Open Journal of Organ Transplant Surgery, 2011, 1, 1-7
doi:10.4236/ojots.2011.11001 Published Online August 2011 (
Copyright © 2011 SciRes. OJOTS
Hypercoagulability in Liver Transplant Recipients:
Does Portal Vein Thr ombosis Predict Post-Operative
Thrombotic Complications?
Brintha K. Enestvedt1, C. Kristian Enestvedt2, Brian Diggs3, Susan L. Orloff4
1Division of Gastroenterology, The University of Pennsylvania, Philadelphia, USA
2Division of Abdominal Transplantation, The University of Pennsylvania, Philadelphia, USA
3Department of Surgery, Oregon Health & Science University, Portland, USA
4Abdominal Transplantation, Oregon Health & Science University
and Portlan d Vet e rans Affairs Medical Center, Portland, USA
Received July 30, 2011; revised August 15, 2011; accepted August 23, 2011
Background: Cirrhotic patients have higher rates of hypercoagulable disorders. We hypothesized that or-
thotopic liver transplant (OLT) recipients with pre-operative portal vein thrombosis (PVT) have more post-
operative thrombotic events than those without PVT. Aims: To compare rates of post-op thrombotic events
and outcomes between those with and without pre-op PVT. Methods: All OLT recipients between 1/02-4/09
were retrospectively reviewed. Outcome measures included survival, deep venous thrombosis, pulmonary
embolism, hepatic artery thrombosis, and recurrent PVT. Minimum follow up was 6 months. Results: In 363
OLTs performed, mean recipient age was 53.1 yrs (±9.2); 268 patients were male. Mean MELD at transplant
was 22.1 (±6.2). The prevalence of pre-op PVT was 11.2% (41/350). There was no difference in the % of
post-op thrombotic events between those with and without PVT (p = 0.77). MELD, recipient and donor age,
and gender were similar in both groups. Mean survival in those with pre-op PVT was 85.2 months vs. 78.7 in
those without PVT (p = 0.19). Conclusions: The rate of post-op thrombotic events was equivalent in OLT
recipients with and without pre-op PVT. The presence of PVT did not adversely impact patient survival and
should not be a contraindication to OLT.
Keywords: Portal Vein Thrombosis, Orthotopic Liver Transplantation, Hypercoagulability, Thromboses
1. Introduction
Portal vein thrombosis is a known complication in those
with advanced end stage liver disease (ESLD), occurring
in 0.6% - 25% [1-4] of these patients in contemporary
reports. In the largest study to date a prevalence of 11%
was reported in 701 patients with cirrhosis [5]. Once
considered an absolute contraindication to orthotopic
liver transplantation (OLT), portal vein thrombosis (PVT)
can be managed operatively with thrombectomy or venous
replacement conduits; however due to the surgical com-
plexity and high risk for recurrence, it remains a for-
midable clinical problem [2,6-10]. While mostly asso-
ciated with hepatocellular carcinoma, PVT in cirrhotic
patients, even in the absence of neoplasia may be the
result of an underlying hypercoagulable disorder, as is
suggested by some preliminary data [11-13].
Mounting evidence suggests that patients with cirr-
hosis, similar to those with pulmonary embolism or deep
venous thrombosis, have underlying inherited or acqui-
red thrombophilic disorders such as prothrombin gene
mutation, hyperhomocysteinemia (MTHFR gene muta-
tion), anti-cardiolipin antibodies or Factor V Leiden [4-5,
14-17]. This hypercoagulable condition may also contri-
bute to post-operative thrombotic events which can be
devastating and life threatening. The identification prior
to OLT of a pre-operative risk factor for post-operative
clot formation (such as portal vein thrombosis), would
enable the institution of preventive strategies to limit these
thrombotic complications. Unfortunately, the available
literature on PVT in cirrhotics is limited by cross sectional
studies with small sample sizes and few controlled data on
which to base clinical decisions in patients with PVT.
We hypothesize that liver transplant recipients with
pre-operative portal vein thrombosis have a higher rate
of post operative thrombotic events than those without
PVT. The aims of the current study were to describe the
prevalence of pre-operative portal vein thrombosis in
liver transplant recipients, describe intra-operative mana-
gement particular to this problem, and compare the rates
of post-operative thrombotic events and overall out-
comes between those with and without pre-operative
PVT. We also evaluated significant risk factors for the
development of portal vein thrombosis and other post-
operative clot development.
