlike other ablative techniques, such as microwave ablation (MWA), cryotherapy and radiofrequency ablation (RFA), IRE is thought to exert its cytotoxic effect without relying on thermal injury [8]. Multiple studies report that IRE spares blood vessels and bile ducts [9][10][11]. Furthermore, IRE is not susceptible to the “heat sink” effect, a phenomenon where blood flowing in vessels adjacent to the cancer being treated prevents the area of ablation from reaching effective temperatures for cellular damage, leaving viable tumour cells [12]; a concern with ablative methods reliant on thermal injury.

Electrical pulses have been known to be cytotoxic since the mid 20th century and have been used in food and water sanitisation programmes [13][14]. In the 1960s Sale and Hamilton reported detecting leakage of intracellular contents following electrical application and postulated that the application of an electrical field resulted in an increase in membrane potential resulting in the loss of cellular integrity [15]. A decade later the term “electroporation” was coined by Neumann and Rosenheck, who demonstrated that the changes in the membrane permeability were temporary and could be reversed [16]. This is now known as reversible electroporation (RE). RE provided a therapeutic route into cells and has been used in recent years to deliver gene therapy (gene electro-transfer) [17] and to target chemotherapeutic agents to cancerous cells (electrochemotherapy) [18].

Irreversible electroporation was largely ignored in oncology until 2005 when Davalos et al. demonstrated that by increasing the electrical field strength and duration of pulses, the changes in membrane permeability were permanent and could therefore induce cell death [19]. In vivo [20][21] and in vitro [22] studies of cancer cells treated with IRE confirmed its cytotoxic effect. Animal studies observing the effect of IRE in healthy organs such as pig pancreas, liver, kidney, and murine liver followed [23][24][25][26][27].

In 2012, Martin et al. published the first human pilot study assessing IRE treatment in pancreatic cancer [28]. Since then, several studies have reported on pancreas IRE [29][30][31][32][33][34][35][36][37][38][39][40][41][42][43]. Unlike liver IRE therapy [44], pancreas IRE therapy has no established protocol. Most studies to date have used 90 pulses per treatment cycle, with each pulse length lasting 70–90 µs and between 1400–2000 V/cm being delivered [45].

IRE therapy for cancer is associated with procedure related complications, the severity of which relate to the site and size of cancer. For pancreatic cancer (PC) the risks are high because the cancer is surrounded by vital structures, such as the coeliac axis and other large blood vessels, and key biliary and pancreatic structures. There is no consensus on how to avoid damage to the adjacent healthy tissues.

IRE treatment protocols used in clinical practice to date have varied [45], and in part have been developed using data from animal studies. However, the animal and human pancreas are significantly different in cellular composition [46] and electrical impedance, which will likely impact IRE efficacy [47]. Similarly, a cancerous pancreas is different in cellular composition and electrical properties compared to a non-cancerous pancreas, which may further impact the success of IRE therapy [48][49]. Variability in current IRE treatment protocols, such as inter-electrode distance, strength of the voltage applied, and the individual electrical properties of the tissue being ablated all have an impact on treatment efficiency and the area of ablation [23][47][50]. Evaluation of the histological changes and clinical benefit following IRE are needed in both human healthy pancreatic and pancreatic cancer tissue, in order to establish appropriate treatment protocols.

A number of retrospective and prospective human clinical studies on pancreas cancer IRE have suggested a survival benefit [29][30][31][33][37][51][52]. However, IRE is not in routine clinical practice in the United Kingdom for a number of reasons. First, evidence from randomised controlled trails (RCT) is awaited, to support the benefits suggested in selected patient cohorts. Second, there is no consensus on the optimal IRE treatment protocol [45] nor the approach needed to protect adjoining pancreatic tissue.

2. Complications of Pancreas IRE Therapy

IRE is an invasive procedure and is associated with a range of procedure-related complications [1][53]. The average rate of severe complications in the table below (defined as greater than Grade III on the Clavien-Dindo scale [54]) following IRE is 12%, but has been reported to be as high as 42% [55]. The average procedure-related mortality rate is 2% and 0% for open and percutaneous IRE, respectively [56]. A common complication is mild acute pancreatitis [57]. The more serious complications include severe acute pancreatitis, portal vein thrombosis, bile leak, perforations of the gastro-intestinal tract, and pancreatic fistula [30][32][40][52]; summarised in Table 2.

Table 2. Incidence and severity of complications reported in clinical studies of IRE treatment for pancreas cancer.

