The role of Doppler ultrasonography in monitoring the hepatic graft in the early post transplantation period

The role of Doppler ultrasonography in monitoring the hepatic graft in the early post transplantation  period

Maha K Abdel Ghaffar, MIJa; Mohamed Sobhy, MIJa;

MohamedAmin Nassef, MD; Mohamed  Bahaa, MJJb

a) Department of Radiodiagnosis, Ain Shams University, Cairo, Egypt. b) Department of Surgery, Ain Shams University, Cairo, Egypt.

Purpose:   To distinguish  the  alarming   from the  non-alarming signs  during  immediate postoperative  Doppler ultrasonography (US) follow up for liver transplantation cases.

Patients  and methods:  From March 2012 to June 2013, 36 patients of post living related donor liver transplantation where followed up in the first month after liver transplantation and the US and Doppler US changes were recorded together with their laboratory data. When there were alarming Doppler US signs CT angiography was done to confirm vascular complications.

Results:  5 cases  (13.8%)  presented  with hyperechoic  segments  due to segmental  venous congestion,  12 cases  {33.3%) showed  raw  surface  collection,  15  cases  (41.6%)  presented with free peritoneal fluid and 18 cases (50%)   had right pleural effusion. One patient (2.7%) presented with occluded hepatic artery and thrombectomy was done. 30 cases {83.3%) showed increased  portal  vein velocity  The mortality  was 8.3% seen in 3 cases, two of them  (5.5%) suffered from  7th day syndrome presented with abrupt sharp decrease in portal flow and one case (2.7%) had a small graft size and presented with marked slowliness of the portal flow on Doppler study and a venous infarct on CT

Conclusion: The early monitoring  of graft hemodynamic  changes by Doppler sonography is of great importance  as  most of these  changes  revert to normal  in the first postoperative week, however sharp decrease in arterial or portal flow indicates  underlying grave vascular complications, some of them are correctable.

Introduction:

End-stage liver disease (ESLD) and (HCC) have become the main cause of mortality in our country in patients with hepatitis B or C vtruses.

Orthotopic  liver transplantation  (OLT) is

the only definitive treatment for patients with irreversible acute and chronic liver disease.l

Patients should be considered for liver transplantation  if they have evidence of fulminant hepatic failure, a life-threatening systemic  complication   of  liver  disease,  or a liver-based metabolic defect or, more commonly,    cirrhosis    with    complications such as hepatic encephalopathy, ascites, hepatocellular carcinoma, hepatorenal syndrome, or bleeding caused by portal hypertension.   While  the   complications   of

cirrhosis can often be managed relatively effectively,  they  indicate  a  change  in  the natural history of the disease that should lead to consideration of liver transplantation.2

Ultrasonography (US) and Doppler examination    is    the    preferred    modality for postoperative  imaging  because  it is portable, is readily available, and provides early  detection   of  complications.   Doppler US is used to detect treatable vascular complications and ensure graft survival. The first 24 hours after transplantation are referred to as the "hyperdynamic phase," in which the transplanted liver demonstrates disordered circulatory patterns and hemodynamic instability.  The  first  postoperative   Doppler US   images   are   obtained   fairly   early  on the  first  postoperative  day,  before  surgical

Am-Shams] Surg 2014; 7(19):1-10

wounds have been closed. 1

The aim of our work is to highlight the alarming and non-alarming  Doppler US findings  in the  immediate  postoperative images, obtained when the effects of surgery are very recent. Most of these changes revert to normal in the first postoperative week; deterioration of transient changes requires further evaluation.

Methods:

During  the  period  from  March  2012  to June 2013, 36 adult patients (25 males, 9 females)  ranging  in age  between  37 to  59 years  with  mean  of  53.4  years  underwent living  related  donor  liver transplantation  in Ain Shams University Specialized hospital (liver transplantation unit). Indication for transplantation was end stage liver disease for

27 cases and HCC in 9 cases. 7 of our patients

had chronic portal vein thrombosis of variable extent  and for  all successful  thrombectomy was done during surgery Table (1).

Routine gray-scale US ofthe transplanted

liver  was  performed  with  detailed  vascular Doppler  US. During the first week, patients were   examined   daily  using   Doppler   US, then every other day till the third week and twice  weekly  for  the  rest  of  the  1st three months.  The  examination  was  done  using a  5  MHz  curved  array  transducer  LOGIQ

500  (GE,   YokogawaMedical   System   Ltd,

Tokyo,  Japan).  All patients  were examined in the supine position during quiet breathing. Doppler tracings of portal vein were obtained from the right branch of the portal vein in the case of right lobe graft and from umbilical portion of the portal vein in the case of left lobe graft. Doppler tracings of hepatic artery were obtained from the right hepatic artery in the case of right lobe graft and from the left hepatic artery in the case of left lobe graft. Veins of the graft were also examined.

