Publications by authors named "Henrik Petrowsky"

113 Publications

Neoadjuvant Therapy for Resectable Pancreatic Cancer: A New Standard of Care. Pooled Data from Three Randomized Controlled Trials.

Ann Surg 2021 Jul 29. Epub 2021 Jul 29.

Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland Department of Surgery, University Hospital Erlangen, Erlangen, Germany Division of Pancreatic Surgery, IRCCS, Azienda Ospedaliero Universitaria di Bologna, Bologna, Italy Department of Internal Medicine and Surgery (DIMEC), Alma Mater Studiorum, University of Bologna, S.Orsola-Malpighi Hospital, Bologna, Italy Epidemiology, Biostatistics and Prevention Institute, University of Zurich, Zurich, Switzerland Department of Oncology, University Hospital Zurich, Zurich, Switzerland Department of Radiation Oncology, University Hospital Magdeburg, Magdeburg, Germany Department of Radiation Oncology, University Hospital Erlangen, Erlangen, Germany Department of Surgery, Hospital Ansbach, Ansbach, Germany Department of Experimental, Diagnostic and Specialty Medicine, S. Orsola-Malpighi University Hospital, Bologna, Italy Medical Oncology, IRCCS Azienda Ospedaliero, University of Bologna, Bologna, Italy Department of General, Visceral- and Transplantation Surgery, University Hospital Frankfurt am Main, Frankfurt, Germany Department of General and Transplantation Surgery, University Hospital Cologne, Köln, Germany Department of Digestive Surgery and Liver Transplantation, Croix Rousse University Hospital, University Lyon, Lyon, France Department of General, Visceral and Transplantation Surgery, University Hospital of Mainz, Mainz, Germany.

Objective: The aim of this study was to pool data from randomized controlled trials (RCT) limited to resectable pancreatic ductal adenocarcinoma (PDAC) to determine whether a neoadjuvant therapy impacts on disease-free survival (DFS) and surgical outcome.Summary Background Data: Few underpowered studies have suggested benefits from neoadjuvant chemo (± radiation) for strictly resectable PDAC without offering conclusive recommendations.

Methods: Three RCTs were identified comparing neoadjuvant chemo (± radio) therapy vs. upfront surgery followed by adjuvant therapy in all cases. Data were pooled targeting DFS as primary endpoint, while OS, postoperative morbidity and mortality were investigated as secondary endpoints. Survival endpoints DFS and OS were compared using Cox proportional hazards regression with study-specific baseline hazards.

Results: 130 patients were randomized (56 in the neoadjuvant and 74 in the control groups). DFS was significantly longer in the neoadjuvant treatment group compared to surgery only (hazard ratio (HR 0.6, 95% CI 0.4 to 0.9) (p= 0.01). Furthermore, DFS for the subgroup of R0 resections was similarly longer in the neoadjuvant treated group (HR 0.6, 95% CI 0.35 to 0.9, p = 0.045). While post-operative complications (CCI) occurred less frequently (p =0.008), patients after neoadjuvant therapy experienced a higher toxicity, but without negative impact on oncological or surgical outcome parameters.

Conclusion: Neoadjuvant therapy can be offered as an acceptable standard of care for patients with purely resectable PDAC. Future research with the advances of precision oncology should now focus on the definition of the optimal regimen.
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http://dx.doi.org/10.1097/SLA.0000000000005126DOI Listing
July 2021

Long-Term Normothermic Machine Preservation of Partial Livers: First Experience With 21 Human Hemi-Livers.

Ann Surg 2021 Jul 29. Epub 2021 Jul 29.

Wyss Zurich, ETH Zurich/University of Zurich, Switzerland Department of Surgery and Transplantation, Swiss Hepato-Pancreato-Biliary (HPB) Center, University Hospital Zurich, Switzerland Department of Pathology and Molecular Pathology and Institute of Molecular Cancer Research (IMCR), University Zurich and University Hospital Zurich, Switzerland Macromolecular Engineering Laboratory, Department of Mechanical and Process Engineering, ETH Zurich, Zurich, Switzerland Transport Processes and Reactions Laboratory, Department of Mechanical and Process Engineering, ETH Zurich, Zurich, Switzerland.

Objective: The aim of this study was to maintain long-term full function and viability of partial livers perfused ex situ for sufficient duration to enable ex situ treatment, repair, and regeneration.

Background: Organ shortage remains the single most important factor limiting the success of transplantation. Autotransplantation in patients with nonresectable liver tumors is rarely feasible due to insufficient tumor-free remnant tissue. This limitation could be solved by the availability of long-term preservation of partial livers that enables functional regeneration and subsequent transplantation.

Methods: Partial swine livers were perfused with autologous blood after being procured from healthy pigs following 70% in-vivo resection, leaving only the right lateral lobe. Partial human livers were recovered from patients undergoing anatomic right or left hepatectomies and perfused with a blood based perfusate together with various medical additives. Assessment of physiologic function during perfusion was based on markers of hepatocyte, cholangiocyte, vascular and immune compartments,, as well as histology.

Results: Following the development phase with partial swine livers, 21 partial human livers (14 right and 7 left hemi-livers) were perfused, eventually reaching the targeted perfusion duration of 1 week with the final protocol. These partial livers disclosed a stable perfusion with normal hepatic function including bile production (5-10 mL/h), lactate clearance, and maintenance of energy exhibited by normal of adenosine triphosphate (ATP) and glycogen levels, and preserved liver architecture for up to 1 week.

Conclusion: This pioneering research presents the inaugural evidence for long-term machine perfusion of partial livers and provides a pathway for innovative and relevant clinical applications to increase the availability of organs and provide novel approaches in hepatic oncology.
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http://dx.doi.org/10.1097/SLA.0000000000005102DOI Listing
July 2021

Phase Ib dose-escalation study of the hypoxia-modifier Myo-inositol trispyrophosphate in patients with hepatopancreatobiliary tumors.

Nat Commun 2021 06 21;12(1):3807. Epub 2021 Jun 21.

Swiss Hepato-Pancreato-Biliary (HPB) and Transplantation Center, University Hospital Zurich, Raemistrasse 100, Zurich, Switzerland.