2. Materials and Methods
A retrospective chart review was performed of all
patients who underwent OLT between 1/02- 4/09. Data
gathered included recipient and donor age and gender,
Model for End Stage Liver Disease (MELD) score,
etiology of ESLD, presence of hepatocellular carcinoma
(HCC), PVT at the time of liver transplant, warm and
cold ischemia times, CMV donor-recipient status, use of
donor after cardiac death (DCD) organ, intra-operative
management of PVT (thrombectomy, iliac conduit), the
development of post operative thromboses (including
deep venous thrombosis, pulmonary embolism, hepatic
artery thrombosis, and recurrent PVT), post operative
biliary stricture, rejection, bile leak and survival. The
diagnosis of portal vein thrombosis was made either by
pre-operative imaging by computer tomography (all
patients underwent immediate pre-operative CT scans),
ultrasound or by intra-operative findings.
The primary outcome measures were post-operative
thrombotic events such as recurrent PVT, hepatic artery
thrombosis, PE and DVT as confirmed by radiographic
studies. Principal diagnostic tests included Duplex
ultrasound of either the hepatic vasculature or the lower
extremities (for DVT) or contrast CT of the chest (for PE)
or of the abdomen (for PVT). These imaging modalities
were pursued for symptoms. Secondary outcomes in-
cluded post-operative biliary stricture, leak, rejection and
survival (measured in months). All transplants were
performed at a single shared transplant center consisting
of Oregon Health & Science University (OHSU) and the
Portland Veteran’s Affairs Medical Center (PVAMC)
and the pre-, peri- and post-operative care was managed
by this shared transplant institution’s staff.
The UNOS listed MELD was used for analyses except
for those patients who had a MELD exception for HCC.
In these patients biologic MELD was substituted to
better reflect their true liver disease severity. We exclu-
ded patients with Status 1 priority as their physiology is
not likely related to underlying cirrhosis. All patients had
a minimum of 6 months of follow up. Univariate stati-
stical analyses included student’s t-test, X2 test, and
Kaplan Meier log-rank were performed using SPSS
version 17.0 (SPSS Inc, Chicago, IL). Binary logistic
regression was performed to identify risk factors for
post-operative clot. A p value of <0.2 on univariate
analysis met inclusion in multivariate analysis. A p value
<0.05 was significant on multivariate analyses. Co-
variates included in the multivariate model included all
significant univariate variables in addition to those
variables deemed clinically relevant to the development
of post operative clot. This study was approved by the
IRB committees at Oregon Health & Science University
and the Portland Veteran’s Affairs Medical Center.
3. Results
A total of 976 orthotopic liver transplants were per-
formed at our institution from 1998 to April, 2009. Three
hundred and sixty two (362) occurred during the study
time frame (2/02-4/09). After excluding patients with
status 1 priority (n = 12), the study cohort was 350 pa-
tients. Table 1 describes the demographics of the study
cohort and compares those with and without portal vein
thrombosis. The overall mean recipient age was 53.1
±9.2 years old. The majority of OLT recipients were
male (76.6%); the mean MELD was 22.1 ± 6.23. Alcohol
(ETOH) and hepatitis C (HCV) comprised 65% of the
etiologies of ESLD. Hepatocellular carcinoma (HCC)
was found in 108 patients (30.9%). The complete distri-
bution of the etiology of end stage liver disease (ESLD)
is as follows: HCV alone 17.4% (61), ETOH/HCV
16.6% (58), HCV/HCC 14.3% (50), PSC 10.6% (37),
ETOH alone 6.9% (24), ETOH/HCV/HCC 6.6% (23),
HBV related 5.1% (18), PBC 4.9% (17), NASH 3.4%
(12), ETOH/HCC 3.1% (11), Autoimmune hepatitis
2.9% (10), Cryptogenic cirrhosis 2.6% (9), other 5.7%
The prevalence of portal vein thrombosis was 11.2%
(n = 41); 77.5% (n = 31) were partial thromboses and 9
patients had complete PVTs. There was no difference in
the recipient or donor age and gender, or MELD between
those with and without pre-operative PVT (Table 1). The
post-operative thrombotic rate in those patients with
pre-operative portal vein thrombosis was 9.8% (4/41)
compared with 8.4% (26/309) in those without PVT (p =
0.77, Table 2). There was no difference in the type of
post-operative thrombosis between the two groups. Of all
the etiologies of ESLD, only alcohol related liver disease
was statistically significantly higher in those who had
PVT compared to those withut (48.8% vs. 32.7%, p = o
Copyright © 2011 SciRes. OJOTS
Copyright © 2011 SciRes. OJOTS
Table 1. Demographics of patients with and without pre-operative portal vein thrombosis.
