Author Affiliations: Department of General, Visceral and Transplantation Surgery, Charité, Campus Virchow, Berlin, Germany (Schmitz V, Schoening W, Globke B, Pascher A, Bahra M, Neuhaus P and Puhl G); Department of General Surgery, Luebeck, Germany (Jelkmann I)

Corresponding Author: Volker Schmitz, MD, Department of General, Visceral and Transplantation Surgery, Charité, Campus Virchow, Augustenburger Platz 1, Berlin 13353, Germany (Tel: 49-30-450-652194; Fax: 49-30-450-552900; Email: volker.schmitz@charite.de)

 

© 2014, Hepatobiliary Pancreat Dis Int. All rights reserved.

doi: 10.1016/S1499-3872(14)60250-2

 

 

Contributors: NP and PG proposed the study; SV, SW, JI and GB did the majority of data retrieval; SV and SW wrote the first draft and analyzed the data. PA and BM did contribute in re-reading the manuscript and giving valuable advice for improvements and interpretations; SV and SW had the generally lead in conducting the study and contributed equally to the manuscript. All authors contributed to the design and interpretation of the study and to further drafts. SV is the guarantor.

Funding: None.

Ethical approval: This study was approved by the local ethical committee.

Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

 

BACKGROUND: Originally, cava reconstruction (CR) in liver transplantation meant complete resection and reinsertion of the donor cava. Alternatively, preservation of the recipients inferior vena cava (IVC) with side-to-side anastomosis (known as "piggyback") can be performed. Here, partial clamping maintains blood flow of the IVC, which may improve cardiovascular stability, reduce blood loss and stabilize kidney function. The aim of this study was to compare both techniques with particular focus on kidney function.

 

METHODS: A series of 414 patients who had had adult liver transplantations (2006-2009) were included. Among them, 176 (42.5%) patients had piggyback and 238 had classical CR operation, 112 (27.1%) of the patients underwent CR accompanied with veno-venous bypass (CR-B) and 126 (30.4%) without a bypass. The choice of either technique was based on the surgeons' individual preference. Kidney function [serum creatinine, calculated glomerular filtration rate (GFR), RIFLE stages] was assessed over 14 days.

 

RESULTS: Lab-MELD scores were significantly higher in CR-B (22.5±11.0) than in CR (17.3±9.0) and piggyback (18.8±10.0) (P=0.008). Unexpectedly, the incidences of arterial stenoses (P=0.045) and biliary leaks (P=0.042) were significantly increased in piggyback. Preoperative serum creatinine levels were the highest in CR-B [1.45±1.17 vs 1.25±0.85 (piggyback) and 1.13±0.60 mg/dL (CR); P=0.033]. Although a worsening of postoperative kidney function was observed among all groups, this was most pronounced in CR-B [creatinine day 14: 1.67±1.40 vs 1.35±0.96 (piggyback) and 1.45±1.03 mg/dL (CR); P=0.102]. Accordingly, the proportion of patients displaying RIFLE stages ≥2 was the highest in CR/CR-B (26%/19%) when compared to piggyback (18%).

 

CONCLUSIONS: Piggyback revealed a shorter warm ischemic time, a reduced blood loss, and a decreased risk of acute kidney failure. Thus, piggyback is a useful technique, which should be applied in standard procedures. When piggyback is unfeasible, cava replacement, which displayed a lower incidence of vascular and biliary complications in our study, remains as a safe alternative.

 

(Hepatobiliary Pancreat Dis Int 2014;13:242-249)

 

KEY WORDS: liver transplantation; anastomosis; surgical procedure

The technique first described for orthotopic liver transplantation consisted of a complete resection of the recipients inferior vena cava (IVC) and interposition of the donor intrahepatic part of the vena cava with two end-to-end anastomoses including the use of a veno-venous bypass for hemodynamic stabilization.^[1] This approach is still performed as a standard in many centers. A modification for cava reconstruction, called the piggyback technique, was later introduced by Tzakis,^[2] which preserved the full length of the recipients cava with subsequent anastomosis of the suprahepatic donor hepatic veins to the ostia of the recipient left and middle hepatic veins. Several modifications eventually lead to the side-to-side cavo-cavostomy, which is referred to as piggyback today.^[3] In this method, the distal and caudal orifices of the donor cava segment are closed and after partial clamping of the recipient inferior cava segment, which still preserves the blood flow from the lower body part to the heart, a side-to-side anatomosis can be made. As first published by Tzakis,^[2] all patients were simultaneously stabilized by using a veno-venous bypass. Although this became basically unnecessary with the latter described modification, some surgeons still perform a temporary portocaval shunt to minimize portal congestion.^[4]