During the  Doppler  US examination  the

following were observed:

-Homogenicity  of the graft which was affected by the effect of reperfusion edema and fluid stasis in the extracellular compartments.

-Presence of collections or free fluid in pleura or peritoneum.

-Patency of hepatic artery and its wave pattern  demonstrated  normally  by  rapid systolic upstroke with systolic acceleration time of less 80 msec and continuous diastolic flow,  and  RI  which  ranges  normally  from

0.55 to 0.8.

-Patency of portal vein presented normally by a centripetal direction of flow and a mean portal velocity of 58 em/sec at the anastomosis site.

-Patency  of hepatic veins  and its normal

triphasic wave pattern.

In cases of persistent  abnormality  in Doppler US study or ifthere were laboratory abnormality   as  increased   level  of  SGOT, SGPT, bilirubin, INR and serum lactate with no significant Doppler explanation, diagnostic CT angiography was recommended.

Results:

36 patients after living related donor liver transplantation were  examined  daily during the first week using US and Doppler US, then every other day till the third week and twice weekly for the rest of the 1st three months Tables (2-3).

Five cases (13.8%) with segmental venous

congestion presented with hyperechoic segments and had increased levels of SGOT and SGPT in the first week Figure (1).

Twelve cases (33.3%) showed raw surface

collection,  15 cases (41.6%)  presented  with free peritoneal fluid and 18 cases (50%) had right pleural effusion Figure (2).

We had one patient with occluded hepatic

artery  in day  2, he presented  with shooting liver  enzymes  and  increased  serum  lactate. Occluded hepatic artery was confirmed by 3D CT MIP (maximum intensity projection) and the patient was explored and a thrombus was found  in  hepatic  artery  at anastomotic  site. Thrombus  was  removed,  anastomosis  was revised and patency was regained Figure (3).

The  increased  portal  vein  velocity  was

detected   in  30  patients   (83.3%)   and  was noticed to be the most frequent  abnormality seen  in the  early post-operative  period however  it  declined  gradually  through  the first month Figure (4).

Additionally   2  cases  (5.5%)  developed

Figure (1): /creased liver enzymes in day 3 after LT in a 50 years old male. Gray scale US shows congested hyperechoic area at segment VII of the graft.

Figure (3): Shooting liver enzymes with increased serum lactate in the second day after LT in a 53 years old male. A and B: 3D CT MIP showing abrupt occlusion of hepatic artery at the surgical anastomosis {arrow). C: Pulsed Doppler and  D: Color Doppler showing patent hepatic artery after removal of thrombectomy.

what is known as 7th day syndrome in which the pmtal flow showed abrupt sharp decrease in day 7 reaching to less than 5 crn!s and unfortunately both patients died in day 8 and day 9. They showed shooting levels in SGOT and SGPT as well as bilimbin and INR.

We also had one patient (2.7%) who presented  with slowliness  of  pmtal  flow at day 7 reaching 18 cm/s with shooting levels

Figure   (2):  Organized  haematoma  in  a

47 year old female. Gray scale US image obtained on the first day after LT shows organized collection (haematoma) at the raw surface of the graft.

Figure (4): Increased portal venous flow in a 56 years old male patient. Pulsed Doppler US obtained on the third day after LT shows increased portal venous velocity {162 em/ sec) due  to  presence of persistence portal hypertension before the surgery.

of SGOT, SGPT and bilimbin. CT was done because Doppler US alone could not explain the laboratmy  abnmmalities  and  it showed a non-enhancing  wedge shaped area around a patent tight  hepatic vein. This area was a venous infarct that occUlTed despite patency of  the  tight  hepatic  vein  due  to  the  small size of the graft. The  patient died on day 9

Figw·e(S).

Figure (5): Shooting liver enzymes with increased serum bilirubin in day 7 after LT in a 48 years old female patient. A: CT scan shows a wedge shaped infarction oriented around a patent right hepatic vein {arrow).B: CT scan shows patent graft artery {arrow), C: CT Shows patent portal vein {arrow), D: Pulsed Doppler study of the right hepatic vein showing its patency with triphasic flow.

Table (1): Patient's clinical presentation before liver transplantation.

Table (2): Summary of ultrasonographic manifestations and the resu/1 of the patient's follow up.

Table (3): Summary of Doppler manifestations and the resu/1 of the patient's follow up.