Hypoxia is prominent in solid tumors and a recognized driver of malignancy. Thus far, targeting tumor hypoxia has remained unsuccessful. Myo-inositol trispyrophosphate (ITPP) is a re-oxygenating compound without apparent toxicity. In preclinical models, ITPP potentiates the efficacy of subsequent chemotherapy through vascular normalization. Here, we report the results of an unrandomized, open-labeled, 3 + 3 dose-escalation phase Ib study (NCT02528526) including 28 patients with advanced primary hepatopancreatobiliary malignancies and liver metastases of colorectal cancer receiving nine 8h-infusions of ITPP over three weeks across eight dose levels (1'866-14'500 mg/m/dose), followed by standard chemotherapy. Primary objectives are assessment of the safety and tolerability and establishment of the maximum tolerated dose, while secondary objectives include assessment of pharmacokinetics, antitumor activity via radiological evaluation and assessment of circulatory tumor-specific and angiogenic markers. The maximum tolerated dose is 12,390 mg/m, and ITPP treatment results in 32 treatment-related toxicities (mostly hypercalcemia) that require little or no intervention. 52% of patients have morphological disease stabilization under ITPP monotherapy. Following subsequent chemotherapy, 10% show partial responses while 60% have stable disease. Decreases in angiogenic markers are noted in ∼60% of patients after ITPP and tend to correlate with responses and survival after chemotherapy.
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http://dx.doi.org/10.1038/s41467-021-24069-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8217170PMC
June 2021

Limitations of current liver donor allocation systems and the impact of newer indications for liver transplantation.

J Hepatol 2021 Jul;75 Suppl 1:S178-S190

Liver Failure Group, Institute for Liver and Digestive Health, University College London, London and European Foundation for the Study of Chronic Liver Failure, Barcelona, Spain.

Liver transplantation represents a life-saving treatment for patients with decompensated cirrhosis, a severe condition associated with a high risk of waiting list mortality. When decompensation occurs rapidly in the presence of extrahepatic organ failures, the condition is called acute-on-chronic liver failure, which is associated with an even higher risk of death, though liver transplantation can also markedly improve survival in affected patients. However, there are still gaps in our understanding of how to optimise prioritisation and organ allocation, as well as survival among patients with acute-on-chronic liver failure (both before and after transplant). Moreover, it is urgent to address inequalities in access to liver transplantation in patients with severe alcoholic hepatitis and non-alcoholic steatohepatitis. Several controversies still exist regarding gender and regional disparities, as well as the use of suboptimal donor grafts. In this review, we aim to provide a critical perspective on the role of liver transplantation in patients with decompensated cirrhosis and address areas of ongoing uncertainty.
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http://dx.doi.org/10.1016/j.jhep.2021.01.007DOI Listing
July 2021

Can magnetic resonance imaging radiomics of the pancreas predict postoperative pancreatic fistula?

Eur J Radiol 2021 Jul 24;140:109733. Epub 2021 Apr 24.

Institute of Diagnostic and Interventional Radiology, University Hospital Zurich, Zurich, Switzerland; University of Zurich, Zurich, Switzerland. Electronic address:

Objectives: To evaluate whether a magnetic resonance imaging (MRI) radiomics-based machine learning classifier can predict postoperative pancreatic fistula (POPF) after pancreaticoduodenectomy (PD) and to compare its performance to T1 signal intensity ratio (T1 SIratio).

Methods: Sixty-two patients who underwent 3 T MRI before PD between 2008 and 2018 were retrospectively analyzed. POPF was graded and split into clinically relevant POPF (CR-POPF) vs. biochemical leak or no POPF. On T1- and T2-weighted images, 2 regions of interest were placed in the pancreatic corpus and cauda. 173 radiomics features were extracted using pyRadiomics. Additionally, the pancreas-to-muscle T1 SIratio was measured. The dataset was augmented and split into training (70 %) and test sets (30 %). A Boruta algorithm was used for feature reduction. For prediction of CR-POPF models were built using a gradient-boosted tree (GBT) and logistic regression from the radiomics features, T1 SIratio and a combination of the two. Diagnostic accuracy of the models was compared using areas under the receiver operating characteristics curve (AUCs).

Results: Five most important radiomics features were identified for prediction of CR-POPF. A GBT using these features achieved an AUC of 0.82 (95 % Confidence Interval [CI]: 0.74 - 0.89) when applied on the original (non-augmented) dataset. Using T1 SIratio, a GBT model resulted in an AUC of 0.75 (CI: 0.63 - 0.84) and a logistic regression model delivered an AUC of 0.75 (CI: 0.63 - 0.84). A GBT model combining radiomics features and T1 SIratio resulted in an AUC of 0.90 (CI 0.84 - 0.95).

Conclusion: MRI-radiomics with routine sequences provides promising prediction of CR-POPF.
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http://dx.doi.org/10.1016/j.ejrad.2021.109733DOI Listing
July 2021

Induction of liver hypertrophy for extended liver surgery and partial liver transplantation: State of the art of parenchyma augmentation-assisted liver surgery.

Langenbecks Arch Surg 2021 Mar 19. Epub 2021 Mar 19.

Swiss HPB and Transplantation Center, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland.

Background: Liver surgery and transplantation currently represent the only curative treatment options for primary and secondary hepatic malignancies. Despite the ability of the liver to regenerate after tissue loss, 25-30% future liver remnant is considered the minimum requirement to prevent serious risk for post-hepatectomy liver failure.

Purpose: The aim of this review is to depict the various interventions for liver parenchyma augmentation-assisting surgery enabling extended liver resections. The article summarizes one- and two-stage procedures with a focus on hypertrophy- and corresponding resection rates.

Conclusions: To induce liver parenchymal augmentation prior to hepatectomy, most techniques rely on portal vein occlusion, but more recently inclusion of parenchymal splitting, hepatic vein occlusion, and partial liver transplantation has extended the technical armamentarium. Safely accomplishing major and ultimately total hepatectomy by these techniques requires integration into a meaningful oncological concept. The advent of highly effective chemotherapeutic regimen in the neo-adjuvant, interstage, and adjuvant setting has underlined an aggressive surgical approach in the given setting to convert formerly "palliative" disease into a curative and sometimes in a "chronic" disease.
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http://dx.doi.org/10.1007/s00423-021-02148-2DOI Listing
March 2021

Repeated hepatectomy after ALPPS for recurrence of colorectal liver metastasis: the edge of limits?

