Abstract
To investigate the effect of radical hepatectomy on the prognosis of patients with hepatic alveolar echinococcosis (HAE) complicated with microvascular invasion (MVI). HAE patients who underwent radical hepatectomy at the Echinococcosis Diagnosis and Treatment Center of Qinghai Provincial People’s Hospital from January 2014 to December 2020 were collected in this study according to the inclusion and exclusion criteria. The clinical data of the patients were collected and analyzed. According to the surgical method, the patients were divided into anatomical hepatectomy group (Anatomical group) and non-anatomical hepatectomy group (Non-anatomical group). Kaplan-Meier survival analysis was used to compare the 5-year recurrence-free survival (RFS) between the two groups. A total of 375 patients were enrolled in the study (with 185 in Anatomical group and 190 in Non-anatomical group). The results of clinicopathological data analysis showed that compared with the Non-anatomical group, the patients in the Anatomical group had less intraoperative blood loss and blood transfusion, and a lower postoperative recurrence rate (all P < 0.05). The survival analysis results showed that the overall survival of the enrolled patients was 92.9%. Compared with the Non-anatomical group, the 5-year RFS of the Anatomical group was higher (98% vs. 87.7%, P < 0.05). Besides, In the Anatomical group, the 5-year RFS of patients with negative MVI was better than that of patients with positive MVI (100% vs. 94.5%, P < 0.05). Similarly, in the Non-anatomical group, the 5-year RFS of patients with negative MVI was also superior to that of patients with positive MVI (99% vs. 75.8%, P < 0.05). In addition to surgical methods, MVI may be another important factor affecting the 5-year RFS of patients with HAE.
Keywords: Hepatic alveolar echinococcosis, Anatomical, Liver resection, Microvascular invasion, Recurrence
Subject terms: Oncology, Surgical oncology
Introduction
Hepatic alveolar echinococcosis (HAE) is a zoonotic parasitic disease caused by the infection of the liver with Echinococcus multilocularis, which has a relatively high mortality and disability rate1–4. Currently, the most effective treatment for HAE remains radical hepatectomy5,6. Studies have shown that the 5-year cumulative survival rate of HAE patients after radical hepatectomy can be as high as 95%−98%, while the 5-year recurrence-free survival rate is 76%7,8. Therefore, even after undergoing radical hepatectomy, HAE patients still have a relatively high recurrence rate9,10. Some scholars have pointed out11 that the recurrence of lesions in HAE patients after surgery is related to the surgical method and the selection of surgical margins. The results of a single-center study12 showed that the recurrence rate of HAE patients who underwent anatomical hepatectomy was significantly lower than that of those who underwent non-anatomical hepatectomy. Anatomical hepatectomy is not only safe and reliable for the treatment of HAE, but also can achieve better long-term efficacy13.
A number of studies14,15 have indicated that the high recurrence rate of HAE after surgery is associated with the failure to completely resect the invasive zone adjacent to the lesion during the operation. The invasive zone refers to the liver tissue approximately 1.0 cm around the HAE lesion. This area is rich in microvessels dominated by the portal vein, which serves as the basis for the proliferation and invasion of alveolar echinococcal lesions16.
Based on the pathological characteristics of the tissue in the invasive zone adjacent to the lesion, this article will take the surgical method and the patient’s recurrence-free survival rate as the main observation indicators to further elaborate on the relationship between the surgical method, microvascular invasion (MVI), and postoperative recurrence in HAE patients, aiming to explore the key mechanisms of postoperative recurrence of HAE at a deeper level.
Methods
General information
The general and clinical data of 426 patients with HAE who underwent hepatectomy at the Hydatid Disease Diagnosis and Treatment Center of Qinghai Provincial People’s Hospital from January 2014 to December 2020 were collected and analyzed through collaboration between the HIS system and medical records room of Qinghai Provincial People’s Hospital. General information included: name, admission number, gender, age, ethnicity, region, epidemiological data (history of close contact with cattle, sheep, and dogs).
