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The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis

  • Rong Xing , Yutong Liu , Yang Liu , Haihong Jiang , Chao Liu EMAIL logo and Jiru Du EMAIL logo
Published/Copyright: December 18, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

Both irreversible electroporation (IRE) and radiofrequency ablation (RFA) are viable ablation methods for localized treatment of liver tumors. We conducted a meta-analysis to access the efficacy and safety of IRE and RFA in liver cancer treatment. Clinical studies on IRE and RFA for the treatment of liver cancer were collected from PubMed and CNKI until June 2023. We screened the literature for ablation success rates at 1 month post-operation, extracting keywords such as “ablation success rate,” “technical success rate,” “recurrence rate,” and “complication” for meta-analysis. A total of 37 articles were included: 24 related to RFA involving 1,685 cases and 13 related to IRE involving 524 cases. The results demonstrate that ablation success rates at post-operative 1 month for IRE and RFA were 86% (95% CI: 82–89%) and 87% (95% CI: 81–92%), respectively. Technical success rates were 96% (95% CI: 88–100%) and 99% (95% CI: 96–100%). In addition, the recurrence rate was 16% (95% CI: 12–22%) in RFA group and 16% (95% CI: 9–23%) in IRE group. In terms of safety, the RFA had a complication rate of 28% (95% CI: 10–50%) and the IRE had a rate of 26% (95% CI: 13–43%). In conclusion, IRE and RFA exhibit similar ablation success rates at 1 month post-operation and comparable complication rates, making them both safe and effective treatment options.

Keywords: irreversible electroporation; radiofrequency; liver cancer; meta-analysis

1 Introduction

Liver cancer is a prevalent malignant tumor of the digestive system worldwide. According to the new data released by GLOBOCAN 2020, the global annual incidence of liver cancer has reached 906,000 new cases, with 830,000 deaths, ranking it sixth in incidence and third in mortality among malignant tumors. Both incidence and death are rising [1].

Clinicians typically choose treatment methods based on the tumor’s characteristics, the patient’s liver function, and overall health. If the focus is limited to the liver, surgical treatment (such as partial hepatectomy or liver transplantation) or local ablation is preferred. Systemic therapy is usually the treatment of choice for extrahepatic metastases [2]. Local ablation treatments mainly include radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation, laser ablation, irreversible electroporation (IRE), etc.

RFA is an earlier ablation method used in clinical studies. Its principle is to utilize a high-frequency electric current to excite the ions in the tissue to generate high-frequency oscillation, and the ions rub against each other and collide to generate heat, resulting in coagulation necrosis of tumor cells [3]. IRE is a novel non-thermal tumor ablation technique. Its principle is to generate a high external electric field by electrode needles in the target area, resulting in the formation of nanometer-sized pores in the cell membrane, causing cell apoptosis due to homeostasis imbalance [4]. Compared with RFA, IRE has two potential advantages [1]. It is tissue-selective due to varying electric field ablation thresholds, allowing it to preserve critical structures such as blood vessels, bile ducts, and nerves [2]. It lacks thermal deposition effects, preventing inadequate tissue damage near blood vessels due to uneven heating.

The ablation success rate is a key indicator for evaluating the efficacy of ablation techniques. It is defined as the absence of enhancement in the arterial phase of the ablated tumor lesion on dynamic contrast-enhanced CT or MRI scans, indicating complete tumor necrosis. Observing whether the tumor is completely ablated in the short-term postoperative period is a very important evaluation endpoint. It can not only reflect the short-term efficacy, but also provide an early reference for whether the patients require secondary ablation or other therapies as soon as possible. To date, no meta-analysis has specifically addressed the ablation success rate 1 month after ablation. Therefore, in order to assess the safety and efficacy of these two procedures, we concentrated on gathering data on the ablation success rate and complications about 1 month after RFA and IRE ablation.

2 Methods

2.1 Search strategy

All clinical studies on IRE and RFA for the treatment of liver cancer were searched from PubMed and CNKI since their database established until June 2023. The search terms were “Radiofrequency AND liver cancer” and “Irreversible Electroporation AND liver cancer,” and the language of the articles was limited to Chinese and English.

