Liver Transplantation Using Allografts With Recent Liver Blunt Trauma: A Nationwide Audit From the French CRISTAL Biomedicine Agency Registry : Transplantation

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Original Clinical Science—Liver

Liver Transplantation Using Allografts With Recent Liver Blunt Trauma: A Nationwide Audit From the French CRISTAL Biomedicine Agency Registry

Seckler, Florian MD1; Turco, Célia MD1,2; Mohkam, Kayvan MD, PhD3; Addeo, Pietro MD, PhD4; Robin, Fabien MD5; Cauchy, François MD, PhD6; Maulat, Charlotte MD7; Brustia, Raffaele MD, PhD8; Paquette, Brice MD1; Faitot, François MD, PhD4; Weil Verhoeven, Delphine MD, PhD9; Minello, Anne MD, PhD10; Lakkis, Zaher MD, PhD1; Di Martino, Vincent MD, PhD9; Latournerie, Marianne MD, PhD10; Chiche, Laurence MD, PhD11; El Amrani, Mehdi MD, PhD12; Bucur, Petru MD, PhD13; Navarro, Francis MD, PhD14; Chopinet, Sophie MD15; Chirica, Mircea MD, PhD16; Gagnière, Johan MD, PhD17; Iannelli, Antonio MD, PhD18; Cheisson, Gaëlle MD19; Chardot, Christophe MD, PhD20; Sommacale, Daniele MD, PhD8; Muscari, Fabrice MD, PhD7; Dondero, Federica MD6; Sulpice, Laurent MD, PhD5; Bachellier, Philippe MD, PhD4; Scatton, Olivier MD, PhD2; Mabrut, Jean Yves MD, PhD3; Heyd, Bruno MD, PhD1; Doussot, Alexandre MD, PhD1

Author Information
Transplantation: November 22, 2022 - Volume - Issue - 10.1097/TP.0000000000004434
doi: 10.1097/TP.0000000000004434
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Abstract

INTRODUCTION

In the current setting of organ shortage, alongside expanding the overall donor pool to donors after circulatory death, extending criteria for brain-dead liver donors remains a relevant option for reducing time and mortality on the waiting list.1 Extended criteria donors (ECDs) for liver transplantation (LT) are classically defined by donor age >65 y, hepatitis C virus–positive donor, split livers, prolonged cold ischemia duration, and graft macrosteatosis >30%.2,3 Another potential pool of donors is represented by brain-dead liver donors from head trauma. Indeed, head trauma stands as the second cause of death of brain-dead donors after brain death from vascular pathology.4 In a significant proportion of head traumas, multiorgan traumas, including liver trauma, are present.5 Yet, multiorgan procurement in patients with multivisceral trauma remains a rare situation. One can hypothesize that multiorgan procurement is generally not considered in this setting. Consequently, outcomes of LT using liver graft from a donor with a recent liver trauma (RLT) remain undefined. Nevertheless, preliminary data limited to 2 retrospective series of 15 and 14 patients and a few case reports suggested that LT using grafts from donors with RLT was feasible and safe.6-8 The current study aimed at evaluating both feasibility and safety of LT using grafts from donors with liver trauma using data from the nationwide French CRISTAL Biomedicine Agency registry.

MATERIALS AND METHODS

Study Population

All liver grafts from brain-dead donors with RLT proposed for LT in France between January 1, 2010, and December 31, 2018, were identified from the nationwide CRISTAL registry from the Biomedicine Agency. In France, donor inventory and graft allocation based on the liver score at a nationwide level are regulated by the Biomedicine Agency.9 Liver grafts from donors with RLT were identified from the CRISTAL registry online database approved by the French Data Protection Authority (Commission Nationale de l’Informatique et des Libertés; Decision no. 96-025 of March 19, 1996). Additional specific data related to the current study were provided by each participating center to the Biomedicine Agency. A waiver of written informed consent was obtained from the Scientific and Ethics Committee of the Biomedicine Agency. This study complied with the Strenghtening the Reporting of Observational Studies in Epidemiology Statement guidelines.10

Data Collection

The following data were collected: recipients’ characteristics at the time of transplantation, donors’ characteristics and cause of death, intraoperative data, and postoperative outcomes. ECDs were donors aged >65 y or with steatosis >30%. All postoperative complications occurring within 90 d after surgery were collected and graded according to the Dindo-Clavien classification.11 Severe morbidity was defined as any complication graded III, IV, or V. In patients with multiple complications, the highest grade was retained for analysis. LT-specific complications‚ such as anastomotic biliary complications and primary nonfunction‚ were defined according to usual definitions.12-15

Liver Trauma Grading and Management

All data related to the liver trauma, such as the nature of the trauma (motor vehicle accident or not), the initial cardiac arrest, the existence, and the number of injured extrahepatic organs, were retrieved. Liver trauma was graded using the American Association for the Surgery of Trauma (AAST) liver injury grading system developed from the Moore et al16 classification described in 1989. As body CT scan details have been routinely included in the CRISTAL registry since 2015, imaging details before 2015 were not available. Additionally, data on pretransplantation RLT management, directed to the liver involving hepatic artery embolization and open abdomen with abdominal packing or directed to other organs involving interventional radiology or surgery, were collected.