 

Advantages of the piggyback procedure are considered to be the shorter operation time (saving one anastomosis), a shorter anhepatic phase/warm ischemia, a reduction of blood loss and thus better hemodynamic stabilization with a lower incidence of kidney dysfunction. All these aspects have been analyzed previously but only a few publications with small and in general uneven distribution of patients and controversial results are available.^[5-12]

 

In our center, the standard for cava reconstruction was classic replacement for many years. This concept was changed towards piggyback in the beginning of 2006 until the middle of 2007 when cava replacement was reinstalled as our standard because of the impression of increasing complications in the piggyback era.

 

The present study was to compare the outcome and complications of the two techniques (piggyback versus cava replacement) based on our centers' experience, we specifically focused on the influence of each technique on kidney function.

 

 

In our retrospective analysis, 414 adult patients that had received a full-size liver transplantation at our institution between January 2006 and September 2009 were included. Patients with combined liver-kidney transplantation, transplantation in children, living-donor and split liver transplantation were excluded.

 

Of these, 176 (42.5%) patients underwent cava reconstruction using the modified piggyback technique (side to side cavo-cavostomy) as described by Belghiti^[3] without complete occlusion of the IVC and thus, no veno-venous bypass. For that, the vena cava of the hepatic graft was sutured one centimeter above the confluence of the hepatic veins on the back table. In the recipient, a complete dissection of the retrohepatic vena cava was performed, transecting and ligating all the short hepatic veins draining the posterior part of the right liver lobe. Eventually, the three hepatic veins were transected and oversewn. Initially, a vascular clamp was applied laterally on the anterior part of the IVC (with preserved cava blood flow) for a couple of minutes to test the hemodynamic stability. For the use of a veno-venous bypass, preservation and operating time (all in minutes) during transplantation were registered. Hemodynamic instability was defined when mean arterial blood pressure decreased by approximately more than 30% during a trial of clamping of the portal vein and IVC. During this 3 to 5 minutes trial, fluids (colloids, crystalloids) were administered to restore preclamping central venous pressure. The number of perioperatively administered units of transfusions or fresh frozen plasmas (FFP) were included. Postoperative measurements contained the number of units of packed red blood cells (RBC) and FFP administered and the highest postoperative serum creatinine levels on the day immediately after operation and day 7 and 14 post-transplant. The creatinine levels at these time points were compared with the preoperative creatinine levels.

 

In the piggyback operation, trial clamping was tolerated by the patients at all times, and thus in these patients, after partial clamping of the IVC, a longitudinal cavotomy on the donor and recipient vena cava followed by a side-to-side running suture anastomosis was achieved. Arterial, portal venous and biliary reconstructions were performed thereafter as described elsewhere.^[3]

 

In the remaining 238 patients (57.5%), a conventional cava reconstruction^[13] was performed with full replacement of the recipients' cava and therefore two anastomoses. Depending on the surgeons' decision and the extent of hemodynamic instability after intra-operative clamping of the vena cava as described before, a veno-venous bypass (CR-B) was performed in 112 patients (27.1%), and a cava replacement was applied without veno-venous bypass in 126 (30.4%).

 

The patients usually received a T-tube for biliary stenting and decompression. Those who had not received T-tubing were enrolled in a randomized trial to determine its necessity, which had been incidentally conducted within the observation period.

 

Patients' demographics included age, gender, primary diagnosis for liver transplantation and (laboratory) model for end-stage liver disease (MELD) score.

