Retrospective Study Open Access
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World J Gastrointest Surg. Jun 27, 2025; 17(6): 105007
Published online Jun 27, 2025. doi: 10.4240/wjgs.v17.i6.105007
Simultaneous combined surgery for hepatic-renal double organ alveolar or cystic echinococcosis: A retrospective study
Alimu Tulahong, Da-Long Zhu, Chang Liu, Tie-Min Jiang, Rui-Qing Zhang, Talaiti Tuergan, Tuerganaili Aji, Ying-Mei Shao, Department of Hepatobiliary and Echinococcosis Surgery, The First Affiliated Hospital of Xinjiang Medical University, Urumqi 830054, Xinjiang Uygur Autonomous Region, China
ORCID number: Alimu Tulahong (0000-0002-7680-8634); Da-Long Zhu (0000-0002-0632-6816); Tuerganaili Aji (0000-0001-6737-8874); Ying-Mei Shao (0000-0001-5154-345X).
Co-first authors: Alimu Tulahong and Da-Long Zhu.
Co-corresponding authors: Tuerganaili Aji and Ying-Mei Shao.
Author contributions: Tulahong A, Zhu DL, Shao YM, and Aji T conceived and designed the study; Tulahong A obtained partial funding for the research; Jiang TM, Zhang RQ, Tuergan T, and Liu C were responsible for data acquisition, preliminary analysis, and interpretation, participating in the discussion and revision of the manuscript to ensure the accuracy and reliability of the data interpretation. Tulahong A and Zhu DL organized the collected data, performed re-analysis, created figures, conducted literature searches, and completed the draft manuscript, making critical contributions that qualify them as co-first authors. Aji T and Shao YM supervised the research process, provided methodological guidance, and played key roles in ensuring the integrity and ethical considerations of the research. They were also responsible for applying for and obtaining funding for this research project. As the main implementers of the surgical plan, they made significant contributions to the design and execution of complex cases, co-revised the manuscript, and participated in discussions and interpretations of the research results. Given their contributions and responsibilities for this research, they are listed as co-corresponding authors. Shao YM managed the submission of the manuscript and coordinated subsequent revisions. All authors have read and approved the final manuscript.
Supported by the National Natural Science Foundation of China, No. 82360111; Xinjiang Science and Technology Department-Leading Talents in Technological Innovation - High-Level Leading Talents, No. 2022TSYCLJ0034; State Key Laboratory for The Cause and Control of High Incidence in Central Asia Jointly Constructed by The Ministry and The Province, No. SKL-HIDCA-2023-2 and No. SKL-HIDCA-2024-22; and Xinjiang Uygur Autonomous Region Graduate Innovation Program, No. XJ2024G153.
Institutional review board statement: The study was reviewed and approved by The First Affiliated Hospital of Xinjiang Medical University Institutional Review Board, No. K202202-04.
Informed consent statement: Informed consent was waived.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: All data from this study are included in the article and its supplementary materials, available for readers to review and use.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Ying-Mei Shao, MD, PhD, Chief Physician, Professor, Department of Hepatobiliary and Echinococcosis Surgery, The First Affiliated Hospital of Xinjiang Medical University, No. 393 Xinyi Road, Urumqi 830054, Xinjiang Uygur Autonomous Region, China. syingmei1@163.com
Received: January 12, 2025
Revised: March 19, 2025
Accepted: March 20, 2025
Published online: June 27, 2025
Processing time: 138 Days and 3.3 Hours

Abstract
BACKGROUND

Alveolar and cystic echinococcoses are lethal zoonotic diseases caused by Echinococcus multilocularis and Echinococcus granulosus infections, leading to alveolar echinococcosis (AE) or cystic echinococcosis (CE), respectively. No study has hitherto reported effective treatment approaches for AE or CE with concurrent hepatorenal involvement.

AIM

To investigate the feasibility and efficacy of simultaneous combined surgery (SCS) as a comprehensive treatment approach for patients with hepatorenal echinococcosis.

METHODS

Clinical datasets of hepatorenal AE (n = 10) and CE (n = 11) patients were retrospectively collected and systematically analyzed. The SCS approach was introduced, and surgical outcomes, complications, and prognoses were documented in detail.

RESULTS

The SCS approach incorporated hybridized techniques, including partial hepatectomy, partial or total nephrectomy, ex vivo liver resection and autotransplantation, and total or subtotal cystectomy with endocystectomy. Radical SCS was achieved in 100% of AE patients and 63.6% of CE patients. All surgeries were completed without intraoperative complications. The short-term complication rate was 28.6% (Clavien-Dindo classification: AE-1 IIIb, 3 IIIa; CE-2 II), while the long-term complication rate was 4.8% (Clavien-Dindo classification: AE-1 IIIb). Patients were followed up for a median of 37 months (AE: 6-81 months; CE: 34-123 months), with no reported deaths or disease relapses.

CONCLUSION

CS appears to be a feasible and effective treatment method for patients with hepatorenal involvement of AE or CE. It fulfills the management criteria for advanced AE or CE cases, aiming to maximize patient benefits.

Key Words: Simultaneous combined surgery; Liver; Kidney; Alveolar echinococcosis; Cystic echinococcosis

Core Tip: This study introduces simultaneous combined surgery (SCS) as a novel and effective approach for treating hepatorenal involvement in alveolar echinococcosis (AE) and cystic echinococcosis (CE). SCS integrates advanced surgical techniques, including ex vivo liver resection and autotransplantation, partial or total nephrectomy, and cystectomy, to achieve radical resection in complex cases. Our study demonstrates that SCS is feasible, safe, and cost-effective, providing a comprehensive solution for advanced AE and CE patients. By addressing extensive lesion invasion and minimizing the risk of disease relapse, this approach maximizes patient outcomes and fulfills the management criteria for these challenging conditions.



INTRODUCTION

Echinococcosis is a chronic infectious disease caused by tapeworms of the genus Echinococcus. The two main types are alveolar echinococcosis (AE) and cystic echinococcosis (CE), caused by Echinococcus multilocularis and Echinococcus granulosus infections, respectively[1,2]. AE exhibits an infiltrative, malignant growth pattern and is predominantly distributed in the northern hemisphere, whereas CE develops through an expansive growth pattern and is endemic worldwide[1,3]. According to reports, over 90% of the global disease burden of AE occurs in China, with the majority of cases concentrated in Western China[1-6].