This study was approved by the Ethics Committee of Qinghai Provincial People’s Hospital and complied with the Collection of Human Genetic Resources regulations set by the Ministry of Science and Technology of the People’s Republic of China (No. 2022SLCJ1332). All methods were performed in accordance with the relevant guidelines and regulations.
Inclusion and exclusion criteria for enrolled patients
The inclusion criteria were as follows: (1) HAE was confirmed through pathological diagnosis. (2) The PNM classification according to WHO/IWGE guidelines was P1 − 3N0 − 1M0. (3) All patients underwent primary liver surgery. (4) None of the patients had liver cirrhosis, and their preoperative liver function was classified as Child-Pugh grade A or B. Patients with grade B liver function were reassessed after treatment, and those whose liver function improved to grade A were included in the study. (5) Open hepatectomy was performed on all patients. (6) All patients were prescribed albendazole as per the expert consensus protocol. The exclusion criteria were as follows: (1) Exclusion of patients who underwent inferior vena cava replacement or ex vivo liver resection combined with autologous liver transplantation (n = 21); (2) Exclusion of patients who underwent palliative lesion resection (n = 17); (3) Exclusion of patients with intracranial, thoracic, and retroperitoneal distant metastasis (n = 4). (4) Exclusion of patients lost to follow-up (n = 5) or those who died accidentally during the study period (n = 4; 3 cases due to traffic accidents and 1 case due to cerebral hemorrhage). According to the inclusion and exclusion criteria, a total of 375 patients were ultimately enrolled in this study. Based on different surgical methods, the patients were categorized into two groups: non-anatomical hepatectomy group (Non-anatomical group) and anatomical hepatectomy group (Anatomical group).
Collection of clinical data
Clinical data included the echinococcosis enzyme-linked immunosorbent assay (ELISA) (echinococcosis antibody IgG titer), alanine aminotransferase (ALT), Child-Pugh classification, PNM staging (the standard staging system for HAE established by WHO/IWGE), and surgical method. According to the postoperative pathological results, whether HAE patients were combined with MVI was determined. The definition of MVI is under the microscope, alveolar echinococcosis or small lesions were observed in the microvascular lumen of the infiltrating zone16.
Preoperative evaluation and surgical methods
All 375 patients underwent enhanced head-thorax-abdomen computed tomography (CT) scan, hepatic computed tomography angiography (CTA), echinococcosis ELISA (echinococcosis antibody IgG), and 8-item infectious disease test after admission. Preoperative evaluation included assessment of liver reserve function, residual liver volume, and the relationship between lesions and blood vessels/bile ducts. The methods for evaluating liver reserve function mainly included Child-Pugh classification and indocyanine green retention rate at 15 min (ICGR15). The evaluation of residual liver volume was mainly calculated based on enhanced liver CT.
Anatomical hepatectomy refers to precise resection according to the portal vein blood supply regions of the liver, ensuring that the resection range is completely consistent with a complete anatomical unit. Non-anatomical hepatectomy does not strictly follow the portal vein anatomical regions; instead, it only resects “local liver tissue containing the lesion” based on the location and size of the lesion. The resection range may cross anatomical units or be only local wedge-shaped/irregular tissue. The Pringle maneuver occludes the entire blood flow within the hepatoduodenal ligament, meaning it blocks the hepatic inflow (hepatic artery and portal vein) simultaneously while leaving the hepatic outflow (hepatic veins) unaffected. The Glisson maneuver blocks the branches of the Glisson system in a specific region of the liver, achieving “regional hepatic blood flow occlusion”.
