Irreversible electroporation of malignant liver tumors: Effect on laboratory values

  • Authors:
    • Mohammed Alnaggar
    • Ammar M. Qaid
    • Jibing Chen
    • Lizhi Niu
    • Kecheng Xu
  • View Affiliations

  • Published online on: July 2, 2018     https://doi.org/10.3892/ol.2018.9058
  • Pages: 3881-3888
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

Liver cancer is often associated with chronic liver diseases. Treatment with percutaneous irreversible electroporation (IRE) may preserve liver function. In the present study, the clinical data of 29 patients with liver tumors between July 2015 and December 2016, all of whom underwent liver IRE at Fuda Cancer Hospital, Guangzhou, China was retrospectively reviewed. All the patients survived the treatment. Of the 29 patients, 7 were positive for hepatitis B, 15 had hepatocellular carcinoma (HCC) and 7 had pancreatic cancer with liver metastases. All patients survived IRE. Despite liver‑protective treatment prior to IRE, the mean alanine transaminase (ALT) and aspartate transaminase (AST) levels were significantly elevated 1‑2 days after IRE, to 540 and 712 U/l, respectively; however they had returned to the preoperative values by 2 weeks following IRE. Prior to IRE, the mean total bilirubin and direct bilirubin measurement levels were normal; however, 8‑10 days after IRE, they had increased to 24 U/l and 12 µmol/l, respectively, and had returned back to the preoperative levels by 2 weeks after IRE. This first group included all patients. The result of the 4 subgroups of cancer patients demonstrated a variation between different measurement days and recovery with patients positive for the hepatitis B virus taking the longest duration to recover (17±3 days) meanwhile patients with pancreatic cancer with liver metastases took the shortest time to achieve recovery (10.78±2 days). The findings of the present study indicate that hepatic injury caused by IRE is transient and self‑limiting in patients with liver tumors.

Introduction

Hepatocellular carcinoma (HCC) is a common tumor worldwide and its incidence rate is increasing (1). Of the affected patients, 80% have chronic liver diseases such as hepatitis or cirrhosis; the presence of these conditions in conjunction with HCC has a major effect on the prognosis and treatment of this type of cancer (2) Currently, percutaneous ablation therapies, including percutaneous ethanol injection, microwave coagulation and radiofrequency ablation, are available and are important therapeutic modalities for the treatment of HCC (38). The hepatitis B virus (HBV) is responsible for 30% of all cases of cirrhosis and >50% of HCC cases with an incident rate of 50 million new cases diagnosed annually in endemic countries (9). Irreversible electroporation (IRE) is a newly developed non-thermal ablation procedure where electrical pulses are delivered for a few milliseconds to induce nanoscale defects that increase cell membrane permeability, the procedure induces apoptosis without harming the extracellular matrix; therefore, the structural components of the tissues are preserved (10,11). IRE is a novel, non-thermal form of tumor ablation that is not affected by heat sink and may result in less collateral damage based on its mechanism of action (12). IRE relies on short pulses of high-frequency energy to induce pores in the lipid bilayer of cells, leading to cell death via apoptosis. In the present study, hepatic injury in 29 patients following a single IRE session was retrospectively assessed. The serum transaminases and bilirubin values were compared between patients who were positive and those who were negative for hepatitis B and for patients with HCC and pancreas cancer with liver Metatases, to study the effects of IRE on liver function and its recovery.

Materials and methods

Ethics

The present study was approved by the Regional Ethics Committee of Guangzhou Fuda Cancer Hospital (Guangzhou China). Written informed consent was obtained from all patients, and the study protocols were in accordance with the tenets of the Declaration of Helsinki.