Statistical Analysis

The χ2 test was used for analysis of categorical variables. Continuous variables with a normal distribution are presented as the mean (standard deviation) and nonnormally distributed variables as the median (range); the t test and Mann-Whitney U test, respectively, were used for statistical analysis. Overall patient and graft survival estimates were calculated using the Kaplan-Meier method. Patient and graft survival corresponded to the interval between LT and the date of last follow-up or death and between LT and date of graft failure, respectively. All P values were based on 2-tailed statistical analysis‚ and a P value <0.050 was considered to indicate statistical significance. Analyses were performed with SPSS software, version 27.0‚ for Windows (IBM, Armonk, NY).

RESULTS

Donors’ Characteristics

Among 11 073 LTs, 142 LTs (1.3%) using grafts with RLT were performed. These 142 LTs (LT+ group) including 23 split LTs were performed from 131 donors (45.8%) of 284 donors with RLT proposed for LT (Figure 1).

F1
FIGURE 1.:
Study flowchart.

Donors’ characteristics are listed in Table 1. Overall, 174 donors (61%) were male. Mean donors’ age was 32 y. Most donors presented with multiorgan trauma (n = 240; 85%).

TABLE 1. - Donors’ characteristics (n = 284)
All (n = 284) LT + group (n = 131) LT group (n = 153) P
Sex 0.503
 Male 174 (61%) 83 (63%) 91 (59%)
 Female 110 (39%) 48 (37%) 62 (41%)
Age, y 32 (17) 31 (15) 33 (19) 0.554
Body mass index, kg/m2 23.5 (4.4) 23.4 (3.7) 23.5 (4.9) 0.754
No past surgical history 184 (65%) 83 (63%) 101 (66%) 0.641
No medical history 186 (66%) 92 (70%) 94 (61%) 0.120
Cause of blunt trauma 0.281
 Traumatic MVA 188 (66%) 91 (70%) 97 (63%)
 Traumatic non-MVA 96 (34%) 40 (31%) 56 (37%)
 Initial cardiac arrest 107 (38%) 44 (34%) 63 (41%) 0.188
 Multiorgan trauma 240 (85%) 116 (89%) 124 (81%) 0.081
No. injured extrahepatic organ 0.131
 0 44 (16%) 15 (12%) 29 (19%)
 1 145 (51%) 76 (58%) 69 (45%)
 2 66 (23%) 27 (21%) 39 (26%)
 3 17 (6%) 8 (6%) 9 (6%)
 4 9 (3%) 5 (4%) 4 (3%)
 5 3 (1%) 0 (0%) 3 (2%)
Biology
 Prothrombin, % 59 (16) 61 (15) 58 (17) 0.029
 ASAT, UI/L 265 (366) 142 (151) 376 (458) <0.001
 ALAT, UI/L 228 (334) 118 (118) 328 (423) <0.001
 GGT, UI/L 56 (108) 42 (61) 69 (137) 0.005
 PAL, UI/L 83 (58) 76 (52) 90 (62) 0.021
 Bilirubin, µmol/L 19 (18.7) 16.9 (15) 20.9 (21.5) 0.345
 Arterial lactates, mmol/L 2.8 (2.4) 2.2 (1.7) 3.4 (2.7) <0.001
CT scan a (n = 124) (n = 84) (n = 40)
 Hemoperitoneum 40 (32%) 16 (19%) 24 (60%) 0.013
 Liver trauma grading <0.001
  AAST grade 1 46 (37%) 38 (45%) 8 (20%)
  AAST grade 2 42 (34%) 27 (32%) 15 (38%)
  AAST grade 3 25 (20%) 19 (23%) 6 (15%)
  AAST grade 4 10 (8%) 0 (0%) 10 (25%)
  AAST grade 5 1 (1%) 0 (0%) 1 (3%)
 Liver trauma location <0.001
  Right 54 (44%) 34 (40%) 20 (50%)
  Left 13 (10%) 12 (14%) 1 (3%)
  Central 18 (15%) 6 (7%) 12 (30%)
  Unknown 39 (31%) 32 (38%) 7 (18%)
Numbers are expressed as mean (standard deviation), unless otherwise specified.
aCT scan data have been routinely recorded since 2015.
AAST, American Association for the Surgery Trauma; ALAT, alanine aminotransferase; ASAT, aspartate aminotransferase; CT, computed tomography; GGT, gamma-glutamyl transferase; LT, liver transplantation; MVA, motor vehicle accident; PAL, alkaline phosphatase.