Postoperative management
Patients in both groups received postoperative analgesia using an intravenous analgesic pump combined with subcutaneous injection of analgesics. The volume of postoperative intravenous infusion was controlled at approximately 2000 mL. Patients were allowed to drink water after regaining consciousness from anesthesia, and early ambulation was encouraged. During postoperative hospitalization, since the patients’ liver function was still in the recovery period, albendazole treatment was temporarily not administered. For discharged patients, albendazole treatment was strictly implemented in accordance with the Guidelines for the Treatment of Echinococcosis. The dosage for adults was 100 mg/kg per day, taken together with liver-protecting drugs (commonly used: Hugan Tablets). After 2–3 weeks of continuous medication, the liver function was reexamined. If there was liver injury, the drug was stopped immediately for liver protection treatment. After treatment, the liver function was reexamined to return to normal range to start the next course of treatment, and the medication cycle was at least 2 years. After 2 years, the decision to discontinue the drug was made based on the echinococcosis antibody IgG titer17,18.
Postoperative follow-up
Within 2 years after discharge, reexaminations were conducted every 6 months; after 2 years, reexaminations were performed every 12 months. The reexamination items mainly included echinococcosis ELISA, liver and kidney function tests, abdominal color Doppler ultrasound, or abdominal CT plain scan (a full abdominal CT scan was performed every 12 months). The diagnostic criteria for recurrence of echinococcosis were: New echinococcal lesions in the liver detected by imaging examination, combined with positive echinococcosis ELISA. Recurrence was classified into margin recurrence and distant intrahepatic recurrence based on the recurrence site. Margin recurrence refers to recurrence where the edge of the new lesion is within 2.0 cm of the residual liver section, while distant intrahepatic recurrence refers to recurrence where the edge of the new lesion is more than 2.0 cm from the residual liver section. The treatment of recurrent echinococcal lesions was carried out in accordance with the WHO Guidelines for the Diagnosis and Treatment of Echinococcosis, including medication, reoperation, and comprehensive treatment. The selection of the treatment plan was determined based on the actual conditions of the lesions and the patients. The long-term efficacy of patients was obtained through follow-up records, telephone follow-up, or face-to-face follow-up, with a median follow-up time of 60 months.
Statistical methods
SPSS 25.0 statistical software was used for data processing. One-sample Kolmogorov-Smirnov test (two-sided test) and Shapiro-Wilk test were used to analyze the normal distribution of measurement data. Measurement data conforming to normal distribution were expressed as mean ± standard deviation (
). Measurement data with non-normal distribution were expressed as M (Q25, Q75), and comparison between the two groups was analyzed using the Mann-Whitney U test. The Mann-Whitney U test was used for ordinal data. Enumeration data were analyzed by four-fold table X2 test or row × table X2 test. The receiver operating characteristic (ROC) curve was used to analyze the cut-off value of the indicators under the maximum Youden index, as well as its sensitivity and specificity. Kaplan-Meier survival analysis was used to compare the recurrence rate of HAE in different groups. Binary Logistic regression model was used to analyze the independent risk factors of HAE recurrence. P<0.05 was considered statistically significant.
Results
Analysis of baseline characteristics of enrolled patients
The patients were divided into Anatomical group (n = 185) and Non-anatomical group (n = 190). The preoperative, intraoperative and postoperative indexes of the two groups were compared. The results showed that the intraoperative blood loss and blood transfusion in the Anatomical group were significantly less than those in the Non-anatomical group (P < 0.05). The hepatic portal occlusion time in the Anatomical group was significantly shorter than that in the Non-anatomical group (P < 0.05). Glissonian pedicle occlusion was the main method of hepatic blood inflow occlusion in the anatomical group, while Pringle total hepatic blood flow occlusion was the main method in the Non-anatomical group, and the difference was statistically significant (P < 0.05). The recurrence rate of the anatomical group was significantly lower than that of the Non-anatomical group (P < 0.05). There was no significant difference in other clinical indicators (P > 0.05) (Tables 1 and 2).
Table 1.