Patient selection

Diagnosis of unresectable HCC and liver metastasis was confirmed by pathological studies. The diagnoses were confirmed blindly by two pathologists at pathology department affiliated with Jinan University (Guangzhou, China) and imaging analyses and measurement of the tumor marker α-fetoprotein. Patients who met the following criteria were considered to be eligible for the study: The presence of one or two significant tumors in the liver, Karnofsky performance status (13) (KPS) score ≥70, white blood cell count ≥3×109/l, neutrophil count ≥2×109/l; hemoglobin ≥90 g/l, platelet count ≥100×109/l, prothrombin time (international normalized ratio, INR) ≥1.5. Furthermore, the present study excluded patients who had severe coronary heart disease, myelosuppression, respiratory disease, acute/chronic infection, or level 3 hypertension, and had adequate hepatic function [total bilirubin (T.BIL) <75 µmol/l, direct bilirubin (D.BIL) <39 µmol/l, and a Child-Pugh score (14) of A or B] and renal function (serum creatinine <130 µm and serum urea <10 mm). Between July 2015 and December 2016, 29 patients (20 males; age range, 32–75 years; mean age, 55 years; and 9 females; age range, 32–70 years; mean age, 53 years) were eligible and enrolled from Fuda cancer hospital, Affiliated with Jinan University (Guangzhou, China).

Irreversible electroporation procedure

All patients underwent gastric decompression and endotracheal intubation. General anesthesia was induced intravenous and inhalation anesthesia by trachea intubation, drugs delivered via vein and trachea by intravenous infusion, including midazolam (0.5 mg) and penehyclidine hydrochloride (0.5 mg). For general anesthesia induction: Etomidate (0.3 mg/kg), benzenesulfonic acid cisatracurium (0.2 mg/kg) and remifentanil (150 µg) were used, and for maintenance: Intravenous pumping of diprivan (50–150 mg/h); remifentanil (320–720 µg/h) and inhalation of sevoflurane (0.6–2%) benzenesulfonic acid cisatracurium (6 µg/kg). Computed tomography (CT) was undertaken and the target region was demarcated. Ultrasound-guided insertion of 2–3 electrodes was performed. Following anesthesia an additional CT image was taken to confirm correct placement of the electrodes. IRE was synchronized to deliver electrical pulses coordinated with cardiac rhythm to prevent cardiac dysrhythmia. Typically, the distance between electrodes was 1.5–2 cm. The voltage was set at 1,500–3,000 kV. Between 70–90 pulses were delivered in 7–9 sets of 10 pulses. Additional pullbacks were performed if the target region was >2 cm in diameter. The baseline and highest heart rate during IRE were recorded by electrocardiography. Arrhythmia of any form was documented. Invasive blood pressure measurement via the femoral artery was applied for precise systolic blood pressure (SBP) monitoring. If SBP was >40 mmHg during ablation or >190 mmHg at any time, electric pulses were suspended for 2–3 min. If no obvious decrease in SBP was observed after 2–3 min, 2–5 mg of phentolamine was administered intravenously to lower blood pressure and prevent hypersensivity.

Assessment of hepatic functional reserve

Hepatic function was assessed with an automatic biochemical analyzer (7100; Hitachi Ltd., Tokyo, Japan). The alanine transaminase (ALT) and aspartate transaminase (AST) levels were measured with the velocity method using a specialized reagent kit (AST kit: Aspartate Aminotransferase kit [Aspartate Substrate Method, cat. no. 1740-2013. ALT kit: Alanine aminotransferase kit. (Alanine low content method) no. 170781], and the T.BIL and D.BIL levels were measured using the vanadate method with a commercially available kit [TBIL: Total Bilirubin kit (Vanadate Oxidation Method) no. 1737-2013. D.Bil: Direct Bilirubin kit (Vanadate Oxidation Method) no. 4523-40-201] (BioSino Bio-Technology and Science Inc., Beijing, China). Blood samples were obtained in the morning, after overnight fasting. The tests were performed every 1–3 days, until the patients were discharged (on day 20). The normal ranges for the measured parameters were as follows: ALT, 5–35 U/l; AST, 8–40 U/l; T.BIL, 0–25.5 µmol/l; and D.BIL, 0–13 µmol/l. Values that were above the upper limit of the normal range were considered to indicate abnormal hepatic function.

Statistical analysis

The revised version of the Response Evaluation Criteria in Solid Tumors (version 1.1) (15) was used to determine the response of the hepatic tumors to the treatment. Statistical tests were performed with commonly used methods, and a nonparametric, one-way AVONA followed by Bonferroni's multiple comparison post-hoc test was used for comparisons between days. Test results are expressed as the mean ± standard error and P<0.05 was considered to indicate a statistically significant difference. All analyses were conducted using GraphPad software version 5.0 (GraphPad, Software, Inc., La Jolla, CA, USA).