Table
Study Date Sample Size Method of IRE Delivery All Complications Severe Complications
Veldhuisen et al. [58] 2020 52 Percutaneous 37% -
Ruarus et al. [55] 2020 50 Percutaneous 58% 42%
Liu et al. [59] 2019 54 Open (16/54) 19% 1%
Liu et al. 2019 54 Percutaneous (38/54) 44% 3%
Holland et al. [31] 2019 152 Percutaneous 18% 13%
Flak et al. [30] 2019 33 Percutaneous 33% 21%
Mansson et al. [36] 2019 24 Percutaneous 33% 25%
Huang et al. [60] 2018 70 Open 23% 4%
Leen et al. [33] 2018 75 Percutaneous 25% 8%
Zhang et al. [61] 2017 21 Percutaneous 19% 0%
Sheffer et al. [42] 2017 25 Percutaneous 48% -
Vogel et al. [62] 2017 15 Percutaneous 53% -
Narayanan et al. [40] 2016 50 Percutaneous 62% 20%
Mansson et al. [35] 2016 24 Percutaneous 46% 13%
Lambert et al. [52] 2016 21 Percutaneous 24% -
Yan et al. [43] 2016 25 Open 36% 8%
Paiella et al. [41] 2015 10 Open 10% 0%
Belfiore et al. [29] 2015 20 Percutaneous 10% 0%
Martin et al. [37] 2015 200 Open + resection (50/200) 40% -
Martin et al. 2015 200 In situ (150/200) 36% -
Kluger et al. [32] 2015 50 Open 46% 20%
Martin et al. [38] 2013 54 Open 39% -
Martin et al. [28] 2012 27 Open 25% 7%

The variability in the reported complication rates across studies may be due to the heterogeneity in treatment protocols used or may be related to the size of the tumours treated. A study by Paiella et al. had one of the lowest complication rates at 10%, with no severe procedure related complications [41]. This study treated patients with tumour sizes less than 4 cm. With their IRE procedure delivering 1500 volts between electrodes placed 1–2 cm apart, with a pulse duration of 70 µs and a total of 90 pulses delivered. In contrast, a study by Narayanan et al. included patients with much larger tumours (up to 8 cm in size) and reported one of the highest rates of complications (a total of 62% of patients developing a procedure-related complication and a severe complication rate of 20%) [40]. The authors did not correlate tumour size with complications. The treatment protocol for this study did not specify the exact voltage applied but reported a higher range using 1500 to 3000 volts, presumably using the highest field strength available commercially (3000 volts) for the largest tumours. Electrodes were placed between 1.8 and 2.2 cm apart and a total of 70 volts each with a duration of 70 µs was delivered.

Other factors contributing to the range of reported complications may be related to the number of years of experience individual centres have with treating patients with IRE, although this information in not always available in the literature. Moreover, the heterogeneity of the rates of reported complications may be related to the method in which IRE is delivered (open vs. percutaneous). The data presented in Table 2 further highlights the need for a robust randomised clinical trial that aims to mitigate for these factors, to better appreciate IRE-associated complications.

3. Radiological Response to Pancreas IRE

IRE-treatment response in clinical studies has been determined by radiological imaging, mainly using computerised tomography scanning (CT) and magnetic resonance imaging (MRI). Akinwande et al. prospectively reviewed five LAPC patients who underwent IRE and evaluated contrast enhanced CT images following IRE [63]. They reported that the ablation zone was ill-defined and irregular, without clearly demarcated margins. Immediately following IRE, the ablation zone appeared larger than the original target lesion, thought to be due to the inclusion of both the tumour lesion, as well as the safety margins. Blood vessels within the area of ablation demonstrated narrowing immediately following IRE, which resolved or remained stable in subsequent scans. Subsequent follow-up imaging demonstrated an increased enhancement of the ablation zone, which the authors concluded was due to the formation of granulation tissue and fibrosis, perhaps correlating with the histological findings reported in animal studies. As the surrounding oedema, hyperaemia, and granulation tissue decreased over time, it facilitated the visualisation of the true ablation zone which was smaller than the region seen immediately after IRE, indicating that the ablation zone size immediately following IRE may not be a reliable indicator of the true extent of the area treated, as it is likely to include the surrounding reactive reaction of oedema and hyperaemia. Alternatively, this initial ablation zone may be an important factor in predicting the true ablation zone once the immediate reactive inflammatory process diminishes. There is no consensus on the optimum time post-treatment to measure ablation zone.

Vroomen and colleagues assessed imaging characteristics in 25 patients with LAPC following CT-guided percutaneous IRE [64]. All patients had biopsy-proven LAPC and underwent contrast enhanced CT (ceCT) prior to IRE. Subsequent contrast enhanced MRI (ceMRI) was performed 1 day, 2 weeks, and 6 weeks following IRE treatment. At the 6-week mark patients additionally underwent a ceCT. A final ceCT was performed 3 months after IRE. Figure 1 and Figure 2 show the median tumour volumes across the imaging modalities and demonstrate an increase in tumour volume in the initial post-IRE period on both ceCT and ceMRI, followed by a decrease. The authors reported that there was a hyperintense border surrounding the IRE ablation zone in the portal venous phase in 71% of patients, noted 1 day and 2 weeks post IRE, and which was identified in only 29% of patients at the 6 week follow up. The observed hyperintense rim surrounding the ablation zone 1 day post-IRE may represent reactive hyperaemia and oedematous inflammation and still include residual disease. A longer follow-up is required in order to evaluate the exact significance of this radiological characteristic.

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Figure 1. Median tumour volumes on contrast enhanced MRI (ceMRI).

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Figure 2. Median tumour volumes on contrast enhanced CT (ceCT).

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Subjects: Oncology
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Zainab Rai
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Update Date: 07 May 2021
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