Comparison of clinical data between anatomical group and non-anatomical group (Counting index).
| Indicators | Non-anatomical group(n = 190) | Anatomical group(n = 185) | X2/Z | P |
|---|---|---|---|---|
| Gender | ||||
| Male | 86 | 78 | 0.366 | 0.545 |
| Female | 104 | 107 | ||
| Ethnic groups | ||||
| Han | 10 | 12 | 0.362 | 0.834 |
| Zang | 176 | 170 | ||
| Hui | 4 | 3 | ||
| HBsAg | ||||
| Positive | 76 | 62 | 1.696 | 0.193 |
| Negative | 114 | 123 | ||
| Child-Pugh classification | ||||
| Grade A | 146 | 154 | 2.400 | 0.121 |
| Grade B | 44 | 31 | ||
| Location of the lesion(s) | ||||
| Left lobe of liver | 42 | 48 | 1.698 | 0.428 |
| Right lobe of liver | 89 | 90 | ||
| Left and right lobes of the liver | 59 | 47 | ||
| PNM typing | ||||
| P1N0M0 | 20 | 22 | 1.625 | 0.104 |
| P1N1M0 | 10 | 10 | ||
| P2N0M0 | 30 | 35 | ||
| P2N1M0 | 87 | 91 | ||
| P3N0M0 | 24 | 17 | ||
| P3N1M0 | 19 | 10 | ||
| Occlusion of hepatic blood flow | ||||
| Pringle | 183 | 7 | 328.572 | 0.001 |
| Glissonian | 5 | 180 | ||
| Surgical margin | ||||
| Wide margins | 96 | 96 | 0.070 | 0.791 |
| Narrow margins | 94 | 89 | ||
| MVI | ||||
| Positive | 73 | 68 | 0.111 | 0.739 |
| Negative | 117 | 117 | ||
| Relapse | ||||
| Yes | 46 | 24 | 7.797 | 0.005 |
| No | 144 | 161 |
Table 2.
Comparison of clinical data between anatomical group and non-anatomical group (Measurement index).
| Indicators | Non-anatomical group(n = 190) | Anatomical group(n = 185) | Z | P |
|---|---|---|---|---|
| Age (years) | 36(26, 48) | 36(23, 48) | 0.621 | 0.534 |
| ICGR15(%) | 4.3(2.2, 7.0) | 4.4(2.1, 7.7) | 0.395 | 0.693 |
| Lesion size(centimeter) | 10.0(7.0, 13.3) | 10.0(7.0, 13.0) | 0.572 | 0.567 |
| Number of lesions(Number) | 1(1, 1) | 1(1, 1) | 0.151 | 0.880 |
| IgG titer of hydatid antibody | 2.7(1.5, 4.3) | 2.5(1.6, 4.1) | 0.563 | 0.573 |
| ALT(U/L) | 27(16, 45) | 27(14, 49) | 0.641 | 0.522 |
| AST(U/L) | 26(19, 41) | 25(19, 38) | 0.661 | 0.509 |
| TBIL(umol/L) | 11.2(8.7, 15.8) | 11.5(8.6, 18.6) | 0.650 | 0.515 |
| ALP(U/L) | 126(91, 207) | 143(96, 227) | 1.173 | 0.241 |
| CHE(U/L) | 6782(5451, 8160) | 6713(5567, 7966) | 0.838 | 0.402 |
| ALB(g/L) | 35.7(31.5, 38.3) | 35.6(32.7, 38.2) | 0.418 | 0.676 |
| GGT(U/L) | 57(30, 114) | 46(26, 105) | 1.225 | 0.220 |
| Ca(mmol/L) | 2.2(2.1, 2.3) | 2.2(2.1, 2.3) | 0.583 | 0.560 |
| Na(mmol/L) | 138(136, 139) | 138(136, 139) | 1.299 | 0.194 |
| PLT(109/L) | 260(198, 332) | 254(206, 319) | 0.308 | 0.758 |
| Operation duration(hours) | 6(5, 7) | 6(5, 7) | 1.015 | 0.310 |
| Intraoperative blood loss(mL) | 400(200, 800) | 150(300, 600) | 2.556 | 0.011 |
| Intraoperative blood transfusion volume(mL) | 0(0, 1030) | 0(0, 610) | 3.220 | 0.001 |
| Duration of hepatic portal occlusion(minutes) | 35(20, 49) | 25(15, 35) | 4.789 | 0.001 |
ICG-R15: Indocyanine green excretion test was performed for 15 min. ALT: Alanine aminotransferase. AST: Aspartate aminotransferase. TBIL: Total bilirubin. ALP: Alkaline phosphatase. CHE: Cholinesterase. ALB: Albumin. GGT: Gamma-glutamyl transpeptidase. Ca: Calcium. Na: Natrium. PLT: Platelet.