Results

Clinical data

Prior to hepatic IRE, detailed data of the patients were extracted and are presented in Table I. Of the 29 patients, 22 (75.9%) had HCC, 7 (24.1%) had a history of hepatitis, 7 (24.1%) had pancreatic cancer with liver metastases, 10 (34.5%) had undergone initial surgical treatment and 22 (75.86%) had undergone systemic chemotherapy at different centers.

Table I.

Detailed data on patients prior to hepatic irreversible electroporation.

Table I.

Detailed data on patients prior to hepatic irreversible electroporation.

Characteristicn (%)
Sex
  Female9 (31.03)
  Male20 (69.97)
  HCC22 (75.9)
  Sex (male/female)15/7
  Median age (years)52
AJCC stage (2010) (37,38)
  IIIA2 (9.09)
  IIIB1 (4.55)
  IIIC2 (9.09)
  IVA17 (77.27)
Hepatitis B positive7 (24.1)
Child-Pugh stage (15)
  A14 (63.64)
  B8 (36.36)
Liver function
  ALT, U/l27±11
  AST, U/l44±43
  T.BIL, µmol/l18±7
  D.BIL, µmol/l7±4
Tumor type
  Single massive17 (77.27)
  Multinodular5 (22.73)
Ascites
  Yes14 (63.64)
  No8 (36.36)
Pancreatic cancer with liver metastasis7 (24.1)
  Sex (male/female)5/2
  Median age (years)53
AJCC stage (24,38)
  III0
  IV7
Liver function
  ALT, U/l35±11
  AST, U/l49±23
  T.BIL, µmol/l14±4
  D.BIL, µmol/l7±4

[i] AJCC, American Joint Committee on Cancer staging system; HCC, hepatocellular carcinoma; ALT, alanine aminotransferase; AST aspartate aminotransferase; T.BIL, total bilirubin; D.BIL, direct bilirubin.

Perioperative outcomes

All the hepatic lesions were treated with IRE, which was performed successfully in all patients. Severe complications (such as rupture or hepatic failure, myoglobinuria and acute renal failure) did not occur following IRE. There were several mild adverse effects [7 patients developed fever (38.2–39.8°C), 15 patients had pain for 3–7 days, 1 patient had infection, 2 patients had abdominal ascites, and 6 patients developed variable degree of nausea and vomiting]; however the patients recovered without symptomatic management.

Changes in hepatic functional reserve after irreversible electroporation

Of the 29 patients, 7 were positive for the hepatitis B virus, 15 had HCC), and 7 had pancreatic cancer with liver metastases. A total of 29 IRE procedures were performed. The transaminase levels were abnormal until the 4th session of ablation, and the bilirubin level was abnormal until the 2nd session of ablation (this was the case for all patients). The serum transaminase levels increased rapidly and reached a peak on day 1 following IRE, after which they gradually decreased. The ALT and AST levels demonstrated a significant decrease from day 5 and 7, respectively (P<0.001; Fig. 1A and B). No significant change in the serum bilirubin level was observed until 20 days after IRE (Fig. 1C and D).

Changes in hepatic functional reserve in seven patients with hepatitis B

Each of the 7 patients who were positive for hepatitis B underwent IRE. Prior to the 2nd and 3rd ablation sessions, the transaminase and bilirubin levels were abnormal (data not shown). Additionally, 1 day after IRE was performed, the serum transaminase levels increased rapidly until they reached a peak (P<0.001), after which they gradually decreased. The ALT and AST levels showed a significant decrease from day 5 (P<0.01) and day 3, respectively (P<0.001; Fig. 2A and B). There was no obvious variation in the serum bilirubin level until 20 days following IRE (Fig. 2C and D).

Changes in hepatic functional reserve in 22 patients without hepatitis B

All the 22 patients who were negative for hepatitis B underwent liver IRE. None of the patients had normal transaminase levels; in addition, the bilirubin level was abnormal before the 8th ablation session. The serum ALT and AST level increased within 2 days after IRE (P<0.01; Fig. 3A and B) and then decreased gradually, a markedly significant decrease was noted after 8–10 days. No significant change in the serum bilirubin level was observed (Fig. 3C and D).