The liver is the predominant target organ for AE, accounting for over 95% of cases, while CE primarily localizes in the liver (70%) and lungs (20%). Both AE and CE induce severe pathological damage and organ dysfunction[1,7]. Concurrent involvement of multiple organs with AE or CE is clinically rare, and evidence-based treatment modalities for such cases are lacking. Surgical resection of AE lesions and CE cysts remains the definitive curative procedure. Renal CE exhibits a low incidence, reported to be only 2%-4% in the literature[1,2,8-10]. For patients with AE, only 20%-40% are indicated for surgical resection at initial diagnosis, with curative resection rates being even lower in cases of multi-organ involvement. The management of CE is notably heterogeneous, particularly in cases involving multiple organs or anatomically complex regions, where complete cyst removal presents a significant challenge. Staged surgical interventions not only elevate the risk of implantation spread but also prolong the treatment duration. Minimally invasive techniques, such as Percutaneous Puncture-Aspiration-Injection-Reaspiration (PAIR), serve as adjunctive therapies but do not achieve radical cure. These treatment limitations highlight the urgent need for comprehensive and individualized surgical treatment strategies[8,9,11-27]. In complex cases, an individualized approach is essential for optimal management. This research aims to develop a novel therapeutic approach for complex multi-organ echinococcosis, with the potential to improve patient cure rates and quality of life.

MATERIALS AND METHODS
Patients

Over the past decade, 865 patients with AE and 2456 patients with CE were admitted to our hospital, a national and provincial referral center for human echinococcosis, according to hospital database records. Among these patients, 10 AE cases and 11 CE cases (incidence rates of 1.2% and 0.4%, respectively) were diagnosed with concurrent hepatic and renal involvement. Most of these patients had a prior history of surgical or medical intervention (Figure 1). All procedures were performed in accordance with the latest version of the Declaration of Helsinki for Medical Research involving human subjects. Written informed consent for the anonymous collection and analysis of clinical data was obtained from all patients prior to surgery in this retrospective cohort. This study was approved by the Medical Ethics Committee of the First Affiliated Hospital of Xinjiang Medical University (No. K202202-04).

Figure 1
Figure 1 Treatment timelines. The majority of patients with alveolar echinococcosis (AE) underwent multiple palliative interventions prior to presentation. All AE patients were deemed suitable for radical simultaneous combined surgery (SCS). Postoperatively, all AE cases adhered to expert consensus guidelines and achieved cure. Conversely, two patients with cystic echinococcosis (CE) received repetitive palliative surgeries, and five others experienced recurrence following a single surgical procedure. Radical SCS was feasible in only seven CE patients. Nonetheless, all CE patients achieved clinical cure. AE: Alveolar echinococcosis; CE: Cystic echinococcosis; SCS: Simultaneous combined surgery.
Clinical features

The median age of the patient cohort was 47 years (range 22-60 years). The male-to-female gender ratio was 16:5. Clinical manifestations exhibited heterogeneity within the cohort. Abdominal and/or flank-back pain was the most frequently observed symptom, followed by nausea, vomiting, gastrointestinal bleeding, melena, fever, and hydatiduria. Five patients (P4, P5, P10, P19, and P20) were asymptomatic; however, surgical intervention was indicated for all based on lesion/cyst features. Most of the lesions/cysts were localized primarily in the right hepatic lobe and the right kidney. All AE lesions were classified as P4N1M1 (stage IV). CE cysts were classified according to the CE1 to CE4 criteria, with each patient presenting at least one CE2 or CE3 cyst (Supplementary Tables 1 and 2).

In the AE cohort, 12 hepatorenal lesions were identified, with an average volume of 623.2 cm3, a median volume of 448.9 cm3, and a range of 51.0 to 1998.0 cm3. In the CE cohort, 27 cases presented with concurrent hepatorenal cysts, with an average volume of 561.9 cm³, a median volume of 91.9 cm³, and a range of 7.2 to 4508.6 cm3. Besides, 7 extra-hepatorenal CE cysts were identified, exhibiting an average volume of 241.5 cm3, a median volume of 113.0 cm3, and a range of 22.4 to 791.2 cm3. The average total lesion/cyst load per patient (sum of all lesions/cysts in each respective patient) was 747.9 cm3 for AE patients and 1532.8 cm3 for CE patients. The predominant AE morphology was central liquefied lesions, followed by polycystic and diffuse calcified lesions. The most frequent CE cyst type was CE2, followed by CE1, CE3, and CE4 (Supplementary Tables 1 and 2).

Pre-operative assessment

Patients were diagnosed and assessed primarily based on prior medical history, clinical manifestations, ultrasonography, computed tomography (CT), magnetic resonance imaging, and serological testing. In advanced cases, further diagnostic analyses were conducted: (1) 18F-fluorodeoxyglucose positron emission tomography/CT was utilized to evaluate lesion viability in patients P1, P6, and P9[28,29]; (2) Digital subtraction angiography was used to evaluate hepatic veins and the inferior vena cava (IVC) in patients P3 and P4; (3) Three-dimensional reconstruction was used to evaluate vascular features in patients P1, P9, and P13[30]; (4) Indocyanine green clearance testing was performed to evaluate future remnant liver function in patients P1 and P9[31]; (5) Head-to-pelvis CT and chest radiography were performed to identify extrahepatic lesions/cysts in patients P1 through P10; and (6) Emission CT was performed for renal evaluation in patients P14 and P21 (Figure 2).

Figure 2
Figure 2 Radiological findings. A-C: Right-sided hepatorenal alveolar echinococcosis (AE) lesion involvement was prevalent in AE cases; D and E: Isolated single lesions were observed in the left kidney (D) and the left lateral lobe of the liver (E); F-H: AE comorbidities included portal vein cavernous transformation (F), bilateral collateral circulation (G) secondary to severe inferior vena cava (IVC) involvement, and abdominal wall invasion (H); I-M: In contrast, cystic echinococcosis (CE) presented with solitary and multiple large cysts bilaterally; N-P: CE comorbidities included psoas muscle invasion (N), renal function impairment (O), and IVC involvement (P). AE: Alveolar echinococcosis; CE: Cystic echinococcosis.
Simultaneous combined surgery

All surgical procedures were performed under general anesthesia, with patients positioned supine. Hemodynamic stability was continuously monitored throughout the duration of each procedure.

Hepatectomy: Following surgical exploration, the liver was mobilized through the dissection of its ligaments, exposing the perihepatic structures. Hepatic parenchyma resection was performed utilizing vascular occlusion or an interrupted Pringle maneuver[32,33].