Upon comparison between donors in the LT+ group (n = 131) and LT group (n = 153), there was no difference in terms of donors’ gender, age, body mass index, or cause of trauma (Table 1). Transplanted grafts (LT+ group) were procured from donors with significantly lower liver enzyme levels and arterial lactates than not transplanted grafts. Regarding liver trauma imaging, descriptive data on liver trauma location and grade were available in 124 patients (44%) and are displayed in Table 1. Grafts in the LT+ group were procured from donors with significantly less advanced liver trauma according to the AAST liver grading system (P < 0.001). None of the transplanted grafts had a liver trauma grade greater than AAST 3.

Multiorgan and Liver Trauma Management

Before organ allocation, 20 (7%) of 284 donors underwent intervention related to RLT (damage control laparotomy, n = 15; hepatic artery embolization, n = 5). Among the 15 donors who underwent damage control laparotomy, most had perihepatic packing with open abdomen (n = 12)‚ and splenectomy (n = 6), colectomy (n = 1), or small bowel resection (n = 1) was performed to achieve damage control. Out of these 15 donors, 8 donors eventually underwent liver procurement‚ including 2 for split LT, resulting then in graft allocation to 10 recipients. Regarding those donors who required selective hepatic artery embolization (n = 5), 3 whole liver grafts were eventually procured and transplanted to 3 recipients.

Recipients’ Characteristics

Recipients’ characteristics are detailed in Table 2. Overall, 20 recipients were pediatric patients with an age ranging from 1 mo to 14 y. Of them, 12 patients (60%) received a left lobe split liver graft‚ and 8 (40%) received a whole liver graft. Out of these 12 split liver grafts, the right lobe was allocated to 12 adults recipients, of which 11 were eventually transplanted and 1 was discarded because of the right lobe trauma.

TABLE 2. - Recipients’ characteristics (n = 142)
Recipients’ characteristics
Sex
 Male 102 (72%)
 Female 40 (28%)
Age, y 46 (20)
BMI, kg.m-2 24.4 (5.1)
Pretransplantation condition
 Recipient at home 91 (64%)
 Recipient in hospital, no ICU 21 (15%)
 Recipient in ICU 29 (20%)
 With multiorgan failure 15 (11%)
Primary indication
 Alcoholic cirrhosis 34 (24%)
 HCC 30 (21%)
 Autoimmune 16 (11%)
 Congenital 11 (8%)
 Metabolic 10 (7%)
 HCV-related cirrhosis 8 (6%)
 Retransplantation 9 (6%)
 Fulminant hepatitis/acute liver failure 7 (5%)
 Other 15 (11%)
MELD score 20 (11)
Numbers are expressed as mean (standard deviation), unless otherwise specified
BMI, body mass index; ICU, intensive care unit; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; MELD, model for end-stage liver disease.

LT Outcomes

Mean cold ischemia time was 7.5 h (±2.4)‚ and mean operative time was 6.6 h (±2.4). The mean estimated blood loss was 1436 mL (±1133) with the need for intraoperative transfusion. During transplantation, specific surgical management directed to the liver trauma was reported in 19 patients (13%), consisting of local hemostatic control using electrocoagulation/topical agents (n = 15) or perihepatic packing (n = 1). Additionally, partial hepatic resection on back-table was performed in 3 patients.

One-year and 90-d mortality rates were 14% (n = 20) and 8.5% (n = 12), respectively. The main reasons for graft loss and mortality were multiple (n = 8), infection (n = 6), biliary complication (n = 3), vascular complication (n = 2), and primary nonfunction (n = 1). Overall, 5 patients experienced primary nonfunction, of which 4 underwent emergent retransplantation and were alive at 1 y after retransplantation, whereas 1 was not retransplanted and died on postoperative day 11.

Severe morbidity rate was 29.5% (n = 42). The main causes of severe morbidity were biliary complications (n = 14), vascular complications (n = 12), and hemorrhage (n = 11). Among those, 1-y overall survival and graft survival rates were 85% and 81%, respectively. Upon univariable analysis, no predictive factor of mortality within the first year after LT was identified (Table 3).