Variations in hepatic functional reserve patients with HCC

In the 15 patients with HCC who underwent IRE, the serum transaminase levels increased rapidly till they reached a peak the day after IRE, following which they decreased gradually. The serum ALT and AST levels showed a significant decrease from day 0, 1, 3 and 5, respectively (P<0.01; Fig. 4A and B). However, no significant change was observed in the serum bilirubin levels until 20 days following IRE (Fig. 4C and D).

Changes in hepatic functional reserve in patients with pancreatic cancer with liver metastases

The 7 patients with pancreatic cancer with liver metastases also underwent liver IRE. The serum ALT and AST value increased within 2 days following IRE (P<0.01) and then fell gradually, with a significant decrease observed after day 10 (Fig. 5A and B; P<0.05). The serum bilirubin levels increased gradually until they reached a peak at 10–12 days after IRE (Fig. 5C and D; P<0.05), following which it decreased gradually.

Changes in hepatic functional reserve in the 4 patient subgroups

Each result of the 4 subgroups of patients with cancer demonstrated a variation between different measurement days and recovery with patients positive for the hepatitis B virus taking the longest duration to recover (recovery was considered to be when liver functions returned to normal) i.e., 17±3 days, meanwhile, the patients negative for the hepatitis B viruses and patients with HCC whose recovery is observed in 15±2.9 and 12.62±4.3 days respectively, by contrast patients with pancreatic cancer with liver metastases took the shortest time to achieve recovery 10.78±2 days. The result was statistically significant between pancreatic cancer with liver metastases and the other groups (HCC, HBV+ and HBV; P<0.05; Fig. 6). Overall patients suffering from primary hepatic diseases took longer duration to recover when compared with patients with metastatic disease.

Discussion

IRE is a promising procedure for unresectable hepatocellular carcinoma (16). The complications of IRE when used to treat malignant hepatic tumors (such as fever, local pain, abdominal distension, ascites, nausea and vomiting) are acceptable and there is evidence to indicate that the therapy may improve survival. Thus, it is an effective liver tumor ablative therapy that results in only mild and transient adverse effects (1720). IRE is a novel ablation technique wherein electroporation or electro-permeabilization is used to generate electric pulses that create nanoscale defects in the cell membrane and alter its permeability (21). Ablative treatment has been identified to be safe and effective in patients with primary and secondary liver cancer, and those who are not suitable for surgery (22). In the present study, one session of IRE was performed for primary liver tumors and secondary metastases to avoid serious adverse effects. Follow-up liver function tests and routine blood tests revealed immediate liver function damage followed by recovery, consistent with the findings of a study by Chen et al (23). IRE causes significant abnormalities in liver function; however, in the majority of patients these are self-limiting, do not preclude treatment and resemble the changes observed following radiofrequency ablation or cryoablation of the liver (24).

IRE for the treatment of liver cancer is associated with hepatocyte destruction and the subsequent release of transaminases and bilirubin, which are considered as important markers of hepatic functional reserve (25). Similarly, a recent study has reported marked elevations in AST, ALT, T.BIL, and D.BIL (26), which are usually transient and normalize within a few days. It was identified that 1 day after ablation, the ALT level was 3.3-fold higher (mean peak level, 241 U/l) and the AST level was 5-fold higher (mean peak level, 427 U/l); however, they had almost reverted to the preoperative levels within 5 days following the procedure (26). A similar study (22,27) identified 15 bile duct injuries (narrowing, n=8; dilation, n=7) in subacute follow-up magnetic resonance images examinations of 3 patients demonstrated transient abnormalities of laboratory values of bilirubin, 1.6–5.2 mg/dl. Short-term laboratory values were abnormal in 1 patient (increased alkaline phosphatase of 533 U/l vs. baseline) as a result of local tumor recurrence.