 

Perioperative morbidity was assessed by analyzing the incidence of vascular (stenosis, thrombosis, bleeding), biliary (leaks, stenosis) and infectious (cholangitis, sepsis) complications. Special emphasis was given to the degree of pre- and post-operative kidney function. This was obtained by serum creatinine levels on days 0, 1, 7 and 14, and the requirement of hemodialysis. The incidence of hepatorenal syndrome (HRS), which was defined by criteria described elsewhere, was also registered.^[14] Based on serum creatinine values at different time points, glomerular filtration rate (GFR) was calculated using the 4-parameter-MDRD-formula.^[15] Dynamic outcome of renal dysfunction was further categorized by calculating the changes of serum creatinine levels on days 1, 7 and 14 from baseline (day 0). According to the extent of change, these values were divided into 7 different groups: 1: decrease >1.0 mg/dL; 2: decrease 0.51-1.0 mg/dL; 3: decrease ≤0.5 mg/dL; 4: no change; 5: increase ≤0.5 mg/dL; 6: increase 0.51-1.0 mg/dL; and 7: increase >1.0 mg/dL.

 

Furthermore, to better display the proportion of different degrees of acute kidney deterioration at each time point, the patients were grouped according to the RIFLE criteria for acute kidney injury [stage 0=no change, stage 1 (Risk)=increase in creatinine ×1.5 or GFR decrease >25%, stage 2 (Injury)=increase in creatinine ×2 or GFR decrease >50%, stage 3 (Failure)= increase in creatinine ×3 or creatinine >4 mg/dL or GFR decrease >75%, stages 4 (Loss)/5 (End-stage renal failure)], defined as persistent kidney failure >4 weeks/>3 months, which were summarized within stage 3, since observation period did not exceed 14 days.^[15]

 

Postoperative liver graft function was characterized by the levels of transaminases [alanine aminotransferase (ALT)/aspartate aminotransferase (AST)] and total bilirubin on corresponding time-points (days 0, 1, 7, 14). All grafts were procured from heart-beating, brain dead, and ABO compatible donors with standard procurement techniques. All grafts were flushed and preserved in HTK solution.

 

Specific operative characteristics included anastomosis time (warm ischemic time), preceding cold ischemic time of the graft and number of intraoperative blood (packed cells) and plasma (FFP) units.

 

All numerical data were presented as mean±standard deviation. An analysis of variance (ANOVA) was used to compare quantitative differences and the Chi-square test to compare qualitative ones. If applicable, additional group comparison was performed using a Holm-Sidak post-hoc analysis (Software IBM SPSS Statistics 20 by IBM® Germany). A P value <0.05 was considered statistically significant.

 

 

Patient age was similar in the three groups (P=0.107). There were a higher proportion of male patients in the CR group (P=0.021) and a significant overall difference for the primary diagnoses for liver transplantation (P=0.001), which was more often acute liver failure (8.0%) in piggyback and more often alcoholic cirrhosis in CR (40.5%). There was also a higher proportion of retransplantations (17.0%) in the CR-B group. Also, hepatocellular carcinoma (41.3%) was found (P=0.015) more often in CR (vs 27.7% in CR-B and 26.7% in piggyback). Subsequently, with this uneven distribution of carcinoma, a higher percentage of "standard-except-MELD" patients could be seen in CR as well, thus leading to significant differences in lab-MELD scores [17.3 in CR vs 18.8 in piggyback and 22.5 in CR-B (P=0.008)].

 

Cold ischemia time was not significantly different among the groups (piggyback: 9.4±2.7 h, CR: 10.4±3.1 h, CR-B: 9.3±2.7 h, P=0.074). However, average anastomosis time was significantly shorter for piggyback (piggyback: 40±9 min, CR: 45±11 min, CR-B: 51±12 min, P=0.000). Also, there was a significant lower requirement for intraoperative blood (RBC) and plasma (FFP) replacement in the piggyback group (Table 2).

 

The number of patients with postoperative abdominal bleeding was similar among all three groups and between CR and CR-B groups (14.3% vs 15.2%, P=0.986). However, the incidence of hepatic artery stenosis was significantly increased in the piggyback group (4.0% vs 1.6% in CR and 0.9% in CR-B, P=0.045). Also, biliary leaks were more often in the piggyback group with an incidence of 9.1% (CR: 2.4%, CR-B: 4.5%, P=0.042). The incidence of biliary stenosis was again similar among all three groups (P=0.865).

 

For the rate of infectious complications as either local cholangitis or general sepsis, there was also no difference among the groups.