HPB (Oxford) 2021 Mar 1. Epub 2021 Mar 1.

Department of Surgery, Division of Hepatobiliary and Pancreatic Surgery, Asklepios Hospital Barmbek, Germany; Semmelweis University of Medicine, Asklepios Campus Hamburg, Hamburg, Germany.

Background: Repeated liver resections for the recurrence of colorectal liver metastasis (CRLM) are described as safe and have similar oncological outcomes compared to first hepatectomy. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) is performed in patients with conventionally non-resectable CRLM. Repeated resections after ALPPS has not yet been described.

Methods: Patients that underwent repeated liver resection in recurrence of CRLM after ALPPS were included in this study. The primary endpoint was morbidity and secondary endpoints were mortality, resection margin and survival.

Results: Thirty patients were included in this study. During ALPPS, most of the patients had classical split (60%, n = 18) and clearance of the FLR (77%, n = 23). Hepatic recurrence was treated with non-anatomical resection (57%, n = 17), resection combined with local ablation (13%, n = 4), open ablation (13%, n = 4), segmentectomy (10%, n = 3) or subtotal segmentectomy (7%, n = 2). Six patients (20%) developed complications (10% minor complications). No post-hepatectomy liver failure or perioperative mortality was observed. One-year patient survival was 87%. Five patients received a third hepatectomy.

Conclusion: Repeated resections after ALPPS for CRLM in selected patients are safe and feasible with low morbidity and no mortality. Survival seems to be comparable with repeated resections after conventional hepatectomy.
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http://dx.doi.org/10.1016/j.hpb.2021.02.008DOI Listing
March 2021

Combination of HAI-FUDR and Systemic Gemcitabine and Cisplatin in Unresectable Cholangiocarcinoma: A Dose Finding Single Center Study.

Oncology 2021 3;99(5):300-309. Epub 2021 Mar 3.

Department of Medical Oncology and Hematology, Division of Medical Oncology, University Hospital Zurich, Zurich, Switzerland,

Background: Unresectable cholangiocarcinoma has a poor prognosis and treatment options are limited. Combined systemic and intrahepatic chemotherapy may improve local control and enable downsizing. The aim of this study was to determine the maximum tolerated dose (MTD) of intravenous gemcitabine combined with intravenous cisplatin and hepatic arterial infusion (HAI) with floxuridine (FUDR) in patients with unresectable intrahepatic or hilar cholangiocarcinoma.

Methods: Twelve patients were treated within a 3 + 3 dose escalation algorithm with 600, 800, or 1,000 mg/m2 gemcitabine and predefined doses of cisplatin 25 mg/m2 on days 1 and 8, q21, for 4 cycles, and FUDR 0.2 mg/kg on days 1-14 as continuous HAI, q28, for 3 cycles. Safety and toxicity as well as resectability rates after 3 months and preliminary survival data are reported.

Results: The determined MTD for gemcitabine was 800 mg/m2. Dose limiting toxicities were neutropenic fever and biliary tract infections. In total, 27% of the patients showed partial remission and 73% stable disease. Although none of the patients achieved resectability after 3 months, the 3-year overall survival rate was 33%, median overall survival 23.9 months (range 1-49), and median progression-free survival 10.1 months (range 2-40).

Conclusions: Intravenous gemcitabine/cisplatin plus HAI-FUDR is feasible and appears effective for disease control. Larger prospective studies evaluating this triplet combination are warranted.
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http://dx.doi.org/10.1159/000512967DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8117395PMC
May 2021

Multimodal treatment strategies for colorectal liver metastases.

Swiss Med Wkly 2021 Feb 15;151:w20390. Epub 2021 Feb 15.

Department of Surgery, Swiss Hepato-pancreato-biliary and Transplantation Centre, University Hospital Zurich, Switzerland.

Colorectal cancer is the third most common cancer worldwide. Half of CRC patients develop liver metastases during the course of the disease, with a 5-year survival rate close to zero in the absence of therapy. Surgical resection remains the only possible curative option, and current guidelines recommend adjuvant chemotherapy, resulting in a 5-year survival rate exceeding 50%. Neoadjuvant systemic therapy is not indicated in cases with simple resection but should be offered to all patients with extensive bilobar disease. Personalised systemic treatment is essential to convert upfront non-resectable lesions to resectable ones. Anatomical resections, non-anatomical resections and two-stage hepatectomies can be performed though open or minimally invasive (laparoscopic or robotic) surgery. The extent of a hepatic resection is limited by the risk of postoperative liver failure due to a too small liver remnant, inflow or outflow obstruction or insufficient biliary drainage. About 75% of patients are diagnosed with non-resectable liver metastases not amenable to a standard upfront resection. In recent years, effective therapeutic approaches have revolutionised liver surgery and new strategies have enabled the conversion of primarily non-resectable metastatic disease for resection. These strategies include oncological and surgical therapies, as well as combinations of the two. From an oncological perspective, colorectal liver metastases  may be treated by systemic chemotherapy or immunotherapy, or selective intra-hepatic arterial infusion chemotherapy, depending on the extent of the disease and the mutational status. In surgery, we often apply two-stage strategies using portal vein occlusion, such as portal vein embolisation or ligation, or complex two-stage hepatectomy such as associating liver partition and portal vein ligation for staged hepatectomy. Other additive tools to reach curative resection are tumour ablations (electroporation, microwave or radiofrequency). The role of stereotactic radiation of liver metastases is not yet well defined. Modern radiation techniques, including image guidance, breath hold and gating, were only introduced for a larger patient population in recent years. Therefore, prospective studies with larger patient cohorts are still pending. Over the last decade, liver transplantation has gained increasing attention in selective cases of non-resectable colorectal liver metastases, with promising cohort studies, but definitive recommendations must await the results of ongoing randomised controlled trials. The optimal treatment of patients with colorectal liver metastases requires the timely association of various strategies, and all cases must be discussed at multidisciplinary team conferences. While colorectal liver metastases was a uniformly lethal condition a few decades ago, it has become amenable to curative therapies, with excellent quality of life in many scenarios. This review reports on up-to-date treatment modalities and their combinations in the treatment algorithm of colorectal liver metastases.    .
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http://dx.doi.org/10.4414/smw.2021.20390DOI Listing
February 2021

When transmigrates from the liver into the pericardium: a case report.