Recently, Silk et al (28) reported where IRE was used to treat 22 hepatic metastases in 11 patients; the laboratory values were abnormal after 4 treatment sessions in 3 patients (bilirubin, 2.6–17.6 mg/dl; alkaline phosphatase, 130–1,035 U/l). These abnormal values were transient after 2 sessions, with 2 patients exhibiting prolonged elevation of these abnormal values and 1 requiring stent placement. In the former 2 patients, these adverse effects appeared to be secondary to tumor progression rather than bile duct injury (28). Conversely, the present study did not identify a prolonged significant increase in serum bilirubin. The participants were classified into the hepatitis B virus-positive and hepatitis B-negative groups, and an increase in T.BIL by >3 times [74 µmol/l following IRE vs. 23 µmol/l prior to IRE (3.2 times greater)] and a similar increase in D.BIL [45 µmol/l after IRE vs. 12 µmol/l prior to IRE (3.8 times greater)] were only observed in the hepatitis B-positive group at 3–5 days following treatment. The increase in AST and ALT levels observed in the present study was consistent with previous studies; however the range of increase varied between studies (18,2931). The minimal increase that was observed in the present study may be explained by the time points of the measurements. Overall, the results indicate the importance of ALT and AST as markers of post-IRE liver function.

In patients with hepatitis B, serum bilirubin increased >3 times compared with the preoperative level 7–9 days following IRE. The reason for this increase remains unclear and warrants further research. In the present study, all the patients tolerated the treatment and there were no records of severe complications following IRE. Compared with radiofrequency ablation, IRE resulted in faster liver regeneration, which demonstrated the safety and efficacy of the technique (32). A recent prospective study of IRE treatment of 44 patients with HCC, colorectal, and other lesions reported the following local, recurrence-free survival rates: 97.4% at 3 months, 94.6% at 6 months and 59.5% at 12 months, the recurrence rates tended to be higher in lesions with diameter >4 cm (32). In a smaller cohort of 28 patients treated with IRE, portal vein thrombosis was reported in only 1 case in which the tumor was located within 1 cm of a major portal pedicle (33). Based on the findings, the authors of the study concluded that IRE was safe even for the treatment of liver lesions present near major vascular structures, and their findings are consistent with the reported theoretical benefits of non-thermal ablation (3436). Cannon et al (32) reported that in a cohort of 44 patients, who underwent IRE for primary and secondary liver cancer, the incidence of complications was low. Only 5 patients were observed to have developed adverse events, but the complications were resolved within 30 days of treatment (32). Thus, of previously published studies, many have demonstrated that IRE is a safe and efficient therapeutic method for the treatment of patients with pancreatic and colorectal liver metastases (36).

The limitations of the present study are as follows: No biochemical, hematologic or immunologic factors other than ALT, AST and serum bilirubin were investigated. Although the long-term results are as yet unknown, the future of IRE is promising; however, significant concerns remain regarding its safety over an extended period of time.

To conclude, IRE for primary and metastatic liver cancer may be considered safe in terms of its short-term effects on liver function; however, further study is required to confirm the findings of the present study.

Acknowledgements

Not applicable.

Funding

The present study was supported by Scientific and Technological Plan, Guangdong province, China (grant no. 2016A020216018) and International Foundation for Sciences of Guangzhou Fuda Cancer Hospital (grant no. Y2016-ZD-008).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

LN, MA and AMQ were responsible for study conception and design. MA and AMQ contributed to the acquisition and interpretation of data; JC drafted the work and revised the manuscript. JC and KX acquired and interpreted the data. All the authors approved the article for publication and KX agreed to be accountable for all the aspects of the work including its integrity.

Ethics approval and consent to participate

The present study was approved by the Regional Ethics Committee of Guangzhou Fuda Cancer Hospital, China. Written informed consent was obtained from all the patients, and the study protocols were in accordance with the tenets of the Declaration of Helsinki.

Patient consent for publication

Participants gave informed consent for data sharing.

Competing interests

The authors declare that they have no competing interests.