 

The serum bilirubin and transaminases (ALT/AST) were not significantly different among all three groups in each time point, indicating a similar degree of graft function recovery during the first two weeks (data not shown).

 

As reflected by the higher lab-MELD, preoperative renal function seemed the worst in the CR-B group. The incidence of a hepatorenal syndrome for that group was also significantly higher (29.5%, P=0.006), which was accompanied by a higher necessity for hemodialysis pre-/post-transplantation (15.2%/44.6% vs 7.1%/32.5% in CR and 7.4%/31.3% in piggyback, P=0.035/P=0.530).

 

Pre- and post-operative serum creatinine (day 0, piggyback: 1.25±0.85; CR: 1.13±0.60; CR-B: 1.45±1.17 mg/dL, P=0.033; day 1, piggyback: 1.37±0.79, CR: 1.38±0.54, CR-B: 1.51±1.05 mg/dL, P=0.401; day 7, piggyback: 1.37±0.85, CR: 1.57±0.98, CR-B: 1.57±1.17 mg/dL, P=0.232; day 14, piggyback: 1.35±0.96, CR: 1.45±1.03, CR-B: 1.67±1.40 mg/dL, P=0.102) and calculated GFR, did not differ significantly among the groups (GFR: day 0, piggyback: 75±37; CR: 79±36; CR-B: 71±43 mL/min, P=0.332; day 1, piggyback: 63±29, CR: 58±24, CR-B: 59±32 mL/min, P=0.169; day 7, piggyback: 67±35, CR: 64±41, CR-B: 66±45 mL/min, P=0.675; day 14, piggyback: 72±38, CR: 71±45, CR-B: 68±48 mL/min, P=0.528). However, further categorizing the patients according to the degree of serum creatinine changes from baseline (day 0) showed that there was a higher proportion of patients with postoperative serum creatinine increases of >0.5 mg/dL in both cava replacement groups (day 1: CR 25%, CR-B 26%; day 7: CR 29%, CR-B 28%; day 14: CR 26%, CR-B 31%) compared with the piggyback group (day 1: 10%, day 7: 20%, day 14: 18%). On the other hand, on day 7 post-transplant, there was also the highest proportion of creatinine decreases >0.5 mg/dL in the cava replacement plus the bypass group (CR-B: 31% vs 6% in CR and 11% in piggyback). Another classification according to the RIFLE criteria (Fig.) revealed that before transplantation there were not only most patients with high degrees (stage ≥2) of kidney failure in the CR-B; this was also the group with the highest proportion of normal kidney function (stage 0). However, within the observation period, although all groups experienced a worsening of kidney function, the most severe changes (stage ≥3) were seen in both the CR and CR-B groups at all time-points.

 

This demonstrated that the majority of patients after piggyback reconstruction obviously experienced less pronounced changes of serum creatinine which stayed within the range of ±0.5 mg/dL (day 1: 87%, day 7: 70%, day 14: 68%) compared with CR (day 1-changes±0.5 mg/dL: 79%, day 7: 65%, day 14: 65%) or CR-B (day 1- changes±0.5 mg/dL: 67%, day 7: 50%, day 14: 54%). In almost the same manner, stages reflected that most piggyback patients only developed mild (stage 1=risk) or no (stage 0) acute renal failure (e.g. day 1: 48% compared with CR: 32%, CR-B: 38%).

 

 

The initially described surgical procedure of liver transplantation, which naturally included a complete resection of the recipient vena cava and its replacement with the graft, has been widely replaced in many centers by the so-called piggyback technique.^{[12, 16, 17]} Presumably, the main advantages of this newer method are the preservation of the venous backflow and avoidance of a veno-venous bypass resulting in a shorter operation time due to the avoidance of one anastomosis. Also, resection of the vena cava as in cava replacement might be associated with an increased risk of retroperitoneal hemorrhage especially in retransplantation. Thus, in theory, the preservation of the recipient cava should better stabilize the patient hemodynamically and this could also contribute to the decrease of the incidence of acute kidney failure. However, results of different studies on the impact of cava reconstruction techniques on kidney function are controversial with some authors describing no difference following either cava replacement or piggyback technique,^{[7, 10, 12]} whereas others stated a clear benefit after using the piggyback method.^{[5, 8, 11]} One dilemma of most trials arises from the usually uneven distribution of groups and the non-standardized definition of kidney failure, which makes it difficult to compare the results (Table 4).