J Surg Case Rep 2021 Feb 9;2021(2):rjaa492. Epub 2021 Feb 9.

Department of Surgery and Transplantation, Swiss HPB and Transplant Center Zurich, University Hospital Zurich, Zurich, Switzerland.

Infection with is a common helminthic disease worldwide with endemic in a region with high endemic areas in Africa, Asia, Middle East, South America and southern Europe. We report a rare case of a young patient with cystic echinococcal disease of the liver invading the pericardium. The patient initially presented with life-threatening cardiac tamponade, which resulted in the discovery of the underlying parasitic disease. He successfully underwent en-bloc hepatic pericystectomy and pericardiac resection with closure of the pericardial defect using a xenogeneic patch. After this procedure, he recovered well and had no cardiac complications in the long term. Under treatment with albendazol, the patient showed no signs of recurrent disease. Cases of complex cystic echinococcosis, which invade adjacent organs or body cavities, often need radical surgery for definitive treatment embedded in a multidisciplinary approach in highly specialized centers.
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http://dx.doi.org/10.1093/jscr/rjaa492DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875092PMC
February 2021

Pancreatic fistulas following distal pancreatectomy are unrelated to the texture quality of the pancreas.

Langenbecks Arch Surg 2021 May 8;406(3):729-734. Epub 2021 Jan 8.

Department of Surgery and Transplantation, Swiss Hepato-Pancreato-Biliary (HPB) Center, University Hospital Zurich, Raemistrasse 100, 8091, Zurich, Switzerland.

Purpose: The relevance of pancreatic texture for pancreatic fistula (POPF) formation after distal pancreatectomy (DP) remains ill defined. Recent POPF definition adjustments and common subjective pancreatic texture assessment are further drawbacks in the investigation of pancreatic texture as a factor for POPF development after DP.

Methods: The predictive value of pancreatic texture by histologic assessment was investigated for POPF formation after DP, respecting the updated 2016 fistula definition. Histologic evaluation at the resection margin included amount of steatosis, degree of fibrosis, and pancreatic duct size.

Results: A total of 102 patients who underwent DP were included. Thirty-six patients developed POPF. There was no difference in histologic variables in patients with and without POPF. In the univariate analysis, none of the three histologic features showed significant correlation with POPF formation. The ROC (receiver operating characteristic) curve demonstrated poor utility for the grade of steatosis 0.481 ± 0.058 (p = 0.75) and grade of fibrosis 0.466 ± 0.058 (p = 0.57) as predictive factors for POPF formation.

Conclusion: Results indicate that pancreatic texture does not predict POPF formation following DP. This is particularly relevant in the context of the increasing use of robotic and laparoscopic approaches for DPs with limited clinical pancreatic texture assessment by palpation.
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http://dx.doi.org/10.1007/s00423-020-02071-yDOI Listing
May 2021

First Long-term Oncologic Results of the ALPPS Procedure in a Large Cohort of Patients With Colorectal Liver Metastases.

Ann Surg 2020 11;272(5):793-800

Department of Surgery, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands.

Objectives: To analyze long-term oncological outcome along with prognostic risk factors in a large cohort of patients with colorectal liver metastases (CRLM) undergoing ALPPS.

Background: ALPPS is a two-stage hepatectomy variant that increases resection rates and R0 resection rates in patients with primarily unresectable CRLM as evidenced in a recent randomized controlled trial. Long-term oncologic results, however, are lacking.

Methods: Cases in- and outside the International ALPPS Registry were collected and completed by direct contacts to ALPPS centers to secure a comprehensive cohort. Overall, cancer-specific (CSS), and recurrence-free (RFS) survivals were analyzed along with independent risk factors using Cox-regression analysis.

Results: The cohort included 510 patients from 22 ALPPS centers over a 10-year period. Ninety-day mortality was 4.9% and median overall survival, CSS, and RFS were 39, 42, and 15 months, respectively. The median follow-up time was 38 months (95% confidence interval 32-43 months). Multivariate analysis identified tumor-characteristics (primary T4, right colon), biological features (K/N-RAS status), and response to chemotherapy (Response Evaluation Criteria in Solid Tumors) as independent predictors of CSS. Traditional factors such as size of metastases, uni versus bilobar involvement, and liver-first approach were not predictive. When hepatic recurrences after ALPPS was amenable to surgical/ablative treatment, median CSS was significantly superior compared to chemotherapy alone (56 vs 30 months, P < 0.001).

Conclusions: This large cohort provides the first evidence that patients with primarily unresectable CRLM treated by ALPPS have not only low perioperative mortality, but achieve appealing long-term oncologic outcome especially those with favorable tumor biology and good response to chemotherapy.
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http://dx.doi.org/10.1097/SLA.0000000000004330DOI Listing
November 2020

Choices of Therapeutic Strategies for Colorectal Liver Metastases Among Expert Liver Surgeons: A Throw of the Dice?

Ann Surg 2020 11;272(5):715-722

Department of Radiology, University Hospital Zurich, Zurich, Switzerland.

Objective: To test the degree of agreement in selecting therapeutic options for patients suffering from colorectal liver metastasis (CRLM) among surgical experts around the globe.

Summary/background: Only few areas in medicine have seen so many novel therapeutic options over the past decades as for liver tumors. Significant variations may therefore exist regarding the choices of treatment, even among experts, which may confuse both the medical community and patients.

Methods: Ten cases of CRLM with different levels of complexity were presented to 43 expert liver surgeons from 23 countries and 4 continents. Experts were defined as experienced surgeons with academic contributions to the field of liver tumors. Experts provided information on their medical education and current practice in liver surgery and transplantation. Using an online platform, they chose their strategy in treating each case from defined multiple choices with added comments. Inter-rater agreement among experts and cases was calculated using free-marginal multirater kappa methodology. A similar, but adjusted survey was presented to 60 general surgeons from Asia, Europe, and North America to test their attitude in treating or referring complex patients to expert centers.