Ex vivo liver resection and autotransplantation: Ex vivo liver resection and autotransplantation (ELRA) was performed using previously described methods[17-20]. The procedure encompassed the following steps: (1) En bloc resection of the entire liver, including the retrohepatic IVC, achieved through temporary clamping of the portal vein (PV), IVC, and hepatic artery; (2) Ex vivo liver resection on a back-table ice bath to prepare the corresponding autograft, coupled with in situ placement of a temporary portocaval shunt using an artificial vascular prosthesis to maintain patient hemodynamic stability; and (3) Autotransplantation of the autograft via revascularization.

Nephrectomy: Partial nephrectomy (PN) was performed utilizing temporary renal vascular clamping with cryogenic renal protection. After resection, the renal parenchymal defect was closed with a 3-0 proline with running sutures to ensure hemostasis and urinary tract integrity. Total nephrectomy (TN) was performed by ligation of the renal vessels and ureter[34].

Cystectomy: Total cystectomy, subtotal cystectomy combined with endocystectomy, and partial cystectomy combined with endocystectomy were performed according to established surgical techniques[1,3,8]. Total cystectomy constituted a complete non-opened cyst (NOC) resection, representing a radical surgical approach. Conversely, subtotal and partial cystectomy combined with endocystectomy involved an incomplete opened lateral cystectomy coupled with complete endocystectomy [opened cyst (OC)], representing palliative surgical approaches. After careful examination of the cystic inner surface, the cyst border was sutured with 4-0 proline using a continuous suture technique[1,7,30,35].

Other procedures: The diaphragm, PV, and IVC were repaired or reconstructed with artificial mesh or vascular prosthesis, as clinically indicated. Adrenalectomy, pulmonary wedge resection, and cholecystectomy were performed utilizing standard surgical techniques[11,18,19].

Surgical procedures were classified as radical simultaneous combined surgery (SCS) if all lesions/cysts were radically excised and as non-radical SCS if any lesion/cyst underwent a non-radical procedure.

Postoperative management and follow-up

Patients underwent routine observation with a minimum of two daily visits. Postoperative complications were systematically graded and classified according to the internationally recognized Clavien-Dindo Classification system, which provides a standardized framework for assessing surgical complications. Two senior physicians independently reviewed and cross-validated the complication grades, adhering to the detailed criteria outlined in Supplementary Table 3, thereby ensuring diagnostic accuracy and inter-rater reliability[36,37].

For patients undergoing radical surgery for SCS, the evaluation of surgical outcomes primarily includes the resolution of clinical indicators, restoration of organ function, and radiological examinations. Ultrasonography (B-mode ultrasound) was the primary imaging modality, with CT or recommended when clinically indicated, to assess the extent of lesion removal and identify any residual lesions. Patients who underwent radical SCS resection were prescribed albendazole (ABZ) at a dosage of 15 mg/kg/day for the first two years and three to six months, respectively, with close monitoring. Patients who underwent non-radical SCS resection were enrolled in ABZ treatment at a dosage of 15-20 mg/kg/day and underwent long-term follow-up by local professional Designated Hospitals for Echinococcosis. The follow-up period primarily focused on imaging examinations.

RESULTS

The overall study design employed in this work is summarized in Figure 3.

Figure 3
Figure 3 Study summary. The upper and lower panels depict the pathogenesis, clinical manifestations, lesion/cyst involvement, and corresponding surgical techniques for alveolar echinococcosis and cystic echinococcosis patients, respectively.
Surgery for AE patients (P1-P10)

Detailed surgical procedures are presented in Table 1 and illustrated in Figure 4. The primary procedures for hepatic and renal lesions included lobectomy, partial hepatectomy, major or extended hepatectomy, and ELRA. ELRA was employed for lesions invading the hepatocaval confluence, encompassing all three hepatic veins with or without IVC and/or PV infiltration -PN and TN. In one case (P2), surgery was planned in two stages with a three-month interval. The stage II operation consisted of SCS, while the stage I procedure involved PN for a small lesion in the left kidney. Additional procedures, necessary to achieve complete resection of extra-parasitic lesions, included right adrenalectomy, diaphragmatic repair or reconstruction, IVC repair or prosthetic replacement, pulmonary wedge resection, PV repair, duodenal repair, abdominal lesion resection and repair, choledochal drainage, and cholecystectomy. Besides, among patients undergoing IVC replacement, two (P3, P4) required infrarenal IVC replacement, as opposed to retrohepatic IVC replacement, due to extensive lesion involvement. Intraoperative thoracic drainage was implemented in four patients who underwent diaphragmatic repair with an artificial patch or pulmonary wedge resection.

Figure 4
Figure 4 Surgical observations. A-E: En bloc resection of the right hemiliver and right kidney (arrow) (A and B), extended prosthetic replacement of the diseased inferior vena cava, sutured and repaired blood vessels (arrow) and artificial blood vessels (triangle) (C) or repair via sutures (D), and (E) near-complete occupation of renal tissue were observed in alveolar echinococcosis cases; F and G: Total cystectomy (F) and open cystectomy (G) were predominantly employed in cystic echinococcosis (CE) subjects; H and I: Additionally, procedures such as inferior vena cava (arrow) repair with sutures (H) and partial nephrectomy (I) were required in select CE cases.
Table 1 Simultaneous combined surgery for hepatorenal involvement of alveolar echinococcosis and patient outcomes.
Patient
Surgery
Blood loss (mL)Blood transfusion (U/mL)2LOS (day)ComplicationMedication (month)Follow-up (month)Prognosis
Hepatic
Renal
Other1
Duration (hour)
Summary
P1ELRA, choledocal drainageRight PNRight ADX, diaphragm and IVC repair; PV repair; pulmonary wedge rection, thorax drainage; cholecystectomy20.0Radical35008/52621No2481Cured
P2Right hemihepatectomy (stage II)Right TN (stage II), left PN (stage I)Right ADX, diaphragm and IVC repair; duodenum and abdominal wall repair4.0Radical6803/68019Hydrothorax (IIIa)2442Cured
P3Right trisectionectomyRight TNRight ADX, diaphragm repair with artificial patch, IVC replacement with vascular prosthesis, PV repair; pulmonary wedge resection, thorax drainage8.5Radical12005/91013No2323Cured
P4Right trisectionectomy, caudate lobectomyRight TNRight ADX, diaphragm repair with artificial patch, IVC replacement with vascular prosthesis; PV repair; thorax drainage; cholecystectomy7.5Radical12003/61023No2222Cured
P5Right hemihepatectomyRight PNRight ADX, diaphragm repair with artificial patch, thorax drainage, abdominal lesion resection and repair, cholecystectomy5.5Radical3000/012Incisional hernia (IIIb)2222Cured
P6Right hemihepatectomy, partial hepatectomyRight TNRight ADX, IVC repair, cholecystectomy5.0Radical4002/6008No2020Cured
P7Right hemihepatectomyRight TNDiaphragm repair, thorax drainage, cholecystectomy5.3Radical8002/4705No1818Cured
P8Right hemihepatectomyRight TNRight ADX, diaphragm repair; IVC replacement with vascular prosthesis; cholecystectomy7.0Radical10003/80013Hydrothorax (IIIa)1414Cured
P9ELRARight TNPV repair; cholecystectomy17.0Radical300014/74023Hydrothorax (IIIa)66Cured
P10Right hemihepatectomy, caudate lobectomyRight PNNo4.5Radical2500/013Urinary leakage (IIIb)66Cured

The median operation time was 6.3 hours (range: 4.0-20.0 hours), and the median estimated blood loss was 900 mL (range: 250-3500 mL).