 

A further potential advantage of the piggyback technique is that typically a veno-venous bypass can be avoided, which could save time and reduce costs. However, the time saving of omitting a bypass is usually abrogated by the fact that preparation of the recipient cava takes more effort than resection of the retrohepatic vena cava together with the diseased liver. In our series, although none of the patients in the piggyback group required a bypass, a significant proportion of patients with complete cava replacement (126/238, 53%) also appeared hemodynamically stable and could be transplanted without a bypass. The outcome of this group (CR) reflected what has been described in a previous randomized trial of standard orthotopic liver transplantation including cava replacement, where the avoidance of a bypass resulted in a decreased requirement of blood products and a less severe impairment of renal function.^[18]

 

Regarding other transplantation-specific complications, we unexpectedly experienced significantly more cases of arterial stenoses and biliary leaks in the piggyback group. Arterial stenoses might cause a possible hypoperfusion of the graft which may lead to biliary leakage. The actual cause for the increase of arterial problems in our piggyback cohort remains unclear. Both, the techniques for arterial and biliary reconstruction were not different among all groups and thus, any differences seen might have developed by chance.

 

However, another marked difference was the higher incidence of bleeding events from the cava anastomosis in the piggyback group. Since all procedures were performed by experienced surgeons with no predominance for either group, and with no clear other possible parameters to explain this finding, this complication, which was related to the only technical aspect different to the cava replacement technique, could actually be a result of a learning curve.

 

Despite these pitfalls, as described in previous reports^[10] and confirmed by our study, the piggyback technique also displayed advantages. First of all, warm ischemia time, defined as the period where the anastomosis was performed, was significantly shorter and the requirement of RBC and plasma units was lower. This was basically in accordance to Lerut et al who also reported a significantly shorter mean implantation time, a reduced need for intraoperative blood products and a lower rate of reoperation due to intra-abdominal bleeding in an early series of latero-lateral piggyback transplantations without a bypass.^[19] The last aspect, however, was contradicted in our series, where the incidence of postoperative abdominal bleeding episodes was comparable among all groups.

 

In a later report, the advantage of a reduced perioperative blood loss for the piggyback operation could also not be confirmed, which was in this study explained by a higher prevalence of a veno-venous bypass (53%) within the piggyback group.^[7] In general, no veno-venous bypass is necessary when the piggyback technique is used, and only anatomical variations such as the presence of a caudate lobe embracing the vena cava might hinder the use of this technique.^[8]

 

Since in acute or fulminant liver failure, portocaval collateralization is usually insufficient, the chance to avoid a veno-venous bypass in cava replacement is low in this subgroup of patients. Thus, such patients, who were in fact in our series predominantly transplanted with the piggyback technique, may especially benefit hemodynamically from preserving the caval blood flow.^[20]

 

A controversial aspect of side-to-side anastomosis as performed in piggyback, emerges from the possible non-anatomical hemodynamic blood flow. If the distance of cranial part of the donor hepatic veins and the closest proportion of the cranial recipient vena cava are below one centimeter, this might lead to graft outflow obstruction. According to the results of different large series, this technique carries a risk between 1.5% and 8% of intra- or postoperative outflow problems of the graft.^[21-23] This risk can be minimized by increasing experience as shown in a recent large scale series where the incidence of caval outflow obstruction was reduced to 0.5% over time.^[16] Although, this complication seems to be low, it may result in major functional problems of the liver graft as reported by Cescon et al who experienced outflow problems in 4.6% of his patients, of whom 40% required a retransplantation and it was the cause of death in 23%.^[24] In our series, we also experienced three cases (1.7%) of venous outflow problems most likely due to a kinking of the hepatic veins. One of these cases required a reoperation with a patch plasty, whereas the remaining two regained normal liver function over time.

 

In total, these were more caval problems than we experienced with the classical technique.

