the role of color doppler ultrasound in living donor liver ... · liver transplantation (lt) is now...

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177 ©Elsevier & CTSUM. All rights reserved. J Med Ultrasound 2008 Vol 16 No 3 Introduction Liver transplantation (LT) is now a well accepted therapy for end-stage liver disease. Due to a short- age of cadaveric donors, advances in modern hep- atectomy techniques have resulted in the success of living donor liver transplantation (LDLT) as a routine procedure for end-stage liver disease. LDLT has also become the major source of livers for transplantation, especially in Asia. However, the threat of vascular complications is still a problem and the major cause of graft failure. If a liver graft fails, it is almost impossible for a patient to receive a second graft in Taiwan; thus, it is necessary to eliminate the possibility of graft failure. Many im- aging modalities and interventional procedures are involved in the diagnosis and management of these problems. Color Doppler ultrasound (CDUS) is performed to ensure perfect vascular reconstruction after he- patic reperfusion. For the immediate assessment of general condition and early detection of vascular complications, CDUS is becoming essential and is the modality of choice to evaluate hepatic hemo- dynamics. Thus, CDUS is an important modality which is widely used in all types of LT and is per- formed in the preoperative, intraoperative and postoperative periods for routine evaluation of vas- culature. Timely recognition of any threat of vascular complications improves the success of LDLT [1–4]. This article will review the current applications of CDUS in LDLT. R E V I E W A R T I C L E The Role of Color Doppler Ultrasound in Living Donor Liver Transplantation Tung-Liang Huang* Color Doppler ultrasound (CDUS) is performed to ensure perfect vascular reconstruction after hepatic reperfusion. For the immediate assessment of general condition and early detection of vascular complications, CDUS is becoming essential and is the modality of choice to evaluate hepatic hemodynamics. Thus, CDUS is an important modality, which is widely used in all types of liver transplantation, and is performed in the preoperative, intraoperative and postoperative periods for routine evaluation of vasculature. Timely recog- nition of any threat of vascular complications improves the success of living donor liver transplantation. This article will review the current applications of CDUS in living donor liver transplantation. KEY WORDS — color Doppler ultrasound, living donor liver transplantation J Med Ultrasound 2008;16(3):177–187 Received: August 2, 2008 Accepted: August 25, 2008 Department of Diagnostic Radiology and Liver Transplant Program, Chang Gung University and Memorial Hospital, Kaohsiung Medical Center, Taiwan. *Address correspondence to: Dr. Tung-Liang Huang, Department of Diagnostic Radiology and Liver Transplant Program, Chang Gung University and Memorial Hospital, Kaohsiung Medical Center, 123 Ta-Pei Road, Niao-Sung Hsiang, Kaohsiung Hsien 833, Taiwan. E-mail: [email protected]

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Page 1: The Role of Color Doppler Ultrasound in Living Donor Liver ... · Liver transplantation (LT) is now a well accepted therapy for end-stage liver disease. Due to a short-age of cadaveric

177©Elsevier & CTSUM. All rights reserved. J Med Ultrasound 2008 • Vol 16 • No 3

Introduction

Liver transplantation (LT) is now a well acceptedtherapy for end-stage liver disease. Due to a short-age of cadaveric donors, advances in modern hep-atectomy techniques have resulted in the successof living donor liver transplantation (LDLT) as aroutine procedure for end-stage liver disease. LDLThas also become the major source of livers fortransplantation, especially in Asia. However, thethreat of vascular complications is still a problemand the major cause of graft failure. If a liver graftfails, it is almost impossible for a patient to receivea second graft in Taiwan; thus, it is necessary toeliminate the possibility of graft failure. Many im-aging modalities and interventional procedures

are involved in the diagnosis and management ofthese problems.