Results: Thirty-eight (88%) experts completed the evaluation. Most of them are in leading positions (92%) with a median clinical experience of 25 years. Agreement on therapeutic strategies among them was none to minimal in more than half of the cases with kappa varying from 0.00 to 0.39. Many general surgeons may not refer the complex cases to expert centers, including in Europe, where they also engage in complex liver surgeries.

Conclusions: Considerable inconsistencies of decision-making exist among expert surgeons when choosing a therapeutic strategy for CRLM. This might confuse both patients and referring physicians and indicate that an international high-level consensus statements and widely accepted guidelines are needed.
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http://dx.doi.org/10.1097/SLA.0000000000004331DOI Listing
November 2020

Liver transplantation and hepatobiliary surgery in 2020.

Int J Surg 2020 10 19;82S:1-3. Epub 2020 Jul 19.

Department of Surgery and Liver Transplantation Unit, Ankara University School of Medicine, Ankara, Turkey.

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http://dx.doi.org/10.1016/j.ijsu.2020.07.028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7369005PMC
October 2020

Modern therapeutic approaches for the treatment of malignant liver tumours.

Nat Rev Gastroenterol Hepatol 2020 12 17;17(12):755-772. Epub 2020 Jul 17.

Swiss HPB and Transplantation Center, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland.

Malignant liver tumours include a wide range of primary and secondary tumours. Although surgery remains the mainstay of curative treatment, modern therapies integrate a variety of neoadjuvant and adjuvant strategies and have achieved dramatic improvements in survival. Extensive tumour loads, which have traditionally been considered unresectable, are now amenable to curative treatment through systemic conversion chemotherapies followed by a variety of interventions such as augmentation of the healthy liver through portal vein occlusion, staged surgeries or ablation modalities. Liver transplantation is established in selected patients with hepatocellular carcinoma but is now emerging as a promising option in many other types of tumour such as perihilar cholangiocarcinomas, neuroendocrine or colorectal liver metastases. In this Review, we summarize the available therapies for the treatment of malignant liver tumours, with an emphasis on surgical and ablative approaches and how they align with other therapies such as modern anticancer drugs or radiotherapy. In addition, we describe three complex case studies of patients with malignant liver tumours. Finally, we discuss the outlook for future treatment, including personalized approaches based on molecular tumour subtyping, response to targeted drugs, novel biomarkers and precision surgery adapted to the specific tumour.
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http://dx.doi.org/10.1038/s41575-020-0314-8DOI Listing
December 2020

Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) procedure for cholangiocarcinoma.

Int J Surg 2020 Oct 7;82S:97-102. Epub 2020 Jul 7.

Swiss HPB and Transplantation Center, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland. Electronic address:

Perihilar cholangiocarcinoma (PHCC) has been a great challenge for surgeons, requiring advanced skills and expertise and was often associated with high morbidity and mortality. Resectability rates are up to 75% even in experienced centers. In patients with PHCC, radical liver and bile duct resection aiming R0 surgical margins offers the best long-term survival. Therefore, extensive resections with low FLR are commonly needed and PVE is offered to induce remnant liver hypertrophy for a long period. Associating liver partition with portal vein ligation for staged hepatectomy (ALPPS) is considered a promising approach inducing rapid remnant hypertrophy to prevent dropouts due to complications or tumor progression and increase resectability. Although poor results were reported initially, refinements in technique and risk adjustment of patient selection improved outcomes. The procedure is still under debate for the indication of PHCC. This article reviews the current literature on ALPPS in treatment of perihilar and intrahepatic cholangiocarcinoma.
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http://dx.doi.org/10.1016/j.ijsu.2020.06.045DOI Listing
October 2020

Replaced right hepatic artery arising from the gastroduodenal artery: a rare and challenging anatomical variant of the Whipple procedure.

J Surg Case Rep 2020 Jun 17;2020(6):rjaa136. Epub 2020 Jun 17.

Department of Surgery, Division of Hepato-Biliary and Pancreatic Surgery, University Hospital del mar, Barcelona, Spain.

Accurate assessment of the vascular anatomy is a prerequisite of any pancreatic resection, since an unnoticed arterial injury in the context of a complex resection such as Whipple procedure, can seriously jeopardize patient's safety. This article aims to describe an infrequent anatomic variant of a replaced right hepatic artery originating directly from the gastroduodenal artery and its potential implications for duodenopancreatectomy, as the gastroduodenal artery is routinely divided. We present here two different cases of this arterial abnormality identified during a Whipple procedure and its implications in each different setting. Preoperative identification of anatomical variations is essential for proficient surgical planning. Nevertheless, when detected during surgery, an meticulous dissection of the hepatoduodenal ligament is required to identify all the vascular relations in order to avoid irreversible damage.
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http://dx.doi.org/10.1093/jscr/rjaa136DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7299609PMC
June 2020

Robotic liver resection: Hurdles and beyond.

Int J Surg 2020 Oct 3;82S:155-162. Epub 2020 Jun 3.

New York-Presbyterian/Weill Cornell Medical Center, New York, NY, USA.

Laparoscopy is currently considered the standard of care for certain procedures such as left-lateral sectionectomies and wedge resections of anterior segments. The role of robotic liver surgery is still under debate, especially with regards to oncological outcomes. The purpose of this review is to describe how the field of robotic liver surgery has expanded, and to identify current limitations and future perspectives of the technology. Available evidences suggest that oncologic results after robotic liver resection are comparable to open and laparoscopic approaches for hepatocellular carcinoma and colorectal liver metastases, with identifiable advantages for cirrhotic patients and patients undergoing repeat resections. Excellent outcomes and optimal patient safety can be only achieved with specific hepato-biliary and general minimally invasive training to overcome the learning curve.
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http://dx.doi.org/10.1016/j.ijsu.2020.05.070DOI Listing
October 2020

Current status of liver transplantation in Europe.

Int J Surg 2020 Oct 23;82S:22-29. Epub 2020 May 23.