References

1 

Ali AM, Lizhi N, Jialiang L, Fei Y, Yuan W, Jianying Z, Jin Y, Jibing C, Feng M and Kecheng X: Cryoprotective therapy for hepatocellular carcinoma: Study of 51 patients with a single lesion. Cryobiology. 69:61–67. 2014. View Article : Google Scholar : PubMed/NCBI

2 

Alnaggar M, Niu L, Li J, Yao F, Wang Y, Zeng J, Ye J, Chen J, Mu F and Xu K: Cryoprotective therapy for huge hepatocellular carcinoma: A study of 14 patients with a single lesion. Cryobiology. 69:457–461. 2014. View Article : Google Scholar : PubMed/NCBI

3 

Pearson AS, Izzo F, Fleming RY, Ellis LM, Delrio P, Roh MS, Granchi J and Curley SA: Intraoperative radiofrequency ablation or cryoablation for hepatic malignancies. Am J Surg. 178:592–599. 1999. View Article : Google Scholar : PubMed/NCBI

4 

Chung CD, Lau LL, Ko KL, Wong AC, Wong S, Chan AC, Poon RT, Lo CM and Fan ST: Laparoscopic liver resection for hepatocellular carcinoma. Asian J Surg. 33:168–172. 2010. View Article : Google Scholar : PubMed/NCBI

5 

Ravikumar TS, Kane R, Cady B, Jenkins R, Clouse M and Steele G Jr: A 5-year study of cryosurgery in the treatment of liver tumors. Arch Surg. 126:1520–1524. 1991. View Article : Google Scholar : PubMed/NCBI

6 

Sarantou T, Bilchik A and Ramming KP: Complications of hepatic cryosurgery. Semin Surg Oncol. 14:156–162. 1998. View Article : Google Scholar : PubMed/NCBI

7 

Seifert JK and Morris DL: World survey on the complications of hepatic and prostate cryotherapy. World J Surg. 23:109–114. 1999. View Article : Google Scholar : PubMed/NCBI

8 

Shafir M, Shapiro R, Sung M, Warner R, Sicular A and Klipfel A: Cryoablation of unresectable malignant liver tumors. Am J Surg. 171:27–31. 1996. View Article : Google Scholar : PubMed/NCBI

9 

Schweitzer A, Horn J, Mikolajczyk RT, Krause G and Ott JJ: Estimations of worldwide prevalence of chronic hepatitis B virus infection: A systematic review of data published between 1965 and 2013. Lancet. 386:1546–1555. 2015. View Article : Google Scholar : PubMed/NCBI

10 

Al-Sakere B, André F, Bernat C, Connault E, Opolon P, Davalos RV, Rubinsky B and Mir LM: Tumor ablation with irreversible electroporation. PloS One. 2:e11352007. View Article : Google Scholar : PubMed/NCBI

11 

Edd JF, Horowitz L, Davalos RV, Mir LM and Rubinsky B: In vivo results of a new focal tissue ablation technique: Irreversible electroporation. IEEE Trans Biomed Eng. 53:1409–1415. 2006. View Article : Google Scholar : PubMed/NCBI

12 

Charpentier KP, Wolf F, Noble L, Winn B, Resnick M and Dupuy DE: Irreversible electroporation of the liver and liver hilum in swine. HPB (Oxford). 13:168–173. 2011. View Article : Google Scholar : PubMed/NCBI

13 

Péus D, Newcomb N and Hofer S: Appraisal of the karnofsky performance status and proposal of a simple algorithmic system for its evaluation. BMC Med Inform Decis Mak. 13:722013. View Article : Google Scholar : PubMed/NCBI

14 

Cholongitas E, Papatheodoridis GV, Vangeli M, Terreni N, Patch D and Burroughs AK: Systematic review: The model for end-stage liver disease-should it replace Child-Pugh's classification for assessing prognosis in cirrhosis? Aliment Pharmacol Ther. 22:1079–1089. 2005. View Article : Google Scholar : PubMed/NCBI

15 

Xu HM, Chen Y, Xu J and Zhou Q: Drug-induced liver injury in hospitalized patients with notably elevated alanine aminotransferase. World J Gastroenterol. 18:5972–5978. 2012. View Article : Google Scholar : PubMed/NCBI

16 

Kos B, Voigt P, Miklavcic D and Moche M: Careful treatment planning enables safe ablation of liver tumors adjacent to major blood vessels by percutaneous irreversible electroporation (IRE). Radiol Oncol. 49:234–241. 2015. View Article : Google Scholar : PubMed/NCBI