Discussion:

Angiography  is the standa.I·d of reference for exploration  in the assessment  of hepatic vessels  patency; it is an invasive  technique

and requires intravenous administration of iodinated   contrast,   increasing   the  tisk   of renal function impainnent,  which is fi:equent dming the eru·ly postoperative  period in liver

transplanted  patients.3 DUS is the screening technique preferably used in the transplanted liver  as  it  is  a  noninvasive  procedure  and very usefulness  in the assessment  of hepatic vessels patency.4

Routine gray-scale US of the transplanted liver is performed before detailed vascular Doppler  US.  It is  fairly  common  for  the effects of reperfusion  edema and fluid stasis in the extracellular compartments to manifest as   the    so-called    starry-sky    appearance of reperfusion hepatic edema, which is characterized by visible portal venules and diminished parenchymal echogenicity that accentuate the portal venule walls. Other common gray-scale US findings include variable amounts of perihepatic hematoma, small fluid collections, and sympathetic right pleural  effusion.1 In our patient  population,

5   cases   (13.8%)   with   segmental   venous

congestion presented with hyperechoic segments and had increased levels of SGOT and SGPT in the first week. 12 cases (33.3%) showed raw surface collection,  15 cases (41.6%)  presented with free peritoneal  fluid and 18 cases (50%) had right pleural effusion.

Angeles Garcia-Criado  et al,4 have performed  DUS routinely  in the first 3 days after OLT in all patients who have had liver transplants. In this early period it is common to  detect  a  high   RI  (>0.8)  that  becomes normal  a few  days  after  transplantation  if there  are  no  abnormalities   in  the  hepatic artery. Transient increased arterial resistance has  been  attributed  to  various  causes,  such as  hepatic  arterial  spasm;  increased  portal flow, which inhibits the release of arterial vasodilators; tissue edema; increased cold ischemia time; and an older age in liver donors.5-7   They    had    surmised    initially that this high resistance would lead to an increased risk of HAT.4 It has been reported that prompt diagnosis of HAT may be of great significance   because   retransplantation   can be avoided  by  prompt  revascularization.s-10

Pulsed Doppler sonography is important since blood flow can be demonstrated.  Findings indicative of anastomotic stenosis are normal flow proximal to the stenosis,  high-velocity

flow  at the  stenosis,  and  turbulence  above

the stenosis. 11- 12  In our  study, we  had  one patient  with occluded  hepatic  artery  in day

3,  exploration  was  done  immediately   and

a thrombus  was found  in the hepatic artery at the anastomotic site. The thrombus  was removed,  anastomosis  was  revised  and patency was regained.

Immediately   after  OLT,  reduced   portal

resistance in the presence  of increased splanchnic  flow  leads  to  increased   portal flow, which manifests as increased portal venous velocity at immediate post-OLT Doppler   US.  Another   cause  of  increased portal venous velocity in the immediate post­ OLT period  is transient  compression  of the pliable  portal  vein  by  postoperative  edema or fluid. Subsequently, the body adapts, and portal blood flow decreases, with an average decrease  in  portal  venous  velocity  of 20% over the next few days.1 In our study, The increased portal vein velocity was detected in

30 patients (83.3%) and was noticed to be the

most frequent  abnormality  seen in the early post-operative period however it declined gradually through the first month.

Portal     vein     thrombosis     (PVT)     is     a

common  complication  of  chronic  liver disease with an incidence that varies between

0.6% and  15.8%.13 In  past years,  PVT has been taken a contraindication for LT.14 With improvement  of surgical techniques  and the use of aggressive approaches have made it possible to overcome PVT during LT, which is  currently  the  only  way  to  cure  patients with end-stage liver disease and concurrent PVT1-14_    Enhancement    of   post-transplant care made the outcomes of PVT patients very close to those of non-PVT patients.15 In the present study, we had 7 patients with chronic portal  vein  thrombosis   that  was  removed during  surgery  and  they   had  high   portal flow in the postoperative period declining gradually to the normal levels during the following  weeks. On the other hand we had

2  patients  (5.5%)  with  7th day  syndrome and one patient (2.7%) with small graft size who presented with abrupt decrease of the portal flow. In the latter case, the slowliness of the portal flow appeared at day 7 reaching

18 cm/s with shooting  levels  of SGOT and

Due  to the  limited number of patients and the  relative short  period of study,  we  agreed with  Wozney et  ai16 and   Lerut  et  ai17 that thrombosis of the IVC and stenosis of the IVC anastomoses are  rare  vascular complications of orthotopic liver transplantation as we were not  confronted with  these  complications.  In the contrary, Yi-Ping Jia et ai15 recognize IVC thrombosis in 10 cases out of 284 LT on  5-13 days   postoperatively.  All   were    subhepatic IVC  thrombosis,  with    4  complete  and   6 partial thromboses. Recanalization occurred in  9  cases   after   anticoagulation.  One   case with  partial thrombosis got natural cure  after

2 months.