Swiss HPB and Transplantation Center, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland. Electronic address:

Liver transplantation (LT) in Europe became an established life-saving treatment for patients with end-stage liver disease, hepatocellular carcinoma, and acute liver conditions with life-threatening hepatic dysfunction. Although there are substantial disparities in donation and transplant rates among European countries, LT can be offered to almost every European citizen today. In order to maximize the LT benefit beyond national levels, many countries cooperate within transnational organizations including Eurotransplant, Scandiatransplant, and Southern Alliance for Transplantation. In the majority of European countries, liver allocation is based on the Model for End-Stage Liver Disease (MELD). Similar to North America, the ongoing extinction of hepatitis C and increase of non-alcoholic steatohepatitis are also a hallmark of change in LT indications in Europe. Apart from Turkey, the organ pool for LT in European countries is mainly based on organs from donors after brain death, although some countries retrieve a substantial proportion of organs from donors after circulatory death. According to the 2018 report of the European Liver Transplant Registry, 146,762 LT have been performed in Europe until 2016. In the most recent period, LT in Europe achieved respectable 1- and 5-year overall survival rates of 86% and 74%.
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http://dx.doi.org/10.1016/j.ijsu.2020.05.062DOI Listing
October 2020

ALPPS for Locally Advanced Intrahepatic Cholangiocarcinoma: Did Aggressive Surgery Lead to the Oncological Benefit? An International Multi-center Study.

Ann Surg Oncol 2020 May 30;27(5):1372-1384. Epub 2020 Jan 30.

Department of General, Visceral and Transplantation Surgery, University Hospital Frankfurt, Frankfurt, Germany.

Background: ALPPS is found to increase the resectability of primary and secondary liver malignancy at the advanced stage. The aim of the study was to verify the surgical and oncological outcome of ALPPS for intrahepatic cholangiocarcinoma (ICC).

Methods: The study cohort was based on the ALPPS registry with patients from 31 international centers between August 2009 and January 2018. Propensity score matched patients receiving chemotherapy only were selected from the SEER database as controls for the survival analysis.

Results: One hundred and two patients undergoing ALPPS were recruited, 99 completed the second stage with median inter-stage duration of 11 days. The median kinetic growth rate was 23 ml/day. R0 resection was achieved in 87 (85%). Initially high rates of morbidity and mortality decreased steadily to a 29% severe complication rate and 7% 90-day morbidity in the last 2 years. Post-hepatectomy liver failure remained the main cause of 90-day mortality. Multivariate analysis revealed insufficient future liver remnant at the stage-2 operation (FLR2) to be the only risk factor for severe complications (OR 2.91, p = 0.02). The propensity score matching analysis showed a superior overall survival in the ALPPS group compared to palliative chemotherapy (median overall survival: 26.4 months vs 14 months; 1-, 2-, and 3-year survival rates: 82.4%, 70.5% and 39.6% vs 51.2%, 21.4% and 11.3%, respectively, p < 0.01). The survival benefit, however, was not confirmed in the subgroup analysis for patients with insufficient FLR2 or multifocal ICC.

Conclusion: ALPPS showed high efficacy in achieving R0 resections in locally advanced ICC. To get the most oncological benefit from this aggressive surgery, ALPPS would be restricted to patients with single lesions and sufficient FLR2.
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http://dx.doi.org/10.1245/s10434-019-08192-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7138775PMC
May 2020

How to Handle Arterial Conduits in Liver Transplantation? Evidence From the First Multicenter Risk Analysis.

Ann Surg 2020 Jan 16. Epub 2020 Jan 16.

Swiss HPB & Transplant Center Zurich, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland.

Objective: The aims of the present study were to identify independent risk factors for conduit occlusion, compare outcomes of different AC placement sites, and investigate whether postoperative platelet antiaggregation is protective.

Background: Arterial conduits (AC) in liver transplantation (LT) offer an effective rescue option when regular arterial graft revascularization is not feasible. However, the role of the conduit placement site and postoperative antiaggregation is insufficiently answered in the literature.

Study Design: This is an international, multicenter cohort study of adult deceased donor LT requiring AC. The study included 14 LT centers and covered the period from January 2007 to December 2016. Primary endpoint was arterial occlusion/patency. Secondary endpoints included intra- and perioperative outcomes and graft and patient survival.

Results: The cohort was composed of 565 LT. Infrarenal aortic placement was performed in 77% of ACs whereas supraceliac placement in 20%. Early occlusion (≤30 days) occurred in 8% of cases. Primary patency was equivalent for supraceliac, infrarenal, and iliac conduits. Multivariate analysis identified donor age >40 years, coronary artery bypass, and no aspirin after LT as independent risk factors for early occlusion. Postoperative antiaggregation regimen differed among centers and was given in 49% of cases. Graft survival was significantly superior for patients receiving aggregation inhibitors after LT.

Conclusion: When AC is required for rescue graft revascularization, the conduit placement site seems to be negligible and should follow the surgeon's preference. In this high-risk group, the study supports the concept of postoperative antiaggregation in LT requiring AC.
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http://dx.doi.org/10.1097/SLA.0000000000003753DOI Listing
January 2020

Renal Impairment Is Associated with Reduced Outcome After Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy.

J Gastrointest Surg 2020 11 19;24(11):2500-2507. Epub 2019 Nov 19.

Department of Surgery, Division of Hepatobiliary and Pancreatic Surgery, Asklepios Hospital Barmbek, Rübenkamp 220, 22291, Hamburg, Germany.

Background: Impaired postoperative renal function is associated with increased morbidity and mortality after liver resection. The role of impaired renal function in the two-stage hepatectomy setting of associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) is unknown.

Methods: An international multicenter cohort of ALPPS patients captured in the ALPPS Registry was analyzed. Particular attention was drawn to the renal function in the interstage interval to determine outcome after stage 2 surgery. Interstage renal impairment (RI) was defined as an increase of serum creatinine of ≥ 0.3 mg/dl referring to a preoperative value or an increase of serum creatinine of ≥ 1.5× of the preoperative value on the fifth postoperative day after stage 1.

Results: A total of 705 patients were identified of which 7.5% had an interstage RI. Patients developing an interstage RI were significantly older. During stage 1, a longer operation time, higher rate of intraoperative transfusions, and additional procedures were observed in patients that developed interstage RI. After stage 1, interstage RI patients had more major complications and higher interstage mortality (1% vs. 8%, p < 0.001). Furthermore, these patients developed more and severe complications after completion of stage 2. Mortality of patients with interstage RI was 38% vs. 8% without interstage RI. In 41% of patients with interstage RI, the renal function recovered before stage 2; however, the mortality after stage 2 remained 28% in those patients. Risk factors for the development of an interstage RI were age over 67 years, prolonged operative time, and additional procedure during stage 1.