17 

Dollinger M, Muller-Wille R, Zeman F, Haimerl M, Niessen C, Beyer LP, Lang SA, Teufel A, Stroszczynski C and Wiggermann P: Irreversible electroporation of malignant hepatic tumors-alterations in venous structures at subacute follow-up and evolution at mid-term follow-up. PloS One. 10:e01357732015. View Article : Google Scholar : PubMed/NCBI

18 

Dollinger M, Zeman F, Niessen C, Lang SA, Beyer LP, Müller M, Stroszczynski C and Wiggermann P: Bile duct injury after irreversible electroporation of hepatic malignancies: Evaluation of MR imaging findings and laboratory values. J Vasc Interv Radiol. 27:96–103. 2016. View Article : Google Scholar : PubMed/NCBI

19 

Dollinger M, Beyer LP, Haimerl M, Niessen C, Jung EM, Zeman F, Stroszczynski C and Wiggermann P: Adverse effects of irreversible electroporation of malignant liver tumors under CT fluoroscopic guidance: A single-center experience. Diagn Interv Radiol. 21:471–475. 2015. View Article : Google Scholar : PubMed/NCBI

20 

Scheffer HJ, Nielsen K, de Jong MC, van Tilborg AA, Vieveen JM, Bouwman AR, Meijer S, van Kuijk C, van den Tol PM and Meijerink MR: Irreversible electroporation for nonthermal tumor ablation in the clinical setting: A systematic review of safety and efficacy. J Vasc Interv Radiol. 25:997–1011; quiz 1011. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Cohen EI, Field D, Lynskey GE and Kim AY: Technology of irreversible electroporation and review of its clinical data on liver cancers. Expert Rev Med Devices. 15:99–106. 2018. View Article : Google Scholar : PubMed/NCBI

22 

Ryan MJ, Willatt J, Majdalany BS, Kielar AZ, Chong S, Ruma JA and Pandya A: Ablation techniques for primary and metastatic liver tumors. World J Hepatol. 8:191–199. 2016. View Article : Google Scholar : PubMed/NCBI

23 

Chen X, Ren Z, Zhu T, Zhang X, Peng Z, Xie H, Zhou L, Yin S, Sun J and Zheng S: Electric ablation with irreversible electroporation (IRE) in vital hepatic structures and follow-up investigation. Sci Rep. 5:162332015. View Article : Google Scholar : PubMed/NCBI

24 

Min JH, Waters P, Vincent A, Lee S, Shin Y H, Lee H K and Kim BJ: Reduced serum uric acid levels in neuromyelitis optica: Serum uric acid levels are reduced during relapses in NMO. Acta Neurol Scand. 126:287–291. 2012. View Article : Google Scholar : PubMed/NCBI

25 

Lord J, Willis S, Eatock J, Tappenden P, Trapero-Bertran M, Miners A, Crossan C, Westby M, Anagnostou A, Taylor S, et al: Economic modelling of diagnostic and treatment pathways in National Institute for Health and Care Excellence clinical guidelines: The modelling algorithm pathways in guidelines (MAPGuide) project. Health Technol Assess. 17(v-vi): 1–192. 2013.

26 

Wichtowski M, Nowaczyk P, Kocur J and Murawa D: Irreversible electroporation in the treatment of locally advanced pancreas and liver metastases of colorectal carcinoma. Contemp Oncol (Pozn). 20:39–44. 2016.PubMed/NCBI

27 

Froud T, Venkat SR, Barbery KJ, Gunjan A and Narayanan G: Liver function tests following irreversible electroporation of liver tumors: Experience in 174 procedures. Techn Vasc Interv Radiol. 18:140–146. 2015. View Article : Google Scholar

28 

Silk MT, Wimmer T, Lee KS, Srimathveeravalli G, Brown KT, Kingham PT, Fong Y, Durack JC, Sofocleous CT and Solomon SB: Percutaneous ablation of peribiliary tumors with irreversible electroporation. J Vasc Interv Radiol. 25:112–118. 2014. View Article : Google Scholar : PubMed/NCBI