Color Doppler ultrasound (CDUS) is performedto ensure perfect vascular reconstruction after he-patic reperfusion. For the immediate assessment ofgeneral condition and early detection of vascularcomplications, CDUS is becoming essential and isthe modality of choice to evaluate hepatic hemo-dynamics. Thus, CDUS is an important modalitywhich is widely used in all types of LT and is per-formed in the preoperative, intraoperative andpostoperative periods for routine evaluation of vas-culature. Timely recognition of any threat of vascularcomplications improves the success of LDLT [1–4].This article will review the current applications ofCDUS in LDLT.

R E V I E W

A R T I C L E

The Role of Color Doppler Ultrasound inLiving Donor Liver Transplantation

Tung-Liang Huang*

Color Doppler ultrasound (CDUS) is performed to ensure perfect vascular reconstructionafter hepatic reperfusion. For the immediate assessment of general condition and earlydetection of vascular complications, CDUS is becoming essential and is the modality ofchoice to evaluate hepatic hemodynamics. Thus, CDUS is an important modality, whichis widely used in all types of liver transplantation, and is performed in the preoperative,intraoperative and postoperative periods for routine evaluation of vasculature. Timely recog-nition of any threat of vascular complications improves the success of living donor livertransplantation. This article will review the current applications of CDUS in living donorliver transplantation.

KEY WORDS — color Doppler ultrasound, living donor liver transplantation

■ J Med Ultrasound 2008;16(3):177–187 ■

Received: August 2, 2008 Accepted: August 25, 2008Department of Diagnostic Radiology and Liver Transplant Program, Chang Gung University and MemorialHospital, Kaohsiung Medical Center, Taiwan.

*Address correspondence to: Dr. Tung-Liang Huang, Department of Diagnostic Radiology and Liver TransplantProgram, Chang Gung University and Memorial Hospital, Kaohsiung Medical Center, 123 Ta-Pei Road,Niao-Sung Hsiang, Kaohsiung Hsien 833, Taiwan. E-mail: [email protected]

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The Principles and Methods forInstrumental Hepatic VascularMeasurements

The CDUS instruments used are Acuson Aspen andSequoia scanners (Acuson, Mountain View, CA,USA; the machines used in most transplant centersand published papers), which have a phased arrayof 3.5, 4.0, 5.0 or 7.0 MHz scanners in the imagingand Doppler mode, respectively. Measurements ofblood flow by Doppler ultrasound include qualita-tive evaluations such as determination of the pres-ence of flow, direction of color signal flow, and anyabnormal flow indicating vascular insufficiency orstenosis. The quantitative evaluations performedinclude the measurement of flow velocity, flow vol-ume and calculation of flow index. The width ofthe sample volume for pulsed Doppler flowmetry,which ranges from 1 to 5 mm, is dependent on thediameter of the detected vessels. The pulse repeti-tion frequency which ranges from 3.0 to 9.0 kHzand is selected to obtain adequate Doppler spec-tral waveforms of the targeted blood vessels with-out aliasing. CDUS examinations are performed forhemodynamic evaluation of the portal vein (PV),hepatic vein (HV) and hepatic artery (HA) in the

pretransplantation, intraoperative and postoperativeperiods, respectively.

Pretransplantation studyIn the pretransplantation study of the native liver ofthe recipient, the measurement of PV flow is ob-tained at the extrahepatic portion of the main PVnear the bifurcation. The size and flow direction ofthe PV are recorded. Any abnormal intraluminalportal thrombus or flow occlusion should be ruledout. The flow of the HA is recorded along with wave-form, peak systolic velocity (PSV), resistance index(RI [RI = PSV − EDV/PSV, where EDV = end-diastolicvelocity]) and pulsatility index (PI [PI = PSV − EDV/Vm, where Vm = mean velocity]), obtained at thehepatic hilum for quantitative evaluation. The ab-sence of HA flow in the liver may be related toarterial occlusion (Fig. 1).