All OLTs PVT No PVT p value
N (%) 350 (100%) 41 (11.2%) 309 (88.3%)
Mean Recipient Age (yrs) 53.1 ± 9.2 55.2 ± 8.6 52.8 ± 9.5 0.12
Recipient Gender M 268 (76.6%)
F 82 (23.4%)
M 31 (75.6%)
F 10 (24.4%)
M 237 (76.7%)
F 71 (23.3%) 0.88
MELD 22.11 ± 6.2 21.0 ± 5.4 22.3 ± 6.8 0.25
Mean Donor Age (yrs) 38.9 ± 16.7 42.6 38.4 0.20
Donor Gender M 207 (60.7%)
F 134 (39.3%)
M 24 (58.5%)
F 7 (39.0%)
M 183 (59.4%)
F 117 (38.0%) 0.87
OLT: orthotopic liver transplant; PVT: portal vein thrombosis; MELD: model for end stage liver disease.
Table 2. Prevalence of post operative thromboses.
Post Operative Thromboses
PVT Other Clot Hepatic Artery Thrombosis Total Clots p value
Pre-Op PVT (41) 2 2 0 4 (9.8%)
No Pre-Op PVT (309) 4 16 6 26 (8.4%)
Total (350) 6 18 6 30
p value 0.10 0.93 0.37
PVT = portal vein thrombosis.
mediate CMV status (donor negative, recipient positive)
was inversely associated with post-operative thrombosis
(OR 0.07, 95% CI 0.07 - 0.81, p = 0.034).
0.042). Operative thrombectomy was performed in 68%
(28) of patients with PVT.
The rates of rejection, biliary stricture, biliary leak and
need for re-transplantation were not significantly differ-
ent between those with and without PVT (Table 3). Me-
dian survival in those with PVT was 82.5 months com-
pared with 78.7 months in those without PVT (p = 0.19.
Figure 1).
4. Discussion
In this study at a single shared transplant center, the
prevalence of pre-operative portal vein thrombosis in
liver transplant recipients was 11.2% which is similar to
Thirty patients (8.6%, 30/350) developed a post-
operative clot. The following variables were included in
a multivariate regression model assessing risk factors for
post operative clot: recipient age, recipient gender,
etiology of ESLD, MELD, pre-op PVT, donor age, donor
gender, warm and cold ischemia time, CMV risk status
(low risk, intermediate risk, high risk), DCD liver, HCC,
rejection (Tables 4(a) and (b)). Female donor gender
was associated with a three-fold greater risk of post-
operative clot compared to male donors (OR 3.06, 95%
CI 1.14 - 8.24, p = 0.027) (Table 4(b)). Increasing warm
ischemia time was associated with post-operative clot
(OR 1.05, 95% CI 1.01-1.09, p = 0.016) for each minute
of warm ischemia time, the post-operative clot risk
increased by 5%. Rejection was associated with a three-
fold increase in post-operative clot (OR 3.36, 95% CI
1.21 - 9.37, p = 0.020). DCD livers were associated with
the highest risk for post-operative thrombotic complica-
tions (OR 7.49, 95% CI 1.03 - 54.28, p = 0.046). Inter-
Figure 1. Median survival post orthotopic liver transplan-
Copyright © 2011 SciRes. OJOTS
Table 3. Prevalence of non thrombotic post operative outcomes.
Post Operative Outcomes PVT (41) No PVT (309) p value
Rejection 9 (22%) 63 (20.6%) 0.84
Biliary Stricture 11 (26.8%) 51 (16.7%) 0.11
Biliary Leak 2 (5.0%) 13 (4.2%) 0.83
Re-Transplant 1 (2.4%) 12 (3.9%) 0.65
Table 4. (a) Risk factors for post operative thrombosis, univariate analysis (significant p < 0.20); (b) Significant
risk factors for post operative thrombosis, multivariate analysis.