Prognostic analysis of patients in the anatomical group and non-anatomical group
After following up with the enrolled cases, we found that the 5-year survival rates of patients in both groups were very high, and none of the discharged patients died due to complications related to HAE. However, when the Kaplan-Meier survival analysis was used to compare the survival of all enrolled patients, the results showed that the 5-year RFS of the enrolled patients was 92.9% (Fig. 1). The 5-year RFS of patients in the Anatomical resection group was 98%, and that of patients in the Non-anatomical resection group was 87.7%. The results indicated that the 5-year RFS of patients with HAE who underwent anatomical hepatectomy was significantly better than that of patients who underwent non-anatomical hepatectomy (P < 0.05) (Fig. 2).
Fig. 1.
5-year recurrence-free survival of all enrolled patients.
Fig. 2.
5-year recurrence-free survival curves of patients in the Anatomical and Non-anatomical groups.
The relationship between MVI and prognosis in patients with hepatic alveolar echinococcosis
In the Anatomical group, the 5-year RFS was 94.5% for patients with positive MVI and 100% for those with negative MVI (Fig. 3). The results showed that the 5-year RFS of patients with negative MVI in the Anatomical group was superior to that of patients with positive MVI (P < 0.05). In the Non-anatomical group, the 5-year RFS was 75.8% for patients with positive MVI and 99% for those with negative MVI. The results indicated that the 5-year RFS of patients with negative MVI in the Non-anatomical group was also better than that of patients with positive MVI (P < 0.05) (Fig. 4).
Fig. 3.
5-year recurrence-free survival curves for MVI-positive and MVI-negative patients in the anatomical group. MVI: microvascular invasion.
Fig. 4.
5-year recurrence-free survival curves for MVI-positive and MVI-negative patients in the non-anatomic group. MVI: microvascular invasion.
Discussion
Studies have shown19 that radical hepatectomy can effectively prolong the RFS of patients with HAE. Currently, prognostic studies on HAE patients mainly focus on surgical methods and drug therapy20–24. Studies have clearly indicated25 that the postoperative recurrence of HAE is mainly associated with the completeness of lesion resection during surgery, especially the resection of micro-metastases within the invasive zone around the lesions. Wen Hao et al.26 argued that the primary cause of recurrence in HAE lies in the quality control of surgical margins. Shabunin et al.27 explicitly pointed out that in radical surgery for HAE, more than 2.0 cm of normal liver tissue around the lesion should be resected. However, domestic experts in echinococcosis diagnosis and treatment held discussions and reached a consensus: while completely removing the echinococcal lesion, it is recommended to resect more than 1.0 cm of normal liver tissue at the edge of the lesion28. The aforementioned studies only indicated that the invasive zone is associated with the recurrence of HAE, without further exploring the specific mechanism by which the invasive zone leads to recurrence29,30.