Intraoperative studyIn the intraoperative study of the liver graft, themeasurements of HV, PV and HA are performed bothjust after graft reperfusion and abdomen closure.All the PV measurements are obtained at the intra-hepatic and extrahepatic portion over and alongthe anastomosis. The size, flow direction and veloc-ity of the PV are recorded. The angle-correctedflow velocity and cross-sectional area of the PV atthe same site should also be recorded. The samplevolume size for the Doppler ultrasound mode is setat 3–5 mm, about half the diameter of the meas-ured PV. The PV mean velocity should be correctedby the angle between the long axis of the PV andthe Doppler beam of less than 60°. The portal flowvolume per body weight is also calculated by thePV sectional area and mean velocity using the formula: portal vein flow volume (PVFV) = A × Vm,where A = sectional area (Fig. 2). The measure-ments of the HA flow including waveform, PSV, RIand PI are performed at the intrahepatic portion ofthe liver graft. The PSV of the HA is detected withsuitable gate and angle correction along the longaxis of the color-coded HA. The angle between thelong axis of the color-coded HA and the Dopplerbeam should be less than 60°. The Doppler sample

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Fig. 1. Standard model of scanning by color Doppler ultra-sound showed hepatic artery flow and measurement of param-eters with angle correction and scale without aliasing. For thiscase, the formula and calculations were as follows: PSV =124 cm/s; PI= (PSV−EDV)/Vm= (124−39)/71=1.21; RI=PSV − EDV/PSV. PI = pulsatility index; RI = resistance index;EDV = end-diastolic velocity; Vm = mean of flow velocity.

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volume is set at 1–2 mm and the waveforms aremade on the lowest possible frequency shift rangewithout aliasing. The flow measurements of theHVs are performed at each anastomotic vein at theintrahepatic portion about 1–2 cm from the infe-rior vena cava. The detected velocities are taken atpeak waveform and angle correction is done underless than 60°. The waveform patterns of the HVsare classified as monophasic, biphasic or triphasic,reflecting the cardiac oscillation from the pressurechange of the right atrium (Fig. 3).

Postoperative studyIn the postoperative study, CDUS examinations areperformed once a day during the first week aftersurgery. The protocol for both qualitative andquantitative hemodynamic evaluations follow theprevious general principles for PV, HV and HA,respectively. The first postoperative CDUS examina-tion is best performed within 12 hours after surgery.After 7 postoperative days, the schedule for CDUSis once per week before discharge or based onneed according to clinical condition.

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Fig. 3. Standard model of scanning by color Doppler ultra-sound showed hepatic vein flow and measurement of parame-ters with angle correction and scale without aliasing. For thesecases, the waveform analysis and calculations were as follows:there are normal triphasic waveform and biphasic waveform in the case of (A) and (B), the peak of flow velocity (Vp) are 59 and 61 cm/s, respectively; otherwise, there is an abnor-mal monophasic waveform in the case of (C) and relatively low Vp.

Fig. 2. Standard model of scanning by color Doppler ultra-sound showed portal vein flow and measurement of parame-ters with angle correction and scale without aliasing. For thiscase, the formula and calculations were as follows: portal veinflow volume (PVFV) = mean of flow velocity (Vm) × cross-section area (A) = 39 × 60 × π × (0.78/2)2 = 1,118 mL/min;further calculation of PVFV in per 100 g graft weight is172 mL/min/100 g.

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The CDUS Study for PretransplantRecipients on the Waiting List

Since the initiation of LDLT in Kaohsiung in 1994,we have evaluated many infants and young childrenwith biliary atresia awaiting LT, and have found ahigh incidence of vascular anomalies in these pa-tients. The incidence of associated vascular anom-alies was found to be up to 42% (16/38 cases).These vascular anomalies included: absence or hy-poplasia of the inferior vena cava (n = 3), congeni-tal absence or hypoplasia of the PV (n = 8), andanomalous origin of the HA (n = 6) [2,3,5].