Conclusion: This study shows that interstage RI is a predictor for interstage and post-stage 2 morbidity and perioperative mortality. The causality of impaired renal function on outcome, however, remains unknown. Interstage RI may directly cause adverse outcome but may also be a surrogate marker for major complications.
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http://dx.doi.org/10.1007/s11605-019-04419-2DOI Listing
November 2020

The potential of machine learning to predict postoperative pancreatic fistula based on preoperative, non-contrast-enhanced CT: A proof-of-principle study.

Surgery 2020 02 11;167(2):448-454. Epub 2019 Nov 11.

Institute of Diagnostic and Interventional Radiology, University of Zurich, University Hospital Zurich, Switzerland.

Background: Postoperative pancreatic fistula remains an unsolved challenge after pancreatoduodenectomy. Important in this regard is the presence of a soft pancreatic texture which is a major risk factor. Advances in machine learning and texture analysis of medical images allow identification of features of parenchyma that are invisible to the human eye. The aim of this study was to investigate the potential of machine learning to predict postoperative pancreatic fistula based on preoperative, non-contrast-enhanced computed tomography.

Methods: We screened a prospectively assessed database including all patients undergoing pancreatoduodenectomy at a tertiary center from 2008 until 2018 for patients based on the occurrence of postoperative pancreatic fistula. In total, 110 patients were included, consisting of 55 patients who developed a postoperative pancreatic fistula and 55 without postoperative pancreatic fistula. For machine learning-based texture analysis preoperative, non-contrast-enhanced computed tomography axial images were used. Machine learning results were tested using 10-fold cross validation. Previously validated clinical fistula risk scores (original and alternative fistula risk scores) served as reference tests.

Results: Both the original and the alternative fistula risk scores showed good discrimination between patients without and with postoperative pancreatic fistula (area under the curve 0.76 and 0.72, respectively). Machine learning-based texture analysis showed potential to detect histologic fibrosis (area under the curve 0.84, sensitivity 75%; specificity 92%), histologic lipomatosis (area under the curve 0.82, sensitivity 78%; specificity 89%), and intraoperative pancreatic hardness (area under the curve 0.70, sensitivity 78%; specificity 74%). The features of the machine learning-based texture analysis were most accurate in predicting the occurrence of postoperative pancreatic fistula (area under the curve 0.95, sensitivity of 96%; specificity 98%) after pancreatoduodenectomy.

Conclusion: This proof-of-principle study suggests the ability of machine learning in recognizing important features of pancreatic texture associated with an increased risk of postoperative pancreatic fistula based on preoperative computed tomography.
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http://dx.doi.org/10.1016/j.surg.2019.09.019DOI Listing
February 2020

Avoiding Dual Graft Loss in Simultaneous Liver Retransplantation and Primary Kidney Transplantation.

Authors:
Henrik Petrowsky

Transplantation 2020 07;104(7):1328-1329

Swiss HPB and Transplantation Center Zurich, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland.

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http://dx.doi.org/10.1097/TP.0000000000003036DOI Listing
July 2020

Perioperative omega-3 fatty acids fail to confer protection in liver surgery: Results of a multicentric, double-blind, randomized controlled trial.

J Hepatol 2020 03 15;72(3):498-505. Epub 2019 Oct 15.

Center of General Surgery and Liver Transplantation, Fundeni Institute Bucharest, Romania.

Background & Aims: In a variety of animal models, omega-3 polyunsaturated fatty acids (Ω3-FAs) conferred strong protective effects, alleviating hepatic ischemia/reperfusion injury and steatosis, as well as enhancing regeneration after major tissue loss. Given these benefits along with its safety profile, we hypothesized that perioperative administration of Ω3-FAs in patients undergoing liver surgery may ameliorate the postoperative course. The aim of this study was to investigate the perioperative use of Ω3-FAs to reduce postoperative complications after liver surgery.

Methods: Between July 2013 and July 2018, we carried out a multicentric, double-blind, randomized, placebo-controlled trial designed to test whether 2 single intravenous infusions of Omegaven® (Ω3-FAs) vs. placebo may decrease morbidity. The primary endpoints were postoperative complications by severity (Clavien-Dindo classification) integrated within the comprehensive complication index (CCI).

Results: A total of 261 patients (132 in the Omegaven and 129 in the placebo groups) from 3 centers were included in the trial. Most cases (87%, n = 227) underwent open liver surgery and 56% (n = 105) were major resections (≥3 segments). In an intention-to-treat analysis including the dropout cases, the mortality rate was 4% and 2% in the Omegaven and placebo groups (odds ratio0.40;95% CI 0.04-2.51; p = 0.447), respectively. Any complications and major complications (Clavien-Dindo ≥ 3b) occurred in 46% vs. 43% (p = 0.709) and 12% vs. 10% (p = 0.69) in the Omegaven and placebo groups, respectively. The mean CCI was 17 (±23) vs.14 (±20) (p = 0.417). An analysis excluding the dropouts provided similar results.

Conclusions: The routine perioperative use of 2 single doses of intravenous Ω3-FAs (100 ml Omegaven) cannot be recommended in patients undergoing liver surgery (Grade A recommendation).

Lay Summary: Despite strong evidence of omega-3 fatty acids having liver-directed, anti-inflammatory and pro-regenerative action in various rodent models, 2 single omega-3 fatty acid infusions given to patients before and during liver surgery failed to reduce complications. Because single omega-3 fatty acid infusions failed to confer liver protection in this trial, they cannot currently be recommended.

Trial Registration: ClinicalTrial.gov: ID: NCT01884948; Institution Ethical Board Approval: KEK-ZH-Nr. 2010-0038; Swissmedic Notification: 2012DR3215.
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http://dx.doi.org/10.1016/j.jhep.2019.10.004DOI Listing
March 2020

Defining Benchmark Outcomes for ALPPS.

Ann Surg 2019 11;270(5):835-841

Swiss HPB and Transplant Center Zurich, Department of Surgery and Transplantation, University Hospital Zurich, Switzerland.