Surgery for CE patients (P11-P21)

Detailed surgical procedures are presented in Table 2 and illustrated in Figure 4. The primary surgical interventions for hepatic and renal cysts were NOC and OC surgeries[38], hemihepatectomy (performed in cases of hepatic atrophy), TN and PN. Furthermore, NOC and OC procedures were also employed for abdominal and retroperitoneal cysts. In addition, right adrenalectomy, diaphragmatic repair, IVC repair, choledochal drainage and cholecystectomy were performed as clinically indicated for cyst involvement or for biliary management. For (1) Multiple surgeries, large lesions with limited operative space; (2) Lesions that are tightly adhered to surrounding tissues, making dissection difficult; and (3) Single CE with thin cyst walls that are prone to rupture, especially when the cysts are closely associated with major blood vessels at the hepatic hilum, making separation challenging. Based on the characteristics of CE lesions, in addition to radical resection, there are also effective non-radical surgical options available for treatment.

Table 2 Simultaneous combined surgery for hepatorenal involvement of cystic echinococcosis and patient outcomes.
PatientSurgery
Blood loss (mL)LOS (day)ComplicationMedication (month)Follow-up (month)Prognosis
Hepatic
Renal
Other1
Duration (hour)
Summary
P11Subtotal cystectomy plus endocystectomy (OC)Partial cystectomy plus endocystectomy (OC)No2.3Non-radical1009No12123Cured
P12Total cystectomy (NOC)Total cystectomy (NOC)Total cystectomy (NOC)2.5Radical508No6106Cured
P13Total cystectomy (NOC)Right PN (NOC)Total cystectomy (NOC); IVC repair2.7Radical1008No655Cured
P14Right hemihepatectomy (NOC)Left TN (NOC)Total cystectomy (NOC); IVC repair, cholecystectomy3.3Radical2007Pneumonia (II)651Cured
P15Subtotal cystectomy plus endocystectomy (OC)Partial cystectomy plus endocystectomy (OC)No3.0Non-radical1007No1249Cured
P16Total cystectomy (NOC)Total cystectomy (NOC)Right ADX, diaphragm repair, cholecystectomy1.8Radical506Pneumonia (II)642Cured
P17Total cystectomy (NOC)Left TN (NOC)No1.6Radical2005No640Cured
P18RL: Total cystectomy (NOC); LLL: Total cystectomy (NOC)Total cystectomy (NOC)Total cystectomy (NOC)2.2Radical1006No337Cured
P19Partial cystectomy plus endocystectomy (OC)Partial cystectomy plus endocystectomy (OC)No3.0Non-radical10010No637Cured
P20Total cystectomy (NOC)Total cystectomy (NOC)No1.4Radical1006No635Cured
P21RL: Subtotal cystectomy plus endocystectomy (OC); LLL: Subtotal cystectomy plus endocystectomy (OC); choledocal drainageRight TN (NOC)Subtotal cystectomy (OC); cholecystectomy4.5Non-radical2009No2434Cured

The median operative time was 2.5 hours (range: 1.4-4.5 hours), and the median estimated blood loss was 100 mL (range: 50-200 mL).

Surgical outcome

Radical SCS was achieved in all AE patients and seven CE patients. Non-radical SCS was performed in the remaining four CE cases. All surgical procedures were completed without significant complications, facilitated by the collaborative efforts of hepatobiliary surgeons, transplant specialists, urologists, and anesthesiologists. Postoperatively, six patients (two undergoing ELRA, two requiring extensive IVC replacement, and patients P2 and P21) were transferred to the intensive care unit for 1-2 days of early postoperative management before returning to the general ward. The median hospital stay was nine days. During the recovery period, patient P10 experienced urinary leakage (Clavien-Dindo classification IIIb), which was successfully managed with 5F ureteral stenting and supportive treatment. Patients P2, P8, and P9 developed hydrothorax (Clavien-Dindo classification IIIa), effectively treated by percutaneous thoracic drainage. Patients P14 and P16 experienced pneumonia (Clavien-Dindo classification II), managed with antibiotics and supportive therapies. No organ failure was observed in any patient. Postoperative pathological diagnoses confirmed the preoperative assessments (Table 3).

Table 3 A comparison of surgical approach and outcomes between the alveolar echinococcosis and cystic echinococcosis cohorts.
Items
AE cohort
CE cohort
Hepatic surgery (n)
    Hemihepatectomy6 (right)1 (right)
    Trisectionectomy2 (right)0
    ELRA20
    Lobectomy10
    Partial hepatectomy10
    NOC surgery08
    OC surgery05
Renal surgery (n)
    PN4 (3 right, 1 left)1 (right)
    TN7 (right)3 (1 right, 2 left)
    NOC surgery08
    OC surgery03
Surgery for extra lesions/cysts (n)
    NOC surgery06 (2 abdominal, 1 pelvic, 3 retroperitoneal)
    OC surgery01 (retroperitoneal)
    Adrenalectomy7 (right)1 (right)
    Diaphragmatic repair4 (right)1 (right)
    Diaphragmatic reconstruction3 (right)0
    IVC repair32
    IVC reconstruction3 (1 retrohepatic IVC, 2 retrohepatic plus below-renal-venous level IVC)0
    PV repair40
    Pulmonary wedge resection2 (right)0
    Thorax drainage4 (right)0
    Choledocal drainage11
    Cholecystectomy73
Surgical summary
    Radicality (%)100 (10/10)63.6 (7/11)
    Median duration (hour)6.32.5
    Estimated blood loss (mL)900100
    Post-OP hospital stay (day)137
Prognosis (%)
    Complication rate50 (5/10: 3 IIIa, 2 IIIb)18.2 (2/11: 2 II)
    Disease-free survival rate 100 (10/10)100 (11/11)

Following discharge, patients were followed for a median of 37 months (AE: 6-81 months; CE: 34-123 months), with ongoing follow-up. At seven months postoperatively, patient P5 was readmitted due to an incisional hernia (Clavien-Dindo classification IIIb), which was managed via laparoscopic repair using an artificial mesh. Postoperative medication was continued for a median of 12 months (AE: 6-24 months; CE: 3-24 months). Two AE patients completed the recommended two-year course of ABZ postoperatively. However, patient P19 discontinued ABZ due to elevated blood aminotransferase levels. Ultimately, all patients achieved clinical cure with disease-free survival (DFS), and patients who underwent unilateral nephrectomy are maintaining a good quality of life (Figure 1).