In the preoperative study, we also found a groupof pediatric recipients with high HA RI (some withan RI > 1.0) and frequent admissions because offever and sepsis. According to the survival analysisfor all relevant risk factors, high HA RI (> 1.0) andlow portal flow velocity (< 10 cm/s) had definitesignificance for mortality [6] (Fig. 4). These casescould no longer wait and required transplantationfor life-saving reasons. For the preoperative evalua-tion of PV quality, a smooth portal wall and patentflow are essential. In our research report of a groupwith portal insults, portal occlusion or absence is acontraindication to LDLT, and low portal flow lessthan 7 cm/s and small portal size less than 4 mmare risk factors for intraoperative portal thrombosis[7]. With advances in surgical techniques, somecases of intraportal partial thrombosis have been

overcome using venous grafts, and successfulLDLT has been achieved in recent years by somecenters. PV thrombosis is not a contraindication toLDLT, but the limit of thrombosis must not be

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Fig. 4. For this case of a young child on the waiting list for livertransplantation, the HA impedance was detected with anresistance index of 1.20 (exceeding 1.0). This case has a highrisk of mortality, and an early transplantation is a priority tosave this patient’s life.

Fig. 5. These cases were evaluated in a pretransplant studyand showed abnormal portal flow by color Doppler ultrasound:(A) the first case had portal vein (PV) occlusion with obscuredPV tract and no portal flow signal; (B) the second had a smallPV tract and slow low inflow (3 cm/s); (C) the third hadreverse hepatofugal portal flow and pulsatile waveform due toan arterioportal shunt. These abnormal portal flows are signif-icant and may be a contraindication to living donor liver trans-plantation or are a risk for post-transplant portal thrombosis.

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beyond the main PV [8] (Fig. 5). All these predis-posing vascular anomalies may be significant inthe decision to transplant and are well detected byCDUS. Therefore, in deciding on the priority of pa-tients waiting for early transplantation, CDUS playsa really important role in pretransplant assessment.

The Major Vascular ComplicationsDetected by Intraoperative CDUS

HA thrombosis and insufficiencyHA thrombosis (HAT) is the most serious vascularcomplication in LT and results in hepatic necrosis,dysfunction and failure. The incidence of HAT in LTvaries from 7.4–13% and is higher in adult LDLT [9].The advancement of HA anastomosis using micro-surgical techniques has improved the success rateof HA reconstruction. The diagnosis of HAT by

CDUS just after reperfusion of the graft is reliable.The diagnostic criterion of HAT is the absence ofDoppler signals, and in this situation, redo of HAanastomosis or thrombectomy for resuscitation mustbe undertaken immediately. If an abnormal flowpattern with dampened systolic peak and slow peakvelocity (< 30 cm/s) occurs, HA angulation, stran-gulation or spasm is usually the cause of HA insuf-ficiency [4]. Rapid thrombosis formation in thesecases is possible. CDUS can help to assess and con-firm the optimal flow change after the problem isresolved. The peak systolic Doppler velocity (PSV)and waveform distal to the HA stenosis are alsodampened, the PI and RI of the HA also fall owingto poststenotic reactive vasodilatation and distal im-pedance [10,11]. Under this condition, a low HAPSV due to a proportional increase in end-diastolicflow velocity is observed (Fig. 6). If the parametersof HA flow detected are distal to the anastomosis,

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Fig. 6. This case was evaluated during intraoperative color Doppler ultrasound (CDUS) after vascular reperfusion. (A) A damp-ened hepatic artery (HA) peak wave, such as tardus-parvus waveform due to partial thrombosis, was found. (B) Reopen forthrombectomy was done with a slight improvement in flow, but optimal flow was not noted. (C, D) Thus, redo of HA anastomosiswas done and normal HA flow was regained as noted on CDUS check-up.

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any dampened flow waveform and velocity will in-dicate the presence of anastomotic stenotic changein the proximal HA [12]. Intraoperative CDUS iseasy to perform and provides the opportunity forimmediate treatment of such inadequate arterialreconstructions. CDUS also plays an important rolein reducing the incidence of HAT following LDLT[13,14].