2.2 Inclusion and exclusion criteria

Inclusion criteria included: (1) patients with primary and metastatic liver cancer, (2) treatment with RFA/IRE technology, (3) clinical research, and (4) evaluation indexes include the success rate of ablation in about 1 month.

Exclusion criteria included: (1) repeated articles; (2) articles with unclear data sources; (3) reviews, conference articles, supporting materials, case reports, and patents; and (4) articles not containing content related to ablation success rate.

2.3 Data collection and synthesis

Two researchers independently reviewed the titles and abstracts of each study, as well as the full texts of studies that met the inclusion criteria. A standardized data collection form was used to extract key information, and any disagreements were resolved through discussion. The extracted data include the main author of the literature, publication year, study population characteristics, duration of follow-up, ablation success rate, technical success rate, recurrence rate, and complications.

The R4.1.3 meta-package was used for all of the meta-analyses. The I 2 statistic can be used to evaluate heterogeneity among research. When I 2 > 50% (P < 0.05), it may be assumed that there is heterogeneity, and the estimates should be summarized using the random effects model; when I 2 < 50% (P > 0.05), it can be assumed that the studies are homogeneous, and the fixed effects model is preferable to the random effects model. In this study, the results of the meta-analysis were presented using forest plots.

2.4 Literature quality evaluation

Of the included 37 studies, 10 were randomized controlled trials and 27 were cohort studies. Thus, we use the Cochrane ROB and Newcastle-Ottawa Score (NOS) to assess the quality of the included studies in meta-analyses. NOS was rated more than 6 stars, which is considered as relatively high-quality.

3 Results

Through database searches, 461 and 553 published articles were identified by RFA and IRE, respectively, and screened independently by two reviewers. The study flow and reasons for exclusion are detailed in Figure 1. A total of 37 articles were finally included, of which 24 were RFA and 13 were IRE.

Figure 1 Details of the study selection process.
Figure 1

Details of the study selection process.

3.1 Characteristics of included studies in the final analysis

A total of 37 studies were used to extract at least one result, and all of them gave information on the success rates of ablation. In addition, 11 of them provided information on technical success rates, 15 on recurrence rates, and 17 on complications. The characteristics of the included studies are described in Table 1.

Table 1

Characteristics of included studies

Studies Country No. of patients Patient age Data collection time Ablation rate (%) Adverse complications (%)
RFA
Liu [5] China 59 60 2003.09–2012.10 84.75 30.51
Huang et al. [6] China 146 54.4 2005.03–2009.03 85.62
Song [7] China 103 39–81 2010.09–2012.03 72.82
Fan and Li [8] China 41 NA 2011.01–2014.01 85.37
Du et al. [9] China 59 NA 2004.03–2006.03 81.36
Wang et al. [10] China 21 48.3 2010.01–2012.03 90.48 0.00
Song et al. [11] China 27 Group 1: 60.4 2004.01–2006.04 62.96
Group 2: 58.8
Liu et al. [12] China 106 Group 1: 54.5 2011.03–2012.03 75.47
Group 2: 52.5
Zhang et al. [13] China 20 61.4 2011.10–2013.03 80.00 100.00
Zhang et al. [14] China 57 Group 1: 55.3 2008.12–2010.10 92.98
Group 2: 57.8
Tang et al. [15] China 48 59.8 2014.01–2015.05 87.50
El-Kady et al. [16] Egypt 40 50.6 2008.05–2010.11 85.00
Azab et al. [17] Egypt 66 46–77 2005–2008 71.21
Giorgio et al. [18] Italy 13 70 2005.01–2008.01 76.92 23.08
Gadaleta et al. [19] Italy 51 70 2006.07–2007.10 88.24
Hou et al. [20] China 177 Group 1: 59.3 2003.01–2007.06 90.40 9.09
Group 2: 61.3
Wong et al. [21] China 208 66.3 2004.01–2006.08 88.94 22.73
Orlacchio et al. [22] UK 15 71.5 2009–2011 86.67 53.33
Poon et al. [23] China 80 Group 1: 63.5 2001.05–2002.10 91.25
Group 2: 64
Orlacchio et al. [24] Italy 8 72.43 2010.12–2013.10 87.50 75.00
Ruzzenente et al. [25] Italy 104 67.9 1998.01–2003.06 73.08 16.92
Abdelaziz et al. [26] Egypt 52 56.8 2009.02 94.23 11.11
Schullian et al. [27] UK 114 65.5 2003–2018 95.61 7.69
Di Costanzo et al. [28] Italy 70 70 2009.01–2012.09 97.14
IRE
Sutter et al. [29] France 75 65.4 2012.03–2015.06 77.33 18.97
Li et al. [30] China 28 58.7 2019.04–2019.09 96.43 17.39
Freeman et al. [31] Australian 33 65.2 2008.12–2019.10 87.88 69.57
Cheung et al. [32] Australian 18 70 2008.11–2009.12 72.22
Mafeld et al. [33] USA 59 64 2013–2017 74.58 17.31
Niessen et al. [34] Germany 103 63.5 2011.10–2015.07 92.23
Zhou et al. [35] China 24 21 2016.05–2019.06 79.17
Beyer et al. [36] Germany 19 60.3 2014.08–2015.08 94.74
Fang et al. [37] UK 69 NA 2014.02–2020.01 81.16
Eisele et al. [38] Germany 14 63 — 78.57
Niessen et al. [39] Germany 65 59.4 2011.12–2013.06 95.38 27.45
Thamtorawat et al. [40] Thailad 11 69.2 2014.01–2020.09 100.00 15.38
Cheng et al. [41] USA 6 61 2011–2013 83.33