 

With many other confounding factors, evaluating the influence of different cava reconstruction techniques on kidney function is a difficult task. Although pretransplant kidney function obtained by calculated GFR (MDRD) revealed no difference, looking further into details, we found the highest incidence of hepatorenal syndrome in those patients who later received a cava replacement using a veno-venous bypass (CR-B) and the lowest in cases of cava replacement with no bypass (CR). Moreover, postoperative changes of serum creatinine seemed to be more severe into both directions, up and down, in both cava replacement groups, whereas changes of creatinine in the piggyback group stayed within the smaller range of ?±0.5 mg/dL in a larger proportion. From this, and the results from categorizing patients according to the RIFLE criteria, which basically confirmed a stronger impact on kidney function under cava replacement with or without bypass (Fig.), we presume that complete clamping of the vena cava may in fact increase the risk for acute kidney failure in some cases. Moreover, since differences between CR and CR-B were less severe, the absence of a veno-venous bypass (after successful trial clamping of the IVC) must not have additional impact on the degree of kidney dysfunction. However again, since the use of a veno-venous bypass was not performed randomly, and patients requiring it, displayed with a slightly worse kidney function before transplantation, this interpretation must be taken cautiously.

 

The limitation of our study is the retrospective feature and the non-randomized use of either technique. This resulted amongst others in a significantly inhomogeneous distribution of kidney dysfunction before transplantation. Thus, further large scale, prospective and randomized trials are warranted to better resolve this issue.

 

In conclusion, the results of this study showed that both techniques displayed different aspects in perioperative morbidity. With the only method that may cause venous outflow problems and which displayed, at least in our study, a higher incidence of arterial and biliary problems, piggyback technique also revealed a shorter anhepatic phase and warm ischemic time, as well as a significantly reduced blood loss. Moreover, partial clamping of the vena cava, as performed in piggyback, may decrease the risk of acute kidney failure. Thus, piggyback, which allows for a simple anastomosis and avoidance of retroperitoneal dissection, is a useful valuable technique, which is not only suitable for retransplantation but can be applied in standard transplant procedures. Cava replacement, which displayed a lower incidence of vascular and biliary complications in our study, also constitutes a safe method that can be considered alternatively.

 

 

1 Starzl TE, Groth CG, Brettschneider L, Penn I, Fulginiti VA, Moon JB, et al. Orthotopic homotransplantation of the human liver. Ann Surg 1968;168:392-415. PMID: 4877589

2 Tzakis A, Todo S, Starzl TE. Orthotopic liver transplantation with preservation of the inferior vena cava. Ann Surg 1989; 210:649-652. PMID: 2818033

3 Belghiti J, Panis Y, Sauvanet A, Gayet B, Fékété F. A new technique of side to side caval anastomosis during orthotopic hepatic transplantation without inferior vena caval occlusion. Surg Gynecol Obstet 1992;175:270-272. PMID: 1514163

4 Tzakis AG, Reyes J, Nour B, Marino IR, Todo S, Starzl TE. Temporary end to side portacaval shunt in orthotopic hepatic transplantation in humans. Surg Gynecol Obstet 1993;176: 180-182. PMID: 8421808

5 Cabezuelo JB, Ramirez P, Acosta F, Torres D, Sansano T, Pons JA, et al. Does the standard vs piggyback surgical technique affect the development of early acute renal failure after orthotopic liver transplantation? Transplant Proc 2003;35:1913-1914. PMID: 12962846

6 Cherqui D, Lauzet JY, Rotman N, Duvoux C, Dhumeaux D, Julien M, et al. Orthotopic liver transplantation with preservation of the caval and portal flows. Technique and results in 62 cases. Transplantation 1994;58:793-796. PMID: 7940712

7 Hesse UJ, Berrevoet F, Troisi R, Pattyn P, Mortier E, Decruyenaere J, et al. Hepato-venous reconstruction in orthotopic liver transplantation with preservation of the recipients' inferior vena cava and veno-venous bypass. Langenbecks Arch Surg 2000;385:350-356. PMID: 11026707

8 Jovine E, Mazziotti A, Grazi GL, Ercolani G, Masetti M, Morganti M, et al. Piggy-back versus conventional technique in liver transplantation: report of a randomized trial. Transpl Int 1997;10:109-112. PMID: 9089994

9 Mehrabi A, Mood ZA, Fonouni H, Kashfi A, Hillebrand N, Müller SA, et al. A single-center experience of 500 liver transplants using the modified piggyback technique by Belghiti. Liver Transpl 2009;15:466-474. PMID: 19399735

10 Miyamoto S, Polak WG, Geuken E, Peeters PM, de Jong KP, Porte RJ, et al. Liver transplantation with preservation of the inferior vena cava. A comparison of conventional and piggyback techniques in adults. Clin Transplant 2004;18:686-693. PMID: 15516245

11 Nikeghbalian S, Dehghani M, Salahi H, Bahador A, Kazemi K, Kakaei F, et al. Effects of surgical technique on postoperative renal function after orthotopic liver transplant. Exp Clin Transplant 2009;7:25-27. PMID: 19364308

12 Nishida S, Nakamura N, Vaidya A, Levi DM, Kato T, Nery JR, et al. Piggyback technique in adult orthotopic liver transplantation: an analysis of 1067 liver transplants at a single center. HPB (Oxford) 2006;8:182-188. PMID: 18333273

13 Neuhaus P, Platz KP. Liver transplantation: newer surgical approaches. Baillieres Clin Gastroenterol 1994;8:481-493. PMID: 8000095

14 Arroyo V, Ginès P, Gerbes AL, Dudley FJ, Gentilini P, Laffi G, et al. Definition and diagnostic criteria of refractory ascites and hepatorenal syndrome in cirrhosis. International Ascites Club. Hepatology 1996;23:164-176. PMID: 8550036

15 Bellomo R, Ronco C, Kellum JA, Mehta RL, Palevsky P; Acute Dialysis Quality Initiative workgroup. Acute renal failure: definitions, outcome measures, animal models, fluid therapy and information technology need: the Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit Care 2004;8:R204-212.

16 Levi DM, Pararas N, Tzakis AG, Nishida S, Tryphonopoulos P, Gonzalez-Pinto I, et al. Liver transplantation with preservation of the inferior vena cava: lessons learned through 2000 cases. J Am Coll Surg 2012;214:691-699. PMID: 22364695

17 Stieber AC. One surgeon's experience with the piggyback versus the standard technique in orthotopic liver transplantation: is one better than the other? Hepatogastroenterology 1995;42:403-405. PMID: 8586377

18 Grande L, Rimola A, Cugat E, Alvarez L, García-Valdecasas JC, Taurá P, et al. Effect of venovenous bypass on perioperative renal function in liver transplantation: results of a randomized, controlled trial. Hepatology 1996;23:1418-1428. PMID: 8675159

19 Lerut JP, Molle G, Donataccio M, De Kock M, Ciccarelli O, Laterre PF, et al. Cavocaval liver transplantation without venovenous bypass and without temporary portocaval shunting: the ideal technique for adult liver grafting? Transpl Int 1997;10:171-179. PMID: 9163855

20 Belghiti J, Noun R, Sauvanet A, Durand F, Aschehoug J, Erlinger S, et al. Transplantation for fulminant and subfulminant hepatic failure with preservation of portal and caval flow. Br J Surg 1995;82:986-989. PMID: 7648127

21 Navarro F, Le Moine MC, Fabre JM, Belghiti J, Cherqui D, Adam R, et al. Specific vascular complications of orthotopic liver transplantation with preservation of the retrohepatic vena cava: review of 1361 cases. Transplantation 1999;68:646-650. PMID: 10507483

22 Nemes B, Kóbori L, Fehérvári I, Fazakas J, Gerlei Z, Ther G, et al. Comparison of the results of conventional, crossclamp and piggyback technique in liver transplantation. Magy Seb 2005;58:155-161. PMID: 16167468

23 Parrilla P, Sánchez-Bueno F, Figueras J, Jaurrieta E, Mir J, Margarit C, et al. Analysis of the complications of the piggy-back technique in 1112 liver transplants. Transplant Proc 1999;31:2388-2389. PMID: 10500633

24 Cescon M, Grazi GL, Varotti G, Ravaioli M, Ercolani G, Gardini A, et al. Venous outflow reconstructions with the piggyback technique in liver transplantation: a single-center experience of 431 cases. Transpl Int 2005;18:318-325. PMID: 15730493