Comparison of surgical approaches and outcomes between AE and CE cohorts

A comprehensive comparison of surgical characteristics between the AE and CE cohorts was conducted based on the data presented in Table 3. In hepatic surgery, the AE cohort exhibited significantly more complex procedures, comprising right hemihepatectomies (n = 6), right trisectionectomies (n = 2), ELRA (n = 2), lobectomy (n = 1), and partial hepatectomy (n = 1). Conversely, the CE cohort underwent one hemihepatectomy (n = 1) and cyst surgeries [NOC (n = 8) and OC (n = 5)]. In renal surgery, the AE cohort underwent PN [right-sided (n = 3), left-sided (n = 1)] and TN [right-sided (n = 7)], whereas the CE cohort underwent fewer procedures, including PN [right-sided (n = 1)] and TN [right-sided (n = 1), left-sided (n = 2)].

Analysis of overall surgical outcomes demonstrated a 100% radical resection rate in the AE cohort; however, this was associated with a significantly prolonged median operative time of 6.3 hours, a higher median estimated blood loss of 900 mL, and a longer median postoperative hospital stay of 13 days. The complication rate in the AE cohort was 50% [Clavien-Dindo grade IIIa (n = 3) and IIIb (n = 2)], compared to 18.2% in the CE cohort [Clavien-Dindo grade II (n = 2)]. Both cohorts exhibited a 100% DFS rate. Furthermore, the AE cohort required a greater number of reconstruction and repair procedures (Table 3).

DISCUSSION

Surgery constitutes the primary and fundamental treatment modality for echinococcosis, with radical resection remaining the optimal curative option[1-3,8,39]. Treatment strategies encompass a spectrum of approaches, including minimally invasive therapies, advanced hepatectomies or nephrectomies, and even liver transplantation and ELRA in end-stage cases[13,15-20,24,40]. Reports indicate that curative resection is not feasible in approximately 70% of patients at the time of AE diagnosis, resulting in a resection rate of only 20%-40%[9]. In CE, curative treatment is achieved through the complete removal of the cyst, irrespective of its location. If complete removal of the cyst with all its layers, including the adventitia, is not achievable, as in subtotal cystectomy, all types of partial cystectomy, and the PAIR technique, the therapeutic procedure should be supplemented with protoscolecidal agents[1].

Multi-organ AE and CE presented both similarities and distinct differences in their clinical manifestations. Prior to admission to our center, 70.0% of AE cases and 63.6% of CE cases had received palliative treatment for hepatic involvement, with no patients diagnosed with renal AE or CE prior to referral. A consistent finding in the AE cohort was direct invasion from the right liver to the right kidney in all cases (100%, n = 10/10), with infiltration being more severe than in the CE cohort (81.8%, n = 9/11). This observation was further supported by the higher frequency of TNs in AE compared to CE (70% vs 27.3%). Bilateral renal involvement occurred in one AE patient (P2), necessitating a two-stage surgical approach. The prevalence of hepatorenal involvement appeared to be higher in AE than CE (1.2% vs 0.4%). AE cases exhibited more severe disease involvement, characterized by various surrounding structural invasions. The IVC, right adrenal gland, hepatic or renal hilum structures, right diaphragm, psoas muscle, biliary system, abdominal wall, and retroperitoneal cavity were additional lesion sites in AE. However, CE cysts were more frequently located within the abdominal, retroperitoneal, or pelvic cavities. Two cases (P14 and P17) presented with right liver and left kidney cysts. Cyst involvement in other structures primarily involved the renal hilum, proximal ureter, psoas muscle, right adrenal gland, IVC, and the abdominal/pelvic or retroperitoneal cavity.

From a surgical standpoint, multi-organ AE and CE exhibited certain similarities. In the AE cohort, surgical techniques were tailored to address the specific challenges presented. Hemihepatectomy or trisectionectomy, with or without partial hepatectomy for caudate or left lobe of liver lesions, were performed in 80% of AE cases. Adequate surgical exposure for en bloc resection of the entire lesion and involved organ tissues was achievable when the lesion was situated between the right liver and the right kidney. Due to extensive lesion invasion, vascular surgical procedures, facilitated by vascular occlusion of the portal vein and IVC, were crucial for achieving radical resection. IVC reconstruction was determined by the extent of IVC infiltration, including location, severity, and range, as well as the resection characteristics. In two cases (P3 and P4), the IVC was replaced with a vascular prosthesis from the sub-confluence (hepatocaval confluence) level to the infrarenal IVC, a procedure less common in AE cases. In situations where en bloc resection proved challenging, reduced-size lesion eradication or a two-stage procedure (major hepatectomy followed by nephrectomy) offered a safer alternative. Furthermore, research suggests that classic liver transplantation may not be optimal for severely damaged end-stage cases and presents several limitations compared to ELRA. Indeed, ELRA represents an innovative autologous liver transplantation technique, mitigating donor shortages and immune rejection. By utilizing the patient's own liver tissue, ELRA reduces waiting times and eliminates the need for long-term immunosuppressive therapy. This approach enhances postoperative safety and provides a personalized solution in transplantation medicine[13,15,16,40-42]. Consequently, for lesions infiltrating the hepatocaval confluence, conventional hepatectomy posed significant risks, and ELRA facilitated complete resection (patients P1 and P9).

In the CE cohort, however, NOC and OC were the primary surgical procedures employed. A fundamental principle was the protection of surrounding tissues from parasitic content contamination. Based on our experience, we advocate that surgeons should not strive to perform NOC in all multi-organ CE patients, as patient safety remains paramount. With proficient surgical expertise, OC can also provide long-term benefits to patients. For instance, in patients P14 and P15, psoas muscle involvement was observed. In patient P14, the corresponding kidney was indicated for TN, allowing for radical management of the involved psoas muscle. However, in patient P15, sufficient evidence for TN was lacking, and a portion of the lateral cyst was intentionally left within the psoas muscle following risk stratification. In addition, a hepatectomy was performed in patient P14 due to right lobe liver cyst involvement coupled with RLU hepatic atrophy.

In addition to SCS of the liver and kidney, IVC and diaphragmatic repair/replacement, as well as adrenalectomy, were required for patients with right adrenal lesion/cyst invasion. Furthermore, pulmonary wedge resection, thoracic drainage, portal vein repair, cholecystectomy, choledochal drainage, the White test, and additional resections for abdominal or psoas invasions were necessary adjuncts to the aforementioned surgeries[35,43]. While these procedures represent standard surgical techniques for hepatic or renal echinococcosis, the application of these techniques in the context of multi-organ involvement, guided by lesion/cyst characteristics and technical considerations, represents a novel therapeutic concept.

Several studies have reported the application of SCS procedures for non-echinococcal diseases[44-46]. However, in contrast to those scenarios, our data indicated more severe lesion invasions in echinococcosis. Hybridized surgical techniques contributed to improved surgical outcomes in our cohort than malignant conditions. The surgical approach varies among different space-occupying diseases, contingent upon their location, size, and number. However, due to the pathological characteristics of AE occurrence and progression, a greater proportion of resection surgeries is performed. In contrast, CE is more frequently managed using NOC or OC techniques[44].

The SCS approach offered several advantages. Due to the infiltrative growth pattern of AE, all hepatorenal multi-organ AE patients presented with contiguous lesions extending from the right liver to the right kidney. En bloc eradication of the entire lesion was demonstrably superior to staged organ-specific surgery in minimizing the risk of disease dissemination. In the CE cohort, the disease burden was less severe, obviating the need for staged interventions. Besides, SCS represented an efficient and cost-effective approach. In our study, we adopted a ‘single surgical intervention’ strategy by implementing SCS, which allowed us to address multiple organ lesions in a single procedure. This approach significantly reduced the need for multiple surgeries, thereby lowering the direct costs associated with surgical interventions. Additionally, the single surgical procedure minimized the indirect costs related to patient recovery and rehabilitation, further enhancing the overall cost-effectiveness of the treatment. Consequently, SCS not only achieved favorable clinical outcomes but also provided a more economically viable solution for patients.

However, when lesions or cysts were concurrently located in both kidneys, staged surgery could be considered following thorough risk stratification. Based on our experience, SCS procedures should be individualized, and surgeons should prioritize patient safety over achieving theoretically radical resection. Notably, TN and NOC in complex cases should be discussed by a multidisciplinary team prior to surgery to optimize patient outcomes. For example, in two cases (P14 and P15), psoas muscle involvement was observed. In patient P14, the corresponding kidney was indicated for TN, enabling radical management of the involved psoas muscle. Conversely, in patient P15, sufficient evidence for TN was lacking, and a portion of the lateral cyst was intentionally left within the psoas muscle following risk stratification and adherence to rigorous surgical protocols.

This study represents a preliminary investigation into the feasibility and efficacy of SCS for patients with hepatorenal echinococcosis, encompassing both AE and CE. However, as this is a retrospective study involving a limited sample size (10 cases in the AE group and 11 cases in the CE group), the findings should be considered exploratory and preliminary. The restricted sample size inherently carries the potential for bias. Therefore, future research necessitates larger-scale studies for validation.

Future research should prioritize the following key areas: (1) Conducting prospective randomized controlled trials is imperative to establish the efficacy and safety of SCS, thereby generating more compelling evidence; (2) Enhancing multicenter collaborative research to integrate data from diverse institutions will improve the generalizability of findings and mitigate bias; and (3) Extending the follow-up period to 5-10 years, particularly for the AE group, is crucial. Although the benign nature of this disease suggests a lower incidence of long-term adverse events, we intend to prolong follow-up to comprehensively assess long-term prognosis and patient quality of life. This will further validate our findings and provide a robust foundation for optimizing surgical strategies.

CONCLUSION

This study presents the initial case series detailing the clinical manifestations, diagnostic evaluation, novel treatment approach-SCS, surgical indications, and prognosis for patients with hepatic-renal multi-organ AE/CE. Furthermore, the application of SCS for multi-organ echinococcosis satisfies the management criteria for patients with advanced AE and CE.

ACKNOWLEDGEMENTS

The authors thank Abudusalamu Aini, Kasimu Aihaiti, Aisika Ainiwa for query and input clinical information.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country of origin: China