PV thrombosis, insufficiency andhyperperfusionIf there are no Doppler flow signals in the recon-structed PV, thrombosis of the PV is highly sus-pected. However, poor PV flow signals with CDUScan be caused by acute angulation of the soundscanning beam to the axis of the portal tract (> 60°)or the obliteration of extrahepatic PV with interven-ing adipose tissue or bowel gas after surgery [10,11].Thus, we should carefully exclude PV thrombosisby CDUS. Immediate thrombectomy is the goldstandard for treatment of PV thrombosis. Inadequatelow PV inflow (mean velocity < 12 cm/s) as PV insuf-ficiency is usually detected in pediatric recipientsowing to persistent large portosystemic collateralssuch as the coronary vein, splenorenal shunt andgastrorenal shunt, sometimes owing to HV outflowobstruction or low cardiac output (Fig. 7). Anincrease in PV inflow can be achieved by ligation of portosystemic collaterals, relief of HV outflowobstruction or redo of PV anastomosis [13,15].

On the contrary, PV hyperperfusion may occur withextremely high PVFV above 250 mL/min/100 g inadult LDLT recipients. These patients will developpost-transplant hepatic dysfunction such as small-for-size syndrome, which is often found amongthose with a relatively small-for-size graft (graft-to-recipient weight ratio < 0.8) (Fig. 8). Portal hyper-perfusion in small-for-size graft is thought to bethe main cause of small-for-size syndrome by portalhypertension and damage to sinusoids and hepa-tocytes [16,17]. To overcome this problem, severaltherapeutic options have also been reported, suchas surgical modulation of splenic arterial ligation orsplenectomy to release portal hyperperfusion andliver tissue congestion [18–20] (Fig. 8). For detec-tion of this disorder, CDUS is the most importantmodality for monitoring portal hemodynamics.

HV outflow obstruction, HV thrombosis, HV stenosisNormal flow velocity and waveforms of HV shouldbe more than 12 cm/s at the peak of biphasic ortriphasic waveforms, which reflect the patency ofhepatic outflow. Hepatic outflow obstruction afterreperfusion will result in a hard consistency and darkdiscoloration of the graft noted by the surgeonduring the operation. CDUS examination is usedimmediately for evaluation. The characteristic CDUSfindings are: (1) mild dilatation of the HVs; (2) flator monophasic HV flow waveform; (3) slow HV

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Fig. 7. (A, B) Intraoperative color Doppler ultrasound detection of portal vein thrombosis in two cases with no signal flow and a marked decrease in hepatic artery resistance index (< 0.5) due to buffer mechanism.

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peak velocity (< 10 cm/s); and (4) extremely low PVflow velocity (< 14 cm/s) [9,21]. Intrahepatic venousthrombus is usually observed in HV thrombosis andimmediate thrombectomy is needed. During trans-plant surgery, torsion of the graft was described by

Broelsch et al [22]. In our experience, right rotationof the graft in the wide abdominal space may resultin outflow stenosis and a flat HV flow waveform(Fig. 9). We can prevent such outflow obstructionby fixing and stabilizing the graft in the optimal

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Fig. 8. (A) This case of low graft-to-recipient weight ratio of 0.8 such as small-for-size graft, and extremely high portal vein flowvolume (PVFV) up to 682 mL/min/100 g was detected by color Doppler ultrasound just after hepatic flow reperfusion. A high possibility of post-transplant dysfunction or graft failure exists in this case. (B) Immediate ligation of the splenic artery was carriedout for modulation of portal hyperperfusion, and the PVFV was dramatically reduced to 233 mL/min/100 g, which was withinnormal limits. The postoperative course of this patient was uneventful.

Fig. 9. Case of a young child with right rotation of the graft in thewide abdomen during operation. (A) Hepatic vein (HV) outflow wasimpeded with a flat waveform and low peak velocity detected by intra-operative color Doppler ultrasound (CDUS). (B, C) For improvementof HV outflow obstruction, left-side fixation for a stable graft positionand posthepatic balloon interposition to correct HV angulation werecarried out until optimal HV flow was regained under CDUS guidance.

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position under the guidance of intraoperative CDUS,until a normal biphasic HV waveform is obtained[1,11].

The Postoperative VascularComplications Detected by CDUS

Postoperative HATPostoperative HAT usually occurs in the first post-operative day but can occur up to 1 week after surgery. We perform routine CDUS examinationson the first postoperative day, especially within 12 hours of surgery and in patients with high risk

factors or with poor arterial quality. HAT is presentin Doppler findings when absent arterial signals arefound in the whole graft scan or when only damp-ened slow HA flow is noted. Further imaging withCT angiography is suggested for confirmation. HATis usually successfully treated by thrombectomy orredo of anastomosis or jump graft following earlydiagnosis [23–25].

Postoperative PV thrombosis or PV stenosisPostoperative PV thrombosis may also occur in theearly postoperative period. CDUS shows slow orabsent portal flow or direct visualization of throm-bus. Sometimes, hepatofugal PV flow is noted and

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Fig. 10. Case of post-transplant pleural effusion and ascites was diagnosed as portal vein stenosis by color Doppler ultrasound. (A, B) Local segmental stenosis and high-flow velocity were noted at the anastomotic site. (C, D) Normal mean of flow velocity was regained after percutaneous transhepatic angioplasty with balloon dilatation.

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may be associated with HV outflow obstruction[10,12,26]. Surgical thrombectomy, redo of anas-tomosis or infusion of a thrombolytic agent is usedin the management of this disorder. PostoperativePV stenosis may develop and cause hepatic dys-function with intractable ascites. CDUS examinationshows marked turbulent flow or slow flow and ex-tremely high-flow velocity (may be up to 200 cm/s)detected at the narrowed anastomosis. Furthermanagement with percutaneous transhepatic por-tal angioplasty with balloon dilatation or Wallstentinterposition is suggested [15,27] (Fig. 10).

Postoperative HV thrombosis or HV stenosisHV outflow obstruction may also develop aftertransplantation, the obstruction usually occurs at theanastomotic site and is mainly caused by chronicfibrosis at the stenotic site and hypertrophy of thegraft [28,29]. CDUS detection shows a flat flowwaveform and slow HV flow velocity (< 10 cm/s);hepatofugal PV flow may occur in severe obstruc-tion. Therapeutic procedures of angioplasty withballoon dilatation or Wallstent interposition are sug-gested for this disorder [30] (Fig. 11). CDUS is used

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Fig. 11. A case of persistent intractable massive ascites (> 2,000 mL/day) at postoperative color Doppler ultrasound examination.(A) Low hepatic vein (HV) peak velocity (Vp) with a flat waveform favored hepatic vein stenosis. (B, C) After percutaneous trans-luminal venoplasty with balloon dilatation and insertion of a Wallstent, (D) the HV waveform improved to a normal multiphasicpattern and Vp increased to 72 cm/s. Following this treatment, the ascites dramatically subsided.

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before and after angioplasty or stenting for effec-tive treatment with successful regain of normal HVoutflow [31,32].

Conclusion

CDUS has wide use in LT and is the modality ofchoice in the evaluation of hepatic graft hemody-namics and the diagnosis of vascular complications.This modality has a very important role in preoper-ative, intraoperative and postoperative evaluationsfor the immediate assessment of general conditionand early detection of complications. Timely re-cognition of any complications could improve thesuccess of LT.

Chang Gung Memorial Hospital was the firstcenter to perform LT in Taiwan and carried out asuccessful case of orthotopic liver transplantationin 1984, and was the first to start a program of LT.Due to the scarcity of source- and size-matched graftdonors for infants and young children, we werethe first to initiate cadaveric split-liver transplanta-tion and LDLT, respectively. CDUS is now performedroutinely for the evaluation of hepatic hemodynam-ics. Although high rates of vascular complicationsresulting in graft failure are still reported by manycenters worldwide, our center has had good results.

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