In this study, MVI was used to confirm the rationality of anatomical hepatectomy in the treatment of HAE. Conversely, the effectiveness of anatomical hepatectomy on the prognosis of patients with MVI was used to verify the reliability of MVI in evaluating patient prognosis. For instance, this study compared the incidence of MVI between patients in the Anatomical and Non-anatomical hepatectomy groups, and the results showed no difference between the two groups. However, when a comprehensive analysis of surgical methods, MVI status, and postoperative recurrence rate was conducted based on this finding, it was observed that patients with positive MVI and those with negative MVI had different RFS after undergoing the same surgical procedure. Specifically, the RFS of patients with positive MVI who underwent either anatomical or non-anatomical hepatectomy was significantly lower than that of patients with negative MVI. Therefore, anatomical hepatectomy should be performed for HAE patients with MVI, as it can effectively improve the postoperative RFS. In short, anatomical hepatectomy can significantly improve the recurrence-free survival rate of patients with HAE, and this advantage is more pronounced especially in patients complicated with MVI. Although this study only explored the recurrence mechanism of HAE from the perspective of surgical treatment, it also provides a brand-new direction for the research and development of anti-echinococcosis drugs specifically, the transformation of traditional anti-echinococcosis drugs from focusing on parasite elimination to vascular inhibition, as well as the repositioning of the scope of drug therapy.
Nevertheless, this study still has some limitations, such as insufficient elimination of confounding factors, limited sample size, the lack of multi-center and large-data verification, the absence of clinical follow-up data, and the fact that some theories still require further clinical validation. In the follow-up study, we will carry out prospective, multi-center, large sample clinical studies as far as possible to further verify the results of this study.
Conclusion
In conclusion, anatomical hepatectomy can significantly improve the RFS of patients with HAE, and this advantage is more pronounced especially in patients complicated with MVI. In addition to surgical methods, MVI may be another important factor affecting the 5-year RFS of patients with HAE.
Acknowledgements
We gratefully acknowledge the helpful suggestions of the reviewers, which have improved the paper.
Author contributions
Thanks to all authors for their contributions to this article. Jide A and Dongye Li conceived and designed the study. Jide A and Jinping Chai collected the data. Genkui Li and Li Yuan contributed to data analysis and interpretation, Jide A writing article. Jinping Chai and Li Yuan approved the study and this submission.
Funding
This work was supported by the High-end Innovative Talent Project of Kunlun Talents of Qinghai Province in 2024 (Qingrencai Zi [2025] No. 5); Special Project of the High-level Health Talent Training Program Jointly Conducted by Qinghai Provincial People’s Hospital and Soochow University(No: 2025-qhsrmyysd-01); National Natural Science Foundation of China(No: 82260412).
Data availability
All data generated or analysed during this study are included in this published article (and its Supplementary Information files).
Declarations
Competing interests
The authors declare no competing interests.
Ethics
The study involving human participants was reviewed and approved by the Ethics Committee of the Qinghai Provincial People’s Hospital (Approval numbers: 2020 − 138). Written informed consent to participate in this study was provided by the participants’ legal guardian/next of kin.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Jide A and Dongye Li contributed equally to this work.
Contributor Information
Jinping Chai, Email: chaijinping0524@163.com.
Li Yuan, Email: 930426991@qq.com.
References
- 1.Tang, J. C. et al. Monosegmental ALPPS combined with ante-situm liver resection: A novel strategy for end-stage hepatic alveolar echinococcosis. Hepatobiliary Pancreat. Dis. Int.21(2), 186–189 (2022). [DOI] [PubMed] [Google Scholar]
- 2.Gottstein, B. & Deplazes, P. Alveolar echinococcosis: what triggers emergence in North America, Central Europe and Asia?. Curr. Opin. Infect. Dis.34(5), 440–446. 10.1097/QCO.0000000000000765 (2021). [DOI] [PubMed] [Google Scholar]
- 3.Dušek, D. et al. Human alveolar Echinococcosis, Croatia. Emerg. Infect. Dis.26 (2), 364–366. 10.3201/eid2602.181826 (2020). PMID: 31961317; PMCID: PMC6986858. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Šimeková, K. et al. Alveolar echinococcosis of the liver with a rare infiltration of the adrenal gland. Helminthologia58 (1), 100–105. 10.2478/helm-2021-0002 (2021). PMID: 33664623; PMCID: PMC7912238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Qu, B. et al. Management of advanced hepatic alveolar echinococcosis: report of 42 cases. Am. J. Trop. Med. Hyg.96 (3), 680–685. 10.4269/ajtmh.16-0557 (2017). Epub 2017 Apr 6. PMID: 28070011; PMCID: PMC5361545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Jiang, T. et al. Collateral circulation caused by end-stage hepatic alveolar echinococcosis. BMC Infect. Dis.23 (1), 322. 10.1186/s12879-022-07970-7 (2023). PMID: 37189056; PMCID: PMC10184362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Zhang, R. Q. The clinical analysis for different surgical treatment against human hepatic alveolar echinococcosis. Xinjiang Med. Univ.10.7666/d.D601387 (2013). [Google Scholar]
- 8.Mairanmunisha·Tuerxun. The Clinical Analysis for Surgical Treatments against Human Hepatic AlveolarEchinococcosis (Xinjiang Medical University, 2016).
- 9.Gloor, S., Candinas, D., Beldi, G. & Lachenmayer, A. Laparoscopic resection of hepatic alveolar echinococcosis: A single-center experience. PLoS Negl. Trop. Dis.16 (9), e0010708. 10.1371/journal.pntd.0010708 (2022). PMID: 36067177; PMCID: PMC9447893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Maimaiti Wasili. The influence of different surgical margins on postoperative recurrence of the hepatic alveolar echinococcosis. Xinjiang Med. Univ., doi:CNKI:CDMD:2.1018.212403. (2018).
- 11.He, W., Liu, X. G., Wang, G., Lu, J. L. & Ye, Z. Radical surgery for treatment of patients with hepatic alveolus echinococcosis[J]. J. Practical Hepatol.25 (3), 435–438. 10.3969/j.issn.1672-5069.2022.03.033 (2022). [Google Scholar]
- 12.Zhang, A. J. et al. Comparison of the efficacy of anatomic and Non-anatomic hepatectomy for hepatic alveolar echinococcosis: clinical experience of 240 cases in a single center. Front. Public. Health9, 816704. 10.3389/fpubh.2021.816704 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Wan, L. et al. Laparoscopic or open treatment for hepatic alveolar echinococcosis: A single-institution experience. Int. J. Infect. Dis.107, 182–187. 10.1016/j.ijid.2021.04.017 (2021). Epub 2021 Apr 20. PMID: 33862206. [DOI] [PubMed] [Google Scholar]
- 14.Buttenschoen, K. et al. Long-term experience on surgical treatment of alveolar echinococcosis. Langenbecks Arch. Surg.394 (4), 689–698. 10.1007/s00423-008-0392-5 (2009). Epub 2008 Jul 24. PMID: 18651165. [DOI] [PubMed] [Google Scholar]
- 15.Hillenbrand, A. et al. Impact of Safe Distance on Long-Term Outcome After Surgical Therapy of Alveolar Echinococcosis. World J. Surg.41(4), 1012–1018. 10.1007/s00268-016-3813-6 (2017). [DOI] [PubMed] [Google Scholar]
- 16.Chai, A. J. D., Zhao, J. P., Yang, S. Y. A. X. R. & An, J. Y. Research progress on infiltrating zone and microvascular invasion of hepatic alveolar echinococcosis. Chin. J. Prev. Med.56 (10), 1514–1519. 10.3760/cma.j.cn112150-20211118-01062 (2022). [DOI] [PubMed] [Google Scholar]