Peer-review report’s classification

Scientific Quality: Grade A, Grade B, Grade B

Novelty: Grade A, Grade B, Grade B

Creativity or Innovation: Grade A, Grade A, Grade A

Scientific Significance: Grade B, Grade B, Grade B

P-Reviewer: Sun PT; Wang XR S-Editor: Li L L-Editor: A P-Editor: Zhang L

References
1.  Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP. Echinococcosis: Advances in the 21st Century. Clin Microbiol Rev. 2019;32:e00075-18.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 421]  [Cited by in RCA: 618]  [Article Influence: 103.0]  [Reference Citation Analysis (0)]
2.  Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RC, Jenkins EJ. Global Distribution of Alveolar and Cystic Echinococcosis. Adv Parasitol. 2017;95:315-493.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 432]  [Cited by in RCA: 626]  [Article Influence: 78.3]  [Reference Citation Analysis (0)]
3.  McManus DP, Gray DJ, Zhang W, Yang Y. Diagnosis, treatment, and management of echinococcosis. BMJ. 2012;344:e3866.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 195]  [Cited by in RCA: 247]  [Article Influence: 19.0]  [Reference Citation Analysis (0)]
4.  Wang Q, Yang L, Wang Y, Zhang GJ, Zhong B, Wu WP, Zheng CJ, Liao S, Yu WJ, He W, Wang Q, Chen F, Li RR, Huang Y, Yao R, Zhou XN. Disease burden of echinococcosis in Tibetan communities-A significant public health issue in an underdeveloped region of western China. Acta Trop. 2020;203:105283.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 11]  [Cited by in RCA: 18]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
5.  Qian MB, Chen J, Bergquist R, Li ZJ, Li SZ, Xiao N, Utzinger J, Zhou XN. Neglected tropical diseases in the People's Republic of China: progress towards elimination. Infect Dis Poverty. 2019;8:86.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 50]  [Cited by in RCA: 40]  [Article Influence: 6.7]  [Reference Citation Analysis (0)]
6.  Vuitton DA, Zhou H, Bresson-hadni S, Wang Q, Piarroux M, Raoul F, Giraudoux P. Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology. 2003;127:S87-S107.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 161]  [Cited by in RCA: 151]  [Article Influence: 7.2]  [Reference Citation Analysis (0)]
7.  Al-Saeedi M, Khajeh E, Hoffmann K, Ghamarnejad O, Stojkovic M, Weber TF, Golriz M, Strobel O, Junghanss T, Büchler MW, Mehrabi A. Standardized endocystectomy technique for surgical treatment of uncomplicated hepatic cystic echinococcosis. PLoS Negl Trop Dis. 2019;13:e0007516.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 12]  [Cited by in RCA: 12]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
8.  Brunetti E, Kern P, Vuitton DA; Writing Panel for the WHO-IWGE. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114:1-16.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 1108]  [Cited by in RCA: 1313]  [Article Influence: 87.5]  [Reference Citation Analysis (0)]
9.  Kamiyama T. Recent advances in surgical strategies for alveolar echinococcosis of the liver. Surg Today. 2020;50:1360-1367.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 10]  [Cited by in RCA: 21]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
10.  Kern P, Wen H, Sato N, Vuitton DA, Gruener B, Shao Y, Delabrousse E, Kratzer W, Bresson-Hadni S. WHO classification of alveolar echinococcosis: principles and application. Parasitol Int. 2006;55 Suppl:S283-S287.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 188]  [Cited by in RCA: 204]  [Article Influence: 10.2]  [Reference Citation Analysis (1)]
11.  Piarroux M, Piarroux R, Giorgi R, Knapp J, Bardonnet K, Sudre B, Watelet J, Dumortier J, Gérard A, Beytout J, Abergel A, Mantion G, Vuitton DA, Bresson-Hadni S. Clinical features and evolution of alveolar echinococcosis in France from 1982 to 2007: results of a survey in 387 patients. J Hepatol. 2011;55:1025-1033.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 95]  [Cited by in RCA: 99]  [Article Influence: 7.1]  [Reference Citation Analysis (0)]
12.  Bresson-Hadni S, Koch S, Miguet JP, Gillet M, Mantion GA, Heyd B, Vuitton DA; European group of clinicians. Indications and results of liver transplantation for Echinococcus alveolar infection: an overview. Langenbecks Arch Surg. 2003;388:231-238.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 74]  [Cited by in RCA: 75]  [Article Influence: 3.4]  [Reference Citation Analysis (0)]
13.  Koch S, Bresson-Hadni S, Miguet JP, Crumbach JP, Gillet M, Mantion GA, Heyd B, Vuitton DA, Minello A, Kurtz S; European Collaborating Clinicians. Experience of liver transplantation for incurable alveolar echinococcosis: a 45-case European collaborative report. Transplantation. 2003;75:856-863.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 119]  [Cited by in RCA: 100]  [Article Influence: 4.5]  [Reference Citation Analysis (1)]
14.  Sozuer E, Akyuz M, Akbulut S. Open surgery for hepatic hydatid disease. Int Surg. 2014;99:764-769.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 40]  [Cited by in RCA: 25]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
15.  Akbulut S, Yilmaz S. Liver transplantation in Turkey: historical review and future perspectives. Transplant Rev (Orlando). 2015;29:161-167.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 38]  [Cited by in RCA: 34]  [Article Influence: 3.4]  [Reference Citation Analysis (1)]
16.  Aydinli B, Ozturk G, Arslan S, Kantarci M, Tan O, Ahıskalioglu A, Özden K, Colak A. Liver transplantation for alveolar echinococcosis in an endemic region. Liver Transpl. 2015;21:1096-1102.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 35]  [Cited by in RCA: 35]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
17.  Weiner J, Hemming A, Levi D, Beduschi T, Matsumoto R, Mathur A, Liou P, Griesemer A, Samstein B, Cherqui D, Emond J, Kato T. Ex Vivo Liver Resection and Autotransplantation: Should It be Used More Frequently? Ann Surg. 2022;276:854-859.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in RCA: 13]  [Reference Citation Analysis (0)]
18.  Qiu Y, Huang B, Yang X, Wang T, Shen S, Yang Y, Wang W. Evaluating the Benefits and Risks of Ex Vivo Liver Resection and Autotransplantation in Treating Hepatic End-stage Alveolar Echinococcosis. Clin Infect Dis. 2022;75:1289-1296.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 1]  [Cited by in RCA: 10]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
19.  Aji T, Dong JH, Shao YM, Zhao JM, Li T, Tuxun T, Shalayiadang P, Ran B, Jiang TM, Zhang RQ, He YB, Huang JF, Wen H. Ex vivo liver resection and autotransplantation as alternative to allotransplantation for end-stage hepatic alveolar echinococcosis. J Hepatol. 2018;69:1037-1046.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 59]  [Cited by in RCA: 74]  [Article Influence: 10.6]  [Reference Citation Analysis (0)]
20.  Aini A, Shao Y, Shalayiadang P, Ran B, Jiang T, Zhang R, Aji T, Wen H. Auxiliary Partial Autologous Liver Transplantation for High-selective Alveolar Echinococcosis: A Proof of Concept. Transplantation. 2020;104:e138-e139.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 3]  [Cited by in RCA: 3]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
21.  Akbulut S, Ozdemir F. Intraperitoneal rupture of the hydatid cyst: Four case reports and literature review. World J Hepatol. 2019;11:318-329.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 20]  [Cited by in RCA: 21]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
22.  Yang C, He J, Yang X, Wang W. Surgical approaches for definitive treatment of hepatic alveolar echinococcosis: results of a survey in 178 patients. Parasitology. 2019;146:1414-1420.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 22]  [Cited by in RCA: 18]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
23.  Lau WY. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) and its further developments in the last decade. Hepatobiliary Surg Nutr. 2019;8:258-259.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 1]  [Cited by in RCA: 3]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
24.  Aliakbarian M, Tohidinezhad F, Eslami S, Akhavan-Rezayat K. Liver transplantation for hepatic alveolar echinococcosis: literature review and three new cases. Infect Dis (Lond). 2018;50:452-459.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 11]  [Cited by in RCA: 9]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
25.  Magistri P, Pecchi A, Franceschini E, Pesi B, Guadagni S, Catellani B, Assirati G, Guidetti C, Guerrini GP, Tarantino G, Ballarin R, Codeluppi M, Morelli L, Coratti A, Di Benedetto F. Not just minor resections: robotic approach for cystic echinococcosis of the liver. Infection. 2019;47:973-979.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 11]  [Cited by in RCA: 10]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
26.  Vuitton DA, Azizi A, Richou C, Vuitton L, Blagosklonov O, Delabrousse E, Mantion GA, Bresson-Hadni S. Current interventional strategy for the treatment of hepatic alveolar echinococcosis. Expert Rev Anti Infect Ther. 2016;14:1179-1194.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 45]  [Cited by in RCA: 37]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
27.  Gomez I Gavara C, López-Andújar R, Belda Ibáñez T, Ramia Ángel JM, Moya Herraiz Á, Orbis Castellanos F, Pareja Ibars E, San Juan Rodríguez F. Review of the treatment of liver hydatid cysts. World J Gastroenterol. 2015;21:124-131.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in CrossRef: 91]  [Cited by in RCA: 110]  [Article Influence: 11.0]  [Reference Citation Analysis (0)]
28.  Liu W, Delabrousse É, Blagosklonov O, Wang J, Zeng H, Jiang Y, Wang J, Qin Y, Vuitton DA, Wen H. Innovation in hepatic alveolar echinococcosis imaging: best use of old tools, and necessary evaluation of new ones. Parasite. 2014;21:74.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 56]  [Cited by in RCA: 56]  [Article Influence: 5.1]  [Reference Citation Analysis (0)]
29.  Caoduro C, Porot C, Vuitton DA, Bresson-Hadni S, Grenouillet F, Richou C, Boulahdour H, Blagosklonov O. The role of delayed 18F-FDG PET imaging in the follow-up of patients with alveolar echinococcosis. J Nucl Med. 2013;54:358-363.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 62]  [Cited by in RCA: 66]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
30.  He YB, Bai L, Aji T, Jiang Y, Zhao JM, Zhang JH, Shao YM, Liu WY, Wen H. Application of 3D reconstruction for surgical treatment of hepatic alveolar echinococcosis. World J Gastroenterol. 2015;21:10200-10207.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in CrossRef: 26]  [Cited by in RCA: 27]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
31.  Kobayashi Y, Kiya Y, Sugawara T, Nishioka Y, Hashimoto M, Shindoh J. Expanded Makuuchi's criteria using estimated indocyanine green clearance rate of future liver remnant as a safety limit for maximum extent of liver resection. HPB (Oxford). 2019;21:990-997.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 40]  [Cited by in RCA: 28]  [Article Influence: 4.7]  [Reference Citation Analysis (0)]
32.  Hester CA, El Mokdad A, Mansour JC, Porembka MR, Yopp AC, Zeh HJ 3rd, Polanco PM. Current Pattern of Use and Impact of Pringle Maneuver in Liver Resections in the United States. J Surg Res. 2019;239:253-260.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 8]  [Cited by in RCA: 12]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
33.  Wei X, Zheng W, Yang Z, Liu H, Tang T, Li X, Liu X. Effect of the intermittent Pringle maneuver on liver damage after hepatectomy: a retrospective cohort study. World J Surg Oncol. 2019;17:142.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 12]  [Cited by in RCA: 23]  [Article Influence: 3.8]  [Reference Citation Analysis (0)]
34.  Ramteke VV, Deshpande NS, Balwani MR, Bawankule CP. Primary Renal Echinococcosis. Indian J Nephrol. 2017;27:316-318.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 7]  [Cited by in RCA: 8]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
35.  Linke R, Ulrich F, Bechstein WO, Schnitzbauer AA. The White-test helps to reduce biliary leakage in liver resection: a systematic review and meta-analysis. Ann Hepatol. 2015;14:161-167.  [PubMed]  [DOI]  [Full Text]
36.  Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205-213.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 18532]  [Cited by in RCA: 24494]  [Article Influence: 1166.4]  [Reference Citation Analysis (0)]
37.  Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187-196.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 6210]  [Cited by in RCA: 8456]  [Article Influence: 528.5]  [Reference Citation Analysis (0)]
38.  Rexiati M, Mutalifu A, Azhati B, Wang W, Yang H, Sheyhedin I, Wang Y. Diagnosis and surgical treatment of renal hydatid disease: a retrospective analysis of 30 cases. PLoS One. 2014;9:e96602.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 20]  [Cited by in RCA: 28]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
39.  Kern P. Clinical features and treatment of alveolar echinococcosis. Curr Opin Infect Dis. 2010;23:505-512.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 143]  [Cited by in RCA: 145]  [Article Influence: 9.7]  [Reference Citation Analysis (0)]
40.  Bresson-Hadni S, Blagosklonov O, Knapp J, Grenouillet F, Sako Y, Delabrousse E, Brientini MP, Richou C, Minello A, Antonino AT, Gillet M, Ito A, Mantion GA, Vuitton DA. Should possible recurrence of disease contraindicate liver transplantation in patients with end-stage alveolar echinococcosis? A 20-year follow-up study. Liver Transpl. 2011;17:855-865.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 74]  [Cited by in RCA: 74]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
41.  Matsuoka N, Weiner JI, Griesemer AD, Samstein BB, Zhao Y, Emond JC, Kato T. Ex vivo pancreaticoduodenectomy and liver autotransplantation for pancreatic head tumor with extensive involvement of the hepatoduodenal ligament. Liver Transpl. 2015;21:1553-1556.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 6]  [Cited by in RCA: 7]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
42.  Hand J, Huprikar S. Liver transplantation for alveolar echinococcosis: Acceptable when necessary but is it preventable? Liver Transpl. 2015;21:1013-1015.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 5]  [Cited by in RCA: 6]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
43.  Wang HQ, Yang J, Yang JY, Yan LN. Bile leakage test in liver resection: a systematic review and meta-analysis. World J Gastroenterol. 2013;19:8420-8426.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in CrossRef: 32]  [Cited by in RCA: 32]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
44.  Yezhelyev M, Master V, Egnatashvili V, Kooby DA. Combined nephrectomy and major hepatectomy: indications, outcomes, and recommendations. J Am Coll Surg. 2009;208:410-418.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Cited by in Crossref: 8]  [Cited by in RCA: 10]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
45.  Langan RC, Ripley RT, Davis JL, Prieto PA, Datrice N, Steinberg SM, Bratslavsky G, Rudloff U, Kammula US, Stojadinovic A, Avital I. Liver directed therapy for renal cell carcinoma. J Cancer. 2012;3:184-190.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 21]  [Cited by in RCA: 21]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
46.  Yoshimatsu M, Shirabe K, Nagao Y, Harada N, Uchiyama H, Yoshizumi T, Taketomi A, Ikeda T, Tatsugami K, Maehara Y. A safe combined nephrectomy and right lobectomy using the liver hanging maneuver for huge renal cell carcinoma directly invading the right lobe of the liver: report of a case. Surg Today. 2014;44:1778-1782.  [RCA]  [PubMed]  [DOI]  [Full Text]  [Full Text (PDF)]  [Cited by in Crossref: 4]  [Cited by in RCA: 4]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]