29 

Kingham TP, Karkar AM, D'Angelica MI, Allen PJ, Dematteo RP, Getrajdman GI, Sofocleous CT, Solomon SB, Jarnagin WR and Fong Y: Ablation of perivascular hepatic malignant tumors with irreversible electroporation. J Am Coll Surg. 215:379–387. 2012. View Article : Google Scholar : PubMed/NCBI

30 

Thomson KR, Cheung W, Ellis SJ, Federman D, Kavnoudias H, Loader-Oliver D, Roberts S, Evans P, Ball C and Haydon A: Investigation of the safety of irreversible electroporation in humans. J Vasc Interv Radiol. 22:611–621. 2011. View Article : Google Scholar : PubMed/NCBI

31 

Sugimoto K, Moriyasu F, Kobayashi Y, Saito K, Takeuchi H, Ogawa S, Ando M, Sano T, Mori T, Furuichi Y and Nakamura I: Irreversible electroporation for nonthermal tumor ablation in patients with hepatocellular carcinoma: Initial clinical experience in Japan. Jpn J Radiol. 33:424–432. 2015. View Article : Google Scholar : PubMed/NCBI

32 

Cannon R, Ellis S, Hayes D, Narayanan G and Martin RC II: Safety and early efficacy of irreversible electroporation for hepatic tumors in proximity to vital structures. J Surg Oncol. 107:544–549. 2013. View Article : Google Scholar : PubMed/NCBI

33 

Hosein PJ, Echenique A, Loaiza-Bonilla A, Froud T, Barbery K, Lima Rocha CM, Yrizarry JM and Narayanan G: Percutaneous irreversible electroporation for the treatment of colorectal cancer liver metastases with a proposal for a new response evaluation system. J Vasc Interv Radiol. 25(1233–1239): e22014.

34 

Distelmaier M, Barabasch A, Heil P, Kraemer NA, Isfort P, Keil S, Kuhl CK and Bruners P: Midterm safety and efficacy of irreversible electroporation of malignant liver tumors located close to major portal or hepatic veins. Radiology. 285:1023–1031. 2017. View Article : Google Scholar : PubMed/NCBI

35 

Zhang Q and Teng G: Interventional therapy of colorectal liver metastasis. Zhonghua Wei Chang Wai Ke Za Zhi. 20:621–624. 2017.(In Chinese). PubMed/NCBI

36 

Lyu T, Wang X, Su Z, Shangguan J, Sun C, Figini M, Wang J, Yaghmai V, Larson AC and Zhang Z: Irreversible electroporation in primary and metastatic hepatic malignancies: A review. Medicine (Baltimore). 96:e63862017. View Article : Google Scholar : PubMed/NCBI

37 

Washington K: 7th edition of the AJCC cancer staging manual: Stomach. Ann Surg Oncol. 17:3077–3079. 2010. View Article : Google Scholar : PubMed/NCBI

38 

Edge SB and Compton CC: The American Joint Committee on Cancer: The 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 17:1471–1474. 2010. View Article : Google Scholar : PubMed/NCBI

Related Articles

Journal Cover

September-2018
Volume 16 Issue 3

Print ISSN: 1792-1074
Online ISSN:1792-1082

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
x
Spandidos Publications style
Alnaggar M, Qaid AM, Chen J, Niu L and Xu K: Irreversible electroporation of malignant liver tumors: Effect on laboratory values. Oncol Lett 16: 3881-3888, 2018
APA
Alnaggar, M., Qaid, A.M., Chen, J., Niu, L., & Xu, K. (2018). Irreversible electroporation of malignant liver tumors: Effect on laboratory values. Oncology Letters, 16, 3881-3888. https://doi.org/10.3892/ol.2018.9058
MLA
Alnaggar, M., Qaid, A. M., Chen, J., Niu, L., Xu, K."Irreversible electroporation of malignant liver tumors: Effect on laboratory values". Oncology Letters 16.3 (2018): 3881-3888.
Chicago
Alnaggar, M., Qaid, A. M., Chen, J., Niu, L., Xu, K."Irreversible electroporation of malignant liver tumors: Effect on laboratory values". Oncology Letters 16, no. 3 (2018): 3881-3888. https://doi.org/10.3892/ol.2018.9058