Objective: The aim of this study was to use the concept of benchmarking to establish robust and standardized outcome references after the procedure ALPPS (Associating Liver Partition and Portal Vein Ligation for Staged hepatectomy).

Background And Aims: The recently developed ALPPS procedure, aiming at removing primarily unresectable liver tumors, has been criticized for safety issues with high variations in the reported morbidity/mortality rates depending on patient, disease, technical characteristics, and center experience. No reference values for relevant outcome parameters are available.

Methods: Among 1036 patients registered in the international ALPPS registry, 120 (12%) were benchmark cases fulfilling 4 criteria: patients ≤67 years of age, with colorectal metastases, without simultaneous abdominal procedures, and centers having performed ≥30 cases. Benchmark values, defined as the 75th percentile of the median outcome parameters of the centers, were established for 10 clinically relevant domains.

Results: The benchmark values were completion of stage 2: ≥96%, postoperative liver failure (ISGLS-criteria) after stage 2: ≤5%, ICU stay after ALPPS stages 1 and 2: ≤1 and ≤2 days, respectively, interstage interval: ≤16 days, hospital stay after ALPPS stage 2: ≤10 days, rates of overall morbidity in combining both stage 1 and 2: ≤65% and for major complications (grade ≥3a): ≤38%, 90-day comprehensive complication index was ≤22, the 30-, 90-day, and 6-month mortality was ≤4%, ≤5%, and 6%, respectively, the overall 1-year, recurrence-free, liver-tumor-free, and extrahepatic disease-free survival was ≥86%, ≥50%, ≥57%, and ≥65%, respectively.

Conclusions: This benchmark analysis sets key reference values for ALPPS, indicating similar outcome as other types of major hepatectomies. Benchmark cutoffs offer valid tools not only for comparisons with other procedures, but also to assess higher risk groups of patients or different indications than colorectal metastases.
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http://dx.doi.org/10.1097/SLA.0000000000003539DOI Listing
November 2019

ALPPS in neuroendocrine liver metastases not amenable for conventional resection - lessons learned from an interim analysis of the International ALPPS Registry.

HPB (Oxford) 2020 04 17;22(4):537-544. Epub 2019 Sep 17.

Department of Surgery and Cancer, Imperial College London, London, UK. Electronic address:

Background: Surgery is the most effective treatment option for neuroendocrine liver metastases (NELM). This study investigated the role of associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) as a novel strategy in treatment of NELM.

Methods: The International ALPPS Registry was reviewed to study patients who underwent ALPPS for NELM.

Results: From 2010 to 2017, 954 ALPPS procedures from 135 international centers were recorded in the International ALPPS Registry. Of them, 24 (2.5%) were performed for NELM. Twenty-one patients entered the final analysis. Overall grade ≥3b morbidity was 9% after stage 1 and 27% after stage 2. Ninety-day mortality was 5%. R0 resection was achieved in 19 cases (90%) at stage 2. Median follow-up was 28 (19-48) months. Median disease free survival (DFS) was 17.3 (95% CI: 7.1-27.4) months, 1-year and 2-year DFS was 73.2% and 41.8%, respectively. Median overall survival (OS) was not reached. One-year and 2-year OS was 95.2% and 95.2%, respectively.

Conclusions: ALPPS appears to be a suitable strategy for inclusion in the multimodal armamentarium of well-selected patients with neuroendocrine liver metastases. In light of the morbidity in this initial series and a high rate of disease-recurrence, the procedure should be taken with caution.
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http://dx.doi.org/10.1016/j.hpb.2019.08.011DOI Listing
April 2020

Editorial: Living-donor liver transplantation: why the Sun rises in the East and sets in the West?

Curr Opin Organ Transplant 2019 10;24(5):620-622

Liver Transplantation and HPB Center, Florence Nightingale Hospital, Istanbul, Turkey.

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http://dx.doi.org/10.1097/MOT.0000000000000700DOI Listing
October 2019

Pancreatectomy and body mass index: an international evaluation of cumulative postoperative complications using the comprehensive complications index.

HPB (Oxford) 2019 12 30;21(12):1761-1772. Epub 2019 May 30.

Department of Surgery, Emory University, Atlanta, GA, USA; Winship Cancer Institute, Emory University, Atlanta, GA, USA. Electronic address:

Background: Overweight and obese patients undergoing pancreatectomy are at increased risk for postoperative complications and readmission. We examined the association between body mass index (BMI) and postoperative complications following major pancreatectomy using the novel Comprehensive Complications Index (CCI), which analyzes the impact of multiple surgical complications rather than just the most severe.

Methods: We performed a retrospective dual institutional international review of 500 consecutive patients who underwent pancreatic resection and assessed the association of BMI with postoperative complications using the CCI and Clavien-Dindo Classification (CDC) with uni- and multivariable analyses.

Results: Overweight and obese patients undergoing pancreatic resection demonstrated a higher incidence and severity of CCI-measured complications (29.3 vs. 21.1, P < 0.001), more pancreatic fistulae (15.4 vs. 8.8%, 95% CI 1.005 -1.902), and an increased 30-day readmission rate (21.1 vs. 12.1%, 95% CI 1.067 -1.852) (all p < 0.05) than normal-BMI patients. The CCI was a more sensitive marker of post-pancreatectomy complications relative to the CDC, with a higher multicomplication rate in overweight/obese patients (54.8% vs. 44.5%).

Conclusion: Patients with overweight and obese body mass index undergoing major pancreatectomy demonstrated higher rates of postoperative complications, pancreatic fistulae, and readmissions. The CCI is a more robust and sensitive tool to assess post-pancreatectomy complications than the CDC.
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http://dx.doi.org/10.1016/j.hpb.2019.04.006DOI Listing
December 2019

The power to predict with biomarkers: carbohydrate antigen 19-9 (CA 19-9) and carcinoembryonic antigen (CEA) serum markers in intrahepatic cholangiocarcinoma.

Transl Gastroenterol Hepatol 2019 4;4:23. Epub 2019 Apr 4.

Swiss HPB and Transplantation Center Zurich, Department of Surgery and Transplantation, University Hospital Zurich, Zurich, Switzerland.

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http://dx.doi.org/10.21037/tgh.2019.03.06DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6509429PMC
April 2019
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