TABLE 3. - Predictive variables of mortality within 1 y after liver transplantation (n = 142)
OR 95% CI P
Donor characteristics
 Age, y 1.005 0.978-1.033 0.699
 Male gender 1.649 0.648-4.195 0.294
 Body mass index, kg/m2 1.056 0.939-1.188 0.303
 Initial cardiac arrest 1.135 0.423-3.044 0.801
 Multiorgan trauma 1.448 0.308-6.814 0.640
 Preprocurement biology
  Prothrombin rate, % 1.011 0.978-1.044 0.515
  ASAT, UI/L 1.002 0.999-1.005 0.129
  ALAT, UI/L 1.001 0.997-1.005 0.708
  GGT, UI/L 0.996 0.984-1.009 0.559
  PAL, UI/L 0.996 0.986-1.007 0.515
  Bilirubin, µmol/L 1.018 0.993-1.044 0.164
  Arterial lactates, mmol/L 1.240 0.983-1.564 0.070
 Liver trauma grading a
  AAST grade 1   Reference 0.876
  AAST grade 2 0.374 0.072-1.950 0.801
  AAST grade 3 0.571 0.107-3.053 0.513
 Preprocurement intervention 0.500 0.061-4.091 0.518
Recipients’ characteristics
 Pediatric 2.208 0.706-6.908 0.173
 Age, y 0.987 0.968-1.007 0.195
 Male gender 0.901 0.546-1.489 0.685
 Body mass index, kg/m2 0.935 0.847-1.032 0.184
 Pretransplantation condition 1.406 0.823-2.401 0.212
 MELD score 0.991 0.949-1.034 0.676
Liver transplantation procedure
 Cold ischemia time, min 1.003 1.001-1.006 0.075
 Use of split liver graft 1.788 0.582-5.492 0.310
Numbers are expressed as mean (standard deviation), unless otherwise specified.
an = 88, CT scan data have been routinely recorded since 2015.
AAST, American Association for the Surgery Trauma; ALAT, alanine aminotransferase; ASAT, aspartate aminotransferase; CI, confidence interval; CT, computed tomography; GGT, gamma-glutamyl transferase; MELD, model for end-stage liver disease; OR, odds ratio; PAL, alkaline phosphatase.

Regarding long-term outcomes, after a median follow-up time of 4.1 y, 5-y overall survival and graft survival rates were 77% and 72%, respectively (Figure 2).

F2
FIGURE 2.:
Overall patient (A) and graft (B) survival estimates among 142 recipients.

DISCUSSION

Using a large nationwide LT registry, including LT performed during a recent period, LT using graft from donors with RLT was found to be feasible and safe. Indeed, 1-y and 5-y overall and graft survivals seemed comparable with those reported from LT using conventional or ECDs.17,18 Additionally, this approach was also feasible and safe after aggressive donor resuscitation strategies involving intervention such as damage control laparotomy with perihepatic packing or interventional radiology with hepatic artery embolization. Yet, such a strategy was rarely required in the current series. Although the pool of donors with RLT remains confidential, >40% of donors with RLT considered for organ allocation eventually underwent organ procurement allowing subsequent LT. In this regard, both feasibility and safety of LT using grafts from donors with RLT should be at the knowledge of intensivists and surgeons managing trauma patients and also hepatologists and transplant surgeons to eventually expand this pool of donors.

As expected in the setting of trauma, donors considered for liver procurement were notably younger than usual donors. Among this pool of donors, donors with relatively limited liver trauma (AAST grades 1–3) were eventually selected for liver procurement with acceptable results after LT. These results are parallel to those observed in cases of surgical hepatic injuries during organ procurement, such as capsule tears, parenchymal ruptures, and subcapsular hematomas.19,20 Alongside the grade of liver trauma, liver grafts eventually transplanted were procured from donors with significantly lower liver enzyme levels than grafts eventually declined during the allocation procedure. Donor alanine aminotransferase/aspartate aminotransferase values have been previously reported as poorly correlated to the grade of liver injury.21 Nevertheless, one can suggest that decreasing alanine aminotransferase/aspartate aminotransferase kinetics should be a prerequisite for selecting donors with RLT, as in the case of anoxic death.