Conclusion:

The early monitoring of graft hemodynamic changes  by   Doppler  ultrasonography  is  of great importance as most  of these changes revert to   normal  in  the   first   postoperative week,  however  sharp   decrease  in   arterial or portal flow  indicates underlying grave vascular complications, some  of them  are correctable.

Reference

1-    Sanyal  R;  Lall   CG;     Lamba   R;  Verma S; Shah SN; Tirkes T:    Orthotopic liver transplantation: Reversible Doppler US findings in the  immediate  postoperative period. RadioGraphies 2012; 32: 199-211.

2-    O'leary JG; lepeR; Davis GL: Indication for liver  transplantation.   Gastoentrology 2008;

134(6): 1764--1776.

3-    Rimola A; Gavaller J; SchadeR; El-Lankany S;  Starzl  TE;  van  Thiel  DH:   Effects   of renal impairment on liver transplantation. Gastroenterology1987; 93(1): 148-156.

4-    Garcia-Criado A; Gilabert R; Nicolau C; Real I; Arguis P; Bianchi L; et al: Early detection of hepatic artery thrombosis after liver transplantation by Doppler ultrasonography.

1Ultrasound Med 2001; 20(1): 51-58.

5-    Chezmar    JL;    Nelson    RC;    Bernardino lVIE:    Portal    venous     gas    after    hepatic transplantation: Sonographic  detection  and clinical  significance.  A1R Am 1 Roentgenol

1989; 153(6): 1203-1205.

6-     Chen  W; Facciuto  lVIE; Rocca  JP; Marvin MR; Sheiner  PA; Rachlin  S; et al: Doppler ultrasonographic findings on hepatic arterial vasospasm early after liver transplantation. 1

Ultrasound Med2006; 25(5): 631--638.

7-     Sanyal R; Shah SN: Role of imaging in the management of splenic artery steal syndrome.

1Ultrasound Med2009; 28(4): 471--477.

8-    Sheiner   PA;  Varma   CVR;   Guarrera   JV; Garratti M; Emre S; Guy SR; et al: Selective revascularization ofhepatic artery thromboses after  liver  transplantation  improves  patient and  graft  survival.   Transplantation 1997;

64(9): 1295-1299.

9-    Pinna  AD; Smith  CV; Furukawa  H;  Starzl TE;  Fung  JJ:  Urgent  revascularization of liver allografts after early hepatic artery thrombosis.   Transplantation 1996;  62(11):

1584-1587.

10- Langnas  AN; Marujo  W; Stratta  RJ; Wood RP; Shaw BW: Hepatic allograft rescue following  arterial thrombosis: role of urgent revascularization. Transplantation   1991;

51(1): 86-90.

11- Longley   DC;   Skolnick   ML;   Zajko   AB; Bron KM: Pictorial essay: Duplex Doppler sonography in the evaluation of adult patients before  and  after  liver  transplantation.   A1R

1988; 151: 687--696.

12-  Taylor KJW; Morse  SS; Weltin GG; Riely CA; Flye MW: Liver transplant recipients: Portable                 Duplex    US    with    correlative angiography.    Radiology    1986;     159(2):

357-363.

13-  Wul  TH; Lin YS; Lee CF; Wu TJ; Yu MC; ChanKM; etal: Clinical analysis and strategy for liver transplantation  in patients with pre­ existing portal vein thrombosis.  Chang Gung Med12011; 34(4): 426--433.

14- Langnas   AN;   Marujo    WC;   Stratta   RJ;

Wood RP; Ranjan D; Ozaki C; et al: A selective   approach   to   preexisting    portal vein thrombosis in patients undergoing  liver transplantation.   Am 1 Surg 1992;  163(1): cl32-136.

with   Doppler   ultrasonography.    World   1

Gastroentero12007; 14; 13(34): 4636-3640.

16-  Wozney P;  Zajko  AB; Bron  KM;  Point  S; Starzl TE: Vascular complications  after liver

transplantation:   a  5-year  expenence.  AJR

1986; 147(4): 657--663.

17- Lerut J; Tzakis AG; Bron K; Gordon RD; lwatsuki S; Esquivel CO; etal: Complications of venous reconstruction in human orthotopic liver transplantation. Ann Surg 1987; 205(4):

404--414.