- 17.Siles-Lucas, M., Casulli, A., Cirilli, R. & Carmena, D. Progress in the Pharmacological treatment of human cystic and alveolar echinococcosis: compounds and therapeutic targets. PLoS Negl. Trop. Dis.12 (4), e0006422. 10.1371/journal.pntd.0006422 (2018). PMID: 29677189; PMCID: PMC5931691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Vuitton, D. A. et al. Current interventional strategy for the treatment of hepatic alveolar echinococcosis. Expert Rev. Anti Infect. Ther.14(12), 1179–1194 (2016). [DOI] [PubMed] [Google Scholar]
- 19.Wen, H. et al. Ex vivo liver resection followed by autotransplantation for end-stage hepatic alveolar echinococcosis. Chin. Med. J. (Engl)124(18), 2813–2817 (2011). [PubMed] [Google Scholar]
- 20.Chai, A. J., Shao, J., Zhao, Z. & Wang, S. Comparison of local ablation with albendazole or laparoscopic hepatectomy combined with albendazole in the treatment of early hepatic alveolar echinococcosis. Front. Public. Health. 10, 960635. 10.3389/fpubh.2022.960635 (2022). PMID: 36276387; PMCID: PMC9580460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.He, J., Yang, C. & Wang, W. Treatment of retroperitoneal echinococcosis: the experience of a single center. Med. (Baltim).100 (8), e24744. 10.1097/MD.0000000000024744 (2021). PMID: 33663088; PMCID: PMC7909149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Hu, C., Zhang, F. & Fan, H. Improvement of the bioavailability and Anti-hepatic alveolar echinococcosis effect of Albendazole-Isethionate/Hypromellose acetate succinate (HPMC-AS) complex. Antimicrob. Agents Chemother.65 (7), e0223320. 10.1128/AAC.02233-20 (2021). Epub 2021 Jun 17. PMID: 33875425; PMCID: PMC8218690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Zavoikin, V. D., Zelya, O. P. & Tumolskaya, N. I. The importance of uninterrupted albendazole treatment in patients with unresectable alveolar echinococcosis undergoing liver transplantation. Transpl. Infect. Dis.22 (4), e13291. 10.1111/tid.13291 (2020). Epub 2020 Apr 23. PMID: 32277859. [DOI] [PubMed] [Google Scholar]
- 24.Bresson-Hadni, S. et al. Primary disease recurrence after liver transplantation for alveolar echinococcosis: long-term evaluation in 15 patients. Hepatology30(4), 857–864. 10.1002/hep.510300426 (1999). [DOI] [PubMed] [Google Scholar]
- 25.Ayifuhan, A. et al. Surgical treatment for hepatic alveolar echinococcosis: report of 50 cases. Hepatogastroenterology59(115), 790. 10.5754/hge10545 (2012). [DOI] [PubMed] [Google Scholar]
- 26.Wen, H. et al. Clinical analysis of surgical treatment for human hepatic cystic and alveolar echinococcosis. Chin. J. Dig. Surg.6 (1), 13–18. 10.3760/cma.j.issn.1673-9752.2007.01.010 (2007). [Google Scholar]
- 27.ShabuninAV, TavobilovMM & KarpovAA Ekhinokokkoz pecheni: Evolyutsiya Khirurgicheskogo Lecheniya [Echinococcosis of the liver: evolution of surgical treatment]. Khirurgiia (Mosk). (5), 95–103. 10.17116/hirurgia202105195 (2021). [DOI] [PubMed]
- 28.Wen, H. Applied Hydatid Disease 226–227 (Science, 2007).
- 29.Sun, Y. Quantitative Analysis of Hepatic Alveolar Echinococcosis by Dynamic contrast-enhanced Magnetic Resonance Imaging (Qinghai University, 2018).
- 30.Yang, X. et al. Magnetic resonance imaging evaluation of characteristics of vascular invasion in intermediate and advanced hepatic alveolar echinococcosis. Exp. Ther. Med.17 (5), 4197–4204. 10.3892/etm.2019.7460 (2019). Epub 2019 Apr 1. PMID: 31007751; PMCID: PMC6468930. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
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Data Availability Statement
All data generated or analysed during this study are included in this published article (and its Supplementary Information files).