In the current series, 12 liver grafts from donors with RLT were procured and allocated to 12 pediatric recipients and 11 adult recipients, as 1 right lobe graft was discarded because of the presence of an AAST grade 3 liver injury affecting segments 7 and 8. The left lobe was transplanted to a 1-y-old child with acute liver failure, still alive 5 y later. This observation underlines that‚ even in the case of advanced liver trauma, liver procurement for a potential split LT can still be considered.8 Further to previous reports showing that split liver grafts could allow using 1 lobe liver grafts from donors with RLT, the current study brings safety data on using the 2 lobes in the case of limited liver trauma.

Although bringing original data from the largest reported cohort of LT using donors with RLT, this study presents limitations warranting discussion. First, its retrospective nature and the small size of the cohort may have hampered the identification of prognostic factors. Second, reports on liver trauma imaging were not standardized, and data were consequently lacking regarding AAST grade and trauma location. Similarly, RLT management details might have been underreported in the BMA registry. Finally, reasons for graft refusal are multiple and potentially related to the donor, such as trauma severity, and to the recipient, such as indication, acuity, morphology, or graft size mismatching. However, data did not clearly indicate whether the presence of liver trauma was the reason for graft refusal. Even further, all donors with RLT included in the nationwide registry are only those who were considered for organ procurement throughout the country over the study period. Available data did not allow evaluating the number of potential donors with RLT who were not considered for organ procurement. Consequently, the real size of this potential pool of donors remains undefined.

In conclusion, using liver grafts from donors with RLT was safe with acceptable long-term outcomes. All brain-dead patients with multiorgan trauma, including AAST grade 1 to 3 liver blunt trauma, should be considered as potential liver donors. Sharing these results may help in confirming and further expanding this potential pool of donors.

ACKNOWLEDGMENTS

The authors thank Aurélie Deshayes and Nicolas Chatauret from the Biomedicine Agency for their assistance. The authors acknowledge all collaborators of the CRISTAL Registry Study Group: Antonini Teresa antonini, Hôpital Edouard Herriot, Hospices Civils de Lyon, Lyon, France; Rodolphe Anty, CHU Nice, France; Bardou-Jacquet Edouard, CHU Rennes, France; BESCH Camille service de Chirurgie Générale, hépatique, Endocrinienne et Transplantation, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, France; Emmanuel BOLESLAWSKI, Hôpital Huriez, CHU Lille, France; Karim Boudjema, CHU Rennes, France; Sophie Branchereau, Hôpital Bicêtre, Le Kremlin-Bicêtre, France; Benjamin Buchard, Hôpital Estaing, CHU Clermont-Ferrand, France; Christophe Camus, Hôpital Pontchaillou, CHU Rennes, France; Faiza chermak, CHU Bordeaux, Pessac, France; Filomena Conti, Hôpital Pitié-Salpêtrière, Paris, France; Dominique Debray, Hôpital Universitaire Necker-Enfants Malades, Paris, France; Thomas Decaens, CHU Grenoble Alpes, Grenoble, France; Sébastien Dharancy, Hôpital Huriez, CHU Lille, France; François Durand, Hôpital Beaujon, Clichy, France; Claire Francoz, Hôpital Beaujon, Clichy, France; Michel Gabriel, CHU Tours, France; Baptiste Giguet, CHU Rennes, France; Edouard Girard, CHU Grenoble Alpes, Grenoble, France; Arnaud Gregoire, Hôpital Edouard Herriot, Hospices Civils de Lyon, France; Jean Hardwigsen, Hôpital la Timone, Marseille, France; Pauline HousseL-Debry, CHU Rennes, France; Emmanuel Jacquemin, Hôpital Bicêtre, Le Kremlin-Bicêtre, France; Caroline Jezequel, CHU Rennes, France; Florence Lallemant, Hôpital Salengro, CHU Lille; Alexis Laurent, Hôpital Henri-Mondor, Créteil, France; Mickaël Lesurtel, Hôpital Beaujon, Clichy, France; Clément Monet, Hôpital Saint-Éloi, CHU Montpellier, France; François-René Pruvot, Hôpital Huriez, CHU Lille, France; Mathieu Raux, Hôpital Pitié-Salpêtrière, Paris, France; Bruno Riou, Hôpital Pitié-Salpêtrière, Paris, France; Julien Rogier, CHU Bordeaux, France; Lawrence Serfaty, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, France; Bertrand Suc, Hôpital Rangueil, CHU Toulouse, France; Nicolas Tabchouri, CHU Tours, France; José Ursic Bedoya, Hôpital St-Eloi, CHU Montpellier, France; Florence Vachiery-Lahaye, CHU Montpellier, France; Jean-Christophe Venhard, CHU Tours, France; Philippe Wolf, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, France.

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