3.2 Assessment of effectiveness outcomes

Data on ablation success rates 1 month following RFA were published in 24 studies (N = 1,685), with results ranging from 63 to 97%. The pooled proportion using a random effect model (I 2 = 74%, P < 0.01) was 86% (95% CI: 82–89%) (Figure 3). In contrast, only 13 studies (N = 524) of IRE provided data on ablation success rates ranging from 72 to 100%. Also employing a random effects model (I 2 = 62%, P < 0.01), the result was 87% (95% CI: 81–92%) (Figure 2).

Figure 2 Forest plot for complete ablation rate for (a) RFA and (b) IRE.
Figure 2

Forest plot for complete ablation rate for (a) RFA and (b) IRE.

Fewer studies reported the technical success rate, with seven (N = 315) studies in RF and four (N = 173) in IRE. The pooled technique success rate of RFA using a random effect model (I 2 = 85%, P < 0.01) was 96% (95% CI: 88–100%). There was no heterogeneity in the IRE meta-analysis (I 2 = 0%, P = 0.60), so the pooled proportion of the fixed-effect model was 99% (95% CI: 96–100%) (Figure 3).

Figure 3 Forest plot for technical success rate for (a) RFA and (b) IRE.
Figure 3

Forest plot for technical success rate for (a) RFA and (b) IRE.

RFA recurrence rates were reported in 11 research, ranging from 7 to 30%, with heterogeneity among research (I 2 = 64%, P < 0.01), so random-effects models were used, resulting in 16% (95% CI: 12–22%). IRE recurrence rates were reported in four research, ranging from 11 to 38%, with no heterogeneity among studies (I 2 = 29%, P = 0.24) and a fixed-effects model result was 16% (95% CI: 9–23%) (Figure 4).

Figure 4 Forest plot for recurrence rate for (a) RFA and (b) IRE.
Figure 4

Forest plot for recurrence rate for (a) RFA and (b) IRE.

3.3 Assessment of safety outcomes

In this study, only the total complication rate was analyzed. There were 11 research (N = 695) that reported total complication rates for RAF. The complication rates reported by different research ranged significantly from 0 to 100%, and I 2 also similarly showed a large heterogeneity between research (I 2 = 91%, P < 0.01). As a result, the pooled incidence rate using a random effect mode was 28% (95% CI: 10–50%). There were six studies (N = 220) that reported total complication rates for IRE, ranging from 15 to 70% with high heterogeneity (I 2 = 78%, P < 0.01), and the result of the random-effects model was 26% (95% CI: 13–43%) (Figure 5).

Figure 5 Forest plot for complications rate for (a) RFA and (b) IRE.
Figure 5

Forest plot for complications rate for (a) RFA and (b) IRE.

3.4 Risk of bias

Of the 37 articles, 27 cohort studies were assessed by NOS and found to be 6 and higher (Table 2), and the Cochrane ROB assessments of ten RCTs are shown in Figure 6. It is worth mentioning that since both RFA and IRE are surgical treatment methods, randomized controlled trials cannot meet the criteria for performance bias in Cochrane ROB.

Table 2

NOS of the included studies

Study Year Selection Comparability Outcome Quality scores (maximum 9)
Liu 2014 ** * *** 6
Huang 2009 ** * *** 6
Song 2012 ** * *** 6
Fan 2015 ** * *** 6
Du 2007 ** * *** 6
Wang 2014 ** * *** 6
Song 2008 *** * *** 7
Zhang 2013 ** * *** 6
Tang 2017 *** * *** 7
Schullian 2019 *** * *** 7
Sutter 2017 *** * *** 7
Freeman 2021 ** * *** 6
Cheung 2013 ** * *** 6
Mafeld 2019 *** * *** 7
Niessen 2017 *** * *** 7
Beyer 2016 *** * *** 7
Fang 2021 *** * *** 7
Thamtorawat 2022 *** * *** 7
Cheng 2015 ** * *** 6
GADALETA 2009 *** * *** 7
Poon 2004 *** * *** 7
Orlacchio 2014 ** * *** 6
Ruzzenente 2004 *** * *** 7
Zhou 2020 ** * *** 6
EISELE 2014 ** * *** 6
Wong 2008 *** * *** 7
Niessen 2016 ** * *** 6
Figure 6 Cochrane ROB result of included studies.
Figure 6

Cochrane ROB result of included studies.

4 Discussion

The treatment of liver cancer is characterized by multidisciplinary involvement and the coexistence of multiple treatment methods. Common treatment methods include hepatectomy, liver transplantation, ablation therapy, TACE, radiation therapy, systematic anti-tumor therapy, etc. By selecting appropriate treatment modalities for patients at different stages of liver cancer, the curative effect can be maximized. Although surgery is considered the first choice for the radical treatment of liver cancer, many patients suffer from varying degrees of cirrhosis and some cannot tolerate surgical intervention. In recent years, image-guided local ablation has become increasingly significant and widely used in the treatment of liver cancer due to the rapid development of minimally invasive interventional therapy technology. At present, commonly utilized ablation procedures including MWA and RFA are notable for their precise efficacy, less trauma, and minimal influence on liver function. In some patients with early liver cancer, similar results can be obtained as surgical resection (SR).

RFA is considered a viable alternative to SR as it uses high-frequency electrical currents to heat tissue, leading to the coagulative necrosis of tumor cells. However, when the temperature reaches 100°C, tissue desiccation (charring) occurs, which leads to an increase in tissue impedance and affects energy transfer. At the same time, the heat around the electrode will be lost with the adjacent blood perfusion, i.e., the “heat-sink” effect, which may lead to incomplete ablation [42]. The effectiveness of RFA in achieving complete tumor eradication depends on tumor size and location. Tumors adjacent to vessels larger than 3 mm in diameter have a higher risk of ablation failure and local tumor progression [43]. In 2005, Lu et al. found the average maximum diameter of successfully treated lesions was 2.0 cm, while that of failure was 3.1 cm, and only 47% of perivascular lesions were successfully treated [44]. Other clinical investigations’ findings have demonstrated that lesions located under the gallbladder pericardium or near the gallbladder have an increased risk of incomplete ablation and local recurrence [45,46]. Therefore, RFA has certain limitations in focal ablation therapy.

In contrast, IRE avoids the thermal deposition effect by perforating cell membranes with an electric field, making it tissue-selective and avoiding thermal ablation. As a result, lesions around bile ducts and perivascular can be removed without affecting their function [47]. The IRE device achieved a comparable ablation effect on liver cancer to that of RFA. It should be noted that the ablation time of IRE was significantly prolonged, which may be related to the large number of discharge electrodes, unstable heart rates, and interference of ECG synchronization during ablation [47]. Theoretically, IRE can solve the problem of ablating lesions in special areas. In pig experiment, Rubinsky et al. discovered that IRE could rapidly ablate tissue next to big venous systems while maintaining the structural integrity of the portal vein and bile ducts [48]. Additionally, animal experiments conducted by Charpentier et al. have shown that IRE could safely ablate periportal tissues without causing collateral damage to the bile ducts, hepatic arteries, and portal vein [49]. Numerous clinical trials have shown that IRE can safely ablate liver tumors near critical structures where thermal ablation is contraindicated [50,51]. A study by Thomson et al. on the safety of IRE in humans found that the adverse effects of IRE on blood vessels near tumors were acceptable [52]. A systematic review of IRE in patients with liver cancer showed that the complete response rate at 3 months ranged from 67 to 100% for tumors bigger than 3 cm and from 93 to 100% for tumors less than 3 cm, and reported no major adverse events [53].

The effectiveness and safety of RFA and IRE have previously been compared in several articles in terms of tumor ablation success, complication, and tumor recurrence rate [40,54,55]. There has been no other meta-analysis discussing the ablation success rate 1 month after ablation. In contrast, the General Office of the National Health and Wellness Commission of China’s Guidelines for the Diagnosis and Treatment of Primary Liver Cancer (2022 Edition) [56] recommends reviewing dynamic enhanced CT, multiparametric MRI scanning, or ultrasonography about a month after ablation to assess the ablation effect. The European Association for the Study of the Liver recommends that localized treatments need to be carefully evaluated by CT at least 4 weeks after surgery [57]. Additionally, in many clinical studies, researchers determine whether patients require a second ablation and develop follow-up treatment plans based on the ablation results observed 1 month after the procedure [16,28,29,32]. Therefore, short-term ablation success data around 1 month are crucial for clinical treatment strategies. This review focuses on literature reporting this metric and verifies that the effectiveness and safety of IRE are comparable to RFA, providing valuable evidence for clinical assessment of efficacy, patient follow-up, and prognosis after IRE. These data also serve as a reference for designing future clinical trial protocols for liver cancer ablation, including assumptions of success rates and sample size calculations.

In addition to the ablation success rate, this article analyzes the technical success rate, recurrence rate, and complication for both techniques. The results of the analysis of the 37 included articles showed that the success rates of IRE and RFA ablation after about 1 month were 86% (95% CI: 82–89%) and 87% (95% CI: 81–92%), respectively. Technical success rates were 96% (95% CI: 88–100%) and 99% (95% CI: 96–100%). In addition, the recurrence rate of RFA group was 16% (95% CI: 12–22%) and IRE group was 16% (95% CI: 9–23%). In terms of safety, the RFA had a complication rate of 28% (95% CI: 10–50%) and the IRE had a rate of 26% (95% CI: 13–43%). Radiofrequency has been on the market for more than 20 years now, both product technology and the skill of operating physicians are becoming more mature. As a newer technology, IRE products are continuously being improved, and the proficiency of physicians in performing the procedure is also increasing. This is reflected in the trend of rising ablation success rates for IRE, which have increased from 72% in previous years to 100% in 2020.

In conclusion, the results of these studies selected in this meta-analysis showed that IRE ablation for liver cancer is safe and effective, and its ablation success rate and complication rate are similar to those of RFA. We anticipate that, with ongoing clinical practice and application, this technique will continue to reduce complication rates and achieve even better outcomes.

5 Conclusion

In patients with liver cancer receiving focal therapy, the ablation success rate of IRE was similar to RFA at about 1 month after surgery. IRE can also ablate some special sites, which has a broad development prospect in the treatment of solid tumors.

Acknowledgements

The authors would like to thank the ChatGPT model for its assistance in refining the grammar and language of this manuscript.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and consented to its submission to the journal, reviewed all the results and approved the final version of the manuscript. Rong Xing is responsible for methodology, data analysis, and article writing; Yutong Liu is responsible for data analysis and article writing; Yang Liu and Haihong Jiang participated in data analysis; Chao Liu and Jiru Du were responsible for methodology, article review, and finalizing the draft.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-03-07
Revised: 2024-09-09
Accepted: 2024-09-25
Published Online: 2024-12-18

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
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https://doi.org/10.1515/biol-2022-0991
Keywords for this article
irreversible electroporation; radiofrequency; liver cancer; meta-analysis
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
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  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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