Variable p value
Age 0.134
Gender 0.987
Etiology of ESLD:
Budd Chiari
MELD 0.274
Recipient Factors
Pre-op PVT 0.778
Donor Gender 0.201
Warm ischemia time 0.009
Cold ischemia time 0.100
CMV donor-recipient status:
Low risk (D–/R–)
Intermediate risk (D+/R+)
Intermediate risk (D–/R+)
High risk (D+/R–)
DCD liver 0.249
Peri-operative Factors
Presence of HCC 0.345
Post transplant factors Rejection 0.490
N = 30; DCD: donor after cardiac death; D–/R–: donor negative CMV, recipient negative CMV.
Variable p value Odds ratio 95% CI
Donor Gender 0.027 3.06 1.14 - 8.24
Warm ischemia time 0.016 1.05 1.01 - 1.09
Cold ischemia time 0.015 1.00 0.99 - 1.00
CMV donor-recipient status Intermediate risk (D-/R+) 0.034 0.07 0.07 - 0.81
Peri-operative factors
DCD liver 0.046 7.49 1.03 - 54.28
Post transplant factors Rejection 0.020 3.36 1.21 - 9.37
per minute of ischemia time.
Copyright © 2011 SciRes. OJOTS
that previously reported [1,3-6,18]. While PVT was once
considered a contraindication to liver transplantation and
thus significantly impacted a patient’s survival, advances
in surgical technique (thrombectomy, venoplasty and
iliac vein conduit) and catheter-directed therapies have
enabled successful liver transplantation in these patients.
However, PVT continues to pose clinical challenges.
Emerging evidence supports the role of acquired or in-
herited hypercoagulability, in particular JAK-2 mutation,
in the formation of portal vein thrombosis, even in pa-
tients with cirrhosis.
This study demonstrated that patients with pre-ope-
rative PVT did not have a higher rate of post operative
thromboses. Therefore, patients with PVT do not need
increased thrombosis surveillance in the post-operative
period. An important finding in this study was that there
was no significant difference in survival between those
who did and did not have portal vein thrombosis. Other
authors have reported decreased graft and patient
survival in patients with PVT. In one of the largest
reports detailing vascular complications in liver trans-
plants, Duffy et al showed a profound decrease in graft
survival for those patients who developed a post-
operative PVT (p < 0.001) [19]. The authors identified
the presence of pre-operative PVT as well as the use of a
portal vein graft as a significant risk factor for post-
operative PVT (p < 0.01), In addition, these authors
noted a significant ‘late’ thrombosis rate, which occurred
in 35% of the PVT patients. However, Duffy and
colleagues reported a post-transplant PVT rate of only
3% in the 215 patients for whom a pre-operative diag-
nosis was made and eversion thromboendovenectomy
was performed, indicating that early identification and
appropriate operative intervention are essential to ensure
good outcomes [19]. It may be that our study has not
captured a percentage of these patients who develop
‘late’ thromboses, due to insufficient follow up time or
subclinical presentation. Additionally, the disparities in
our findings may be further explained by the smaller
cohort and number of post-operative PVTs, as well as
improvements in operative and radiologic imaging tech-
niques, and post-operative therapies. In particular, ade-
quate pre-operative recognition of this problem leads to
better operative planning and management of the diffi-
cult portal vein. At the time of listing patients for trans-
plantation at our center, routine pre-operative review of all
imaging is performed to prepare for intra-operative and
anatomic challenges. Our findings are supported by other
series that have demonstrated excellent outcomes with
operative thrombectomy in patients with preop PVT
Multivariate regression analysis identified several
significant risk factors for the development of post-
operative clot. These included longer warm ischemia
time, DCD liver, donor gender and rejection. The finding
that both increased warm ischemia time and the use of
DCD livers contributed to a higher complication rate is
consistent with the existing body of literature. Previous
authors have also shown an association between female
donor gender and post-transplant complications, as sup-
ported in the present study [22-27]. It may be that the
higher estrogen milieu of the female donor influences
thrombotic events in the recipient; however, further
study is needed to confirm this hypothesis. Further
analysis of the treatment regimens used for rejection
might indicate an association between thromboses and
the therapeutic agents commonly used to treat rejection
and could be an excellent area for further investigation.
The current study has several limitations. First, it is
prone to those shortcomings inherent in a retrospective
database review. Additionally, if patient follow-up occu-
rred outside our transplant institution, some of the post-
transplant thrombotic events may have been missed in
the data-capture process. We have extensive follow-up
and event reