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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):177187

Introduction are involved in the diagnosis and management of


these problems.
Liver transplantation (LT) is now a well accepted Color Doppler ultrasound (CDUS) is performed
therapy for end-stage liver disease. Due to a short- to ensure perfect vascular reconstruction after he-
age of cadaveric donors, advances in modern hep- patic reperfusion. For the immediate assessment of
atectomy techniques have resulted in the success general condition and early detection of vascular
of living donor liver transplantation (LDLT) as a complications, CDUS is becoming essential and is
routine procedure for end-stage liver disease. LDLT the modality of choice to evaluate hepatic hemo-
has also become the major source of livers for dynamics. Thus, CDUS is an important modality
transplantation, especially in Asia. However, the which is widely used in all types of LT and is per-
threat of vascular complications is still a problem formed in the preoperative, intraoperative and
and the major cause of graft failure. If a liver graft postoperative periods for routine evaluation of vas-
fails, it is almost impossible for a patient to receive culature. Timely recognition of any threat of vascular
a second graft in Taiwan; thus, it is necessary to complications improves the success of LDLT [14].
eliminate the possibility of graft failure. Many im- This article will review the current applications of
aging modalities and interventional procedures CDUS in LDLT.

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: tlhuang@adm.cgmh.org.tw

Elsevier & CTSUM. All rights reserved. J Med Ultrasound 2008 Vol 16 No 3 177
T.L. Huang

The Principles and Methods for pretransplantation, intraoperative and postoperative


Instrumental Hepatic Vascular periods, respectively.
Measurements
Pretransplantation study
The CDUS instruments used are Acuson Aspen and In the pretransplantation study of the native liver of
Sequoia scanners (Acuson, Mountain View, CA, the recipient, the measurement of PV flow is ob-
USA; the machines used in most transplant centers tained at the extrahepatic portion of the main PV
and published papers), which have a phased array near the bifurcation. The size and flow direction of
of 3.5, 4.0, 5.0 or 7.0 MHz scanners in the imaging the PV are recorded. Any abnormal intraluminal
and Doppler mode, respectively. Measurements of portal thrombus or flow occlusion should be ruled
blood flow by Doppler ultrasound include qualita- out. The flow of the HA is recorded along with wave-
tive evaluations such as determination of the pres- form, peak systolic velocity (PSV), resistance index
ence of flow, direction of color signal flow, and any (RI [RI = PSV EDV/PSV, where EDV = end-diastolic
abnormal flow indicating vascular insufficiency or velocity]) and pulsatility index (PI [PI = PSV EDV/
stenosis. The quantitative evaluations performed Vm, where Vm = mean velocity]), obtained at the
include the measurement of flow velocity, flow vol- hepatic hilum for quantitative evaluation. The ab-
ume and calculation of flow index. The width of sence of HA flow in the liver may be related to
the sample volume for pulsed Doppler flowmetry, arterial occlusion (Fig. 1).
which ranges from 1 to 5 mm, is dependent on the
diameter of the detected vessels. The pulse repeti- Intraoperative study
tion frequency which ranges from 3.0 to 9.0 kHz In the intraoperative study of the liver graft, the
and is selected to obtain adequate Doppler spec- measurements of HV, PV and HA are performed both
tral waveforms of the targeted blood vessels with- just after graft reperfusion and abdomen closure.
out aliasing. CDUS examinations are performed for All the PV measurements are obtained at the intra-
hemodynamic evaluation of the portal vein (PV), hepatic and extrahepatic portion over and along
hepatic vein (HV) and hepatic artery (HA) in the the anastomosis. The size, flow direction and veloc-
ity of the PV are recorded. The angle-corrected
flow velocity and cross-sectional area of the PV at
the same site should also be recorded. The sample
volume size for the Doppler ultrasound mode is set
at 35 mm, about half the diameter of the meas-
ured PV. The PV mean velocity should be corrected
by the angle between the long axis of the PV and
the Doppler beam of less than 60. The portal flow
volume per body weight is also calculated by the
PV 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, RI
Fig. 1. Standard model of scanning by color Doppler ultra- and PI are performed at the intrahepatic portion of
sound showed hepatic artery flow and measurement of param- the liver graft. The PSV of the HA is detected with
eters with angle correction and scale without aliasing. For this
suitable gate and angle correction along the long
case, the formula and calculations were as follows: PSV =
124 cm/s; PI = (PSV EDV)/Vm = (124 39)/71 = 1.21; RI = axis of the color-coded HA. The angle between the
PSV EDV/PSV. PI = pulsatility index; RI = resistance index; long axis of the color-coded HA and the Doppler
EDV = end-diastolic velocity; Vm = mean of flow velocity. beam should be less than 60. The Doppler sample

178 J Med Ultrasound 2008 Vol 16 No 3


CDUS in LDLT

B
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 this
case, the formula and calculations were as follows: portal vein
flow volume (PVFV) = mean of flow velocity (Vm) cross-
section area (A) = 39 60 (0.78/2)2 = 1,118 mL/min;
further calculation of PVFV in per 100 g graft weight is
172 mL/min/100 g.

volume is set at 12 mm and the waveforms are


made on the lowest possible frequency shift range
without aliasing. The flow measurements of the
HVs are performed at each anastomotic vein at the C
intrahepatic portion about 12 cm from the infe-
rior vena cava. The detected velocities are taken at
peak waveform and angle correction is done under
less than 60. The waveform patterns of the HVs
are classified as monophasic, biphasic or triphasic,
reflecting the cardiac oscillation from the pressure
change of the right atrium (Fig. 3).

Postoperative study
In the postoperative study, CDUS examinations are
performed once a day during the first week after
surgery. The protocol for both qualitative and Fig. 3. Standard model of scanning by color Doppler ultra-
quantitative hemodynamic evaluations follow the sound showed hepatic vein flow and measurement of parame-
previous general principles for PV, HV and HA, ters with angle correction and scale without aliasing. For these
respectively. The first postoperative CDUS examina- cases, the waveform analysis and calculations were as follows:
there are normal triphasic waveform and biphasic waveform
tion is best performed within 12 hours after surgery.
in the case of (A) and (B), the peak of flow velocity (Vp)
After 7 postoperative days, the schedule for CDUS are 59 and 61 cm/s, respectively; otherwise, there is an abnor-
is once per week before discharge or based on mal monophasic waveform in the case of (C) and relatively
need according to clinical condition. low Vp.

J Med Ultrasound 2008 Vol 16 No 3 179


T.L. Huang

The CDUS Study for Pretransplant overcome using venous grafts, and successful
Recipients on the Waiting List LDLT has been achieved in recent years by some
centers. PV thrombosis is not a contraindication to
Since the initiation of LDLT in Kaohsiung in 1994, LDLT, but the limit of thrombosis must not be
we have evaluated many infants and young children
with biliary atresia awaiting LT, and have found a A
high 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), and
anomalous origin of the HA (n = 6) [2,3,5].
In the preoperative study, we also found a group
of pediatric recipients with high HA RI (some with
an RI > 1.0) and frequent admissions because of
fever and sepsis. According to the survival analysis
B
for all relevant risk factors, high HA RI (> 1.0) and
low portal flow velocity (< 10 cm/s) had definite
significance for mortality [6] (Fig. 4). These cases
could no longer wait and required transplantation
for life-saving reasons. For the preoperative evalua-
tion of PV quality, a smooth portal wall and patent
flow are essential. In our research report of a group
with portal insults, portal occlusion or absence is a
contraindication to LDLT, and low portal flow less
than 7 cm/s and small portal size less than 4 mm
are risk factors for intraoperative portal thrombosis C
[7]. With advances in surgical techniques, some
cases of intraportal partial thrombosis have been

Fig. 5. These cases were evaluated in a pretransplant study


and showed abnormal portal flow by color Doppler ultrasound:
(A) the first case had portal vein (PV) occlusion with obscured
PV tract and no portal flow signal; (B) the second had a small
Fig. 4. For this case of a young child on the waiting list for liver PV tract and slow low inflow (3 cm/s); (C) the third had
transplantation, the HA impedance was detected with an reverse hepatofugal portal flow and pulsatile waveform due to
resistance index of 1.20 (exceeding 1.0). This case has a high an arterioportal shunt. These abnormal portal flows are signif-
risk of mortality, and an early transplantation is a priority to icant and may be a contraindication to living donor liver trans-
save this patients life. plantation or are a risk for post-transplant portal thrombosis.

180 J Med Ultrasound 2008 Vol 16 No 3


CDUS in LDLT

beyond the main PV [8] (Fig. 5). All these predis- CDUS just after reperfusion of the graft is reliable.
posing vascular anomalies may be significant in The diagnostic criterion of HAT is the absence of
the decision to transplant and are well detected by Doppler signals, and in this situation, redo of HA
CDUS. Therefore, in deciding on the priority of pa- anastomosis or thrombectomy for resuscitation must
tients waiting for early transplantation, CDUS plays be undertaken immediately. If an abnormal flow
a really important role in pretransplant assessment. pattern with dampened systolic peak and slow peak
velocity (< 30 cm/s) occurs, HA angulation, stran-
gulation or spasm is usually the cause of HA insuf-
The Major Vascular Complications ficiency [4]. Rapid thrombosis formation in these
Detected by Intraoperative CDUS cases is possible. CDUS can help to assess and con-
firm the optimal flow change after the problem is
HA thrombosis and insufficiency resolved. The peak systolic Doppler velocity (PSV)
HA thrombosis (HAT) is the most serious vascular and waveform distal to the HA stenosis are also
complication in LT and results in hepatic necrosis, dampened, the PI and RI of the HA also fall owing
dysfunction and failure. The incidence of HAT in LT to poststenotic reactive vasodilatation and distal im-
varies from 7.413% and is higher in adult LDLT [9]. pedance [10,11]. Under this condition, a low HA
The advancement of HA anastomosis using micro- PSV due to a proportional increase in end-diastolic
surgical techniques has improved the success rate flow velocity is observed (Fig. 6). If the parameters
of HA reconstruction. The diagnosis of HAT by of HA flow detected are distal to the anastomosis,

A B

C D

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 for
thrombectomy was done with a slight improvement in flow, but optimal flow was not noted. (C, D) Thus, redo of HA anastomosis
was done and normal HA flow was regained as noted on CDUS check-up.

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T.L. Huang

A B

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.

any dampened flow waveform and velocity will in- On the contrary, PV hyperperfusion may occur with
dicate the presence of anastomotic stenotic change extremely high PVFV above 250 mL/min/100 g in
in the proximal HA [12]. Intraoperative CDUS is adult LDLT recipients. These patients will develop
easy to perform and provides the opportunity for post-transplant hepatic dysfunction such as small-
immediate treatment of such inadequate arterial for-size syndrome, which is often found among
reconstructions. CDUS also plays an important role those with a relatively small-for-size graft (graft-to-
in reducing the incidence of HAT following LDLT recipient weight ratio < 0.8) (Fig. 8). Portal hyper-
[13,14]. perfusion in small-for-size graft is thought to be
the main cause of small-for-size syndrome by portal
PV thrombosis, insufficiency and hypertension and damage to sinusoids and hepa-
hyperperfusion tocytes [16,17]. To overcome this problem, several
If there are no Doppler flow signals in the recon- therapeutic options have also been reported, such
structed PV, thrombosis of the PV is highly sus- as surgical modulation of splenic arterial ligation or
pected. However, poor PV flow signals with CDUS splenectomy to release portal hyperperfusion and
can be caused by acute angulation of the sound liver tissue congestion [1820] (Fig. 8). For detec-
scanning beam to the axis of the portal tract (> 60) tion of this disorder, CDUS is the most important
or the obliteration of extrahepatic PV with interven- modality for monitoring portal hemodynamics.
ing adipose tissue or bowel gas after surgery [10,11].
Thus, we should carefully exclude PV thrombosis HV outflow obstruction, HV thrombosis,
by CDUS. Immediate thrombectomy is the gold HV stenosis
standard for treatment of PV thrombosis. Inadequate Normal flow velocity and waveforms of HV should
low PV inflow (mean velocity < 12 cm/s) as PV insuf- be more than 12 cm/s at the peak of biphasic or
ficiency is usually detected in pediatric recipients triphasic waveforms, which reflect the patency of
owing to persistent large portosystemic collaterals hepatic outflow. Hepatic outflow obstruction after
such as the coronary vein, splenorenal shunt and reperfusion will result in a hard consistency and dark
gastrorenal shunt, sometimes owing to HV outflow discoloration of the graft noted by the surgeon
obstruction or low cardiac output (Fig. 7). An during the operation. CDUS examination is used
increase in PV inflow can be achieved by ligation immediately for evaluation. The characteristic CDUS
of portosystemic collaterals, relief of HV outflow findings are: (1) mild dilatation of the HVs; (2) flat
obstruction or redo of PV anastomosis [13,15]. or monophasic HV flow waveform; (3) slow HV

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CDUS in LDLT

A B

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 flow
volume (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 carried
out for modulation of portal hyperperfusion, and the PVFV was dramatically reduced to 233 mL/min/100 g, which was within
normal limits. The postoperative course of this patient was uneventful.

A B

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

peak velocity (< 10 cm/s); and (4) extremely low PV Broelsch et al [22]. In our experience, right rotation
flow velocity (< 14 cm/s) [9,21]. Intrahepatic venous of the graft in the wide abdominal space may result
thrombus is usually observed in HV thrombosis and in outflow stenosis and a flat HV flow waveform
immediate thrombectomy is needed. During trans- (Fig. 9). We can prevent such outflow obstruction
plant surgery, torsion of the graft was described by by fixing and stabilizing the graft in the optimal

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T.L. Huang

A B

C D

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.

position under the guidance of intraoperative CDUS, factors or with poor arterial quality. HAT is present
until a normal biphasic HV waveform is obtained in Doppler findings when absent arterial signals are
[1,11]. found in the whole graft scan or when only damp-
ened slow HA flow is noted. Further imaging with
CT angiography is suggested for confirmation. HAT
The Postoperative Vascular is usually successfully treated by thrombectomy or
Complications Detected by CDUS redo of anastomosis or jump graft following early
diagnosis [2325].
Postoperative HAT
Postoperative HAT usually occurs in the first post- Postoperative PV thrombosis or PV stenosis
operative day but can occur up to 1 week after Postoperative PV thrombosis may also occur in the
surgery. We perform routine CDUS examinations early postoperative period. CDUS shows slow or
on the first postoperative day, especially within absent portal flow or direct visualization of throm-
12 hours of surgery and in patients with high risk bus. Sometimes, hepatofugal PV flow is noted and

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CDUS in LDLT

A B

C D

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 multiphasic
pattern and Vp increased to 72 cm/s. Following this treatment, the ascites dramatically subsided.

may be associated with HV outflow obstruction Postoperative HV thrombosis or


[10,12,26]. Surgical thrombectomy, redo of anas- HV stenosis
tomosis or infusion of a thrombolytic agent is used HV outflow obstruction may also develop after
in the management of this disorder. Postoperative transplantation, the obstruction usually occurs at the
PV stenosis may develop and cause hepatic dys- anastomotic site and is mainly caused by chronic
function with intractable ascites. CDUS examination fibrosis at the stenotic site and hypertrophy of the
shows marked turbulent flow or slow flow and ex- graft [28,29]. CDUS detection shows a flat flow
tremely high-flow velocity (may be up to 200 cm/s) waveform and slow HV flow velocity (< 10 cm/s);
detected at the narrowed anastomosis. Further hepatofugal PV flow may occur in severe obstruc-
management with percutaneous transhepatic por- tion. Therapeutic procedures of angioplasty with
tal angioplasty with balloon dilatation or Wallstent balloon dilatation or Wallstent interposition are sug-
interposition is suggested [15,27] (Fig. 10). gested for this disorder [30] (Fig. 11). CDUS is used

J Med Ultrasound 2008 Vol 16 No 3 185


T.L. Huang

before and after angioplasty or stenting for effec- 5. Chen TY, Cheng YF, Huang TL, et al. Preoperative
tive treatment with successful regain of normal HV assessment of the portal vein in potential pediatric liver
outflow [31,32]. transplantation recipients: comparison of sonography
and invasive portography. Transplant Proc 1998;30:
31956.
6. Huang TL, Chen CL, Chen TY, et al. Doppler ultra-
Conclusion sound in prediction of the early mortality risk factors
on the waiting list for pediatric liver transplantation
CDUS has wide use in LT and is the modality of recipients. Transplant Proc 2001;33:899900.
choice in the evaluation of hepatic graft hemody- 7. Cheng YF, Chen CL, Huang TL, et al. Risk factors for
namics and the diagnosis of vascular complications. intraoperative portal vein thrombosis in pediatric living
This modality has a very important role in preoper- donor liver transplantation. Clin Transplant 2004;18:
ative, intraoperative and postoperative evaluations 3904.
8. Cho JY, Suh KS, Shin WY, et al. Thrombosis confined to
for the immediate assessment of general condition
the portal vein is not a contraindication for living donor
and early detection of complications. Timely re-
liver transplantation. World J Surg 2008;32:17317.
cognition of any complications could improve the 9. Someda H, Moriyasu F, Fujimoto M, et al. Vascular
success of LT. complications in living related liver transplantation
Chang Gung Memorial Hospital was the first detected with intraoperative and postoperative
center to perform LT in Taiwan and carried out a Doppler US. J Hepatol 1995;22:62332.
successful case of orthotopic liver transplantation 10. Huang TL, Cheng YF, Chen TY, et al. Portal hemody-
in 1984, and was the first to start a program of LT. namics in living-related liver transplantation: quanti-
Due to the scarcity of source- and size-matched graft tative measurement by Doppler ultrasound. Transplant
Proc 1998;30:31867.
donors for infants and young children, we were
11. Cheng YF, Huang TL, Chen CL, et al. Intraoperative
the first to initiate cadaveric split-liver transplanta-
Doppler ultrasound in liver transplantation. Clin
tion and LDLT, respectively. CDUS is now performed Transplant 1998;12:2929.
routinely for the evaluation of hepatic hemodynam- 12. Huang TL, Cheng YF, Chen CL, et al. Intraoperative
ics. Although high rates of vascular complications Doppler ultrasound in living-related liver transplan-
resulting in graft failure are still reported by many tation. Transplant Proc 2000;32:20978.
centers worldwide, our center has had good results. 13. Cheng YF, Chen YS, Huang TL, et al. Interventional
radiologic procedures in liver transplantation. Transpl
Int 2001;14:2239.
14. Sidhu PS, Ellis SM, Karani JB, et al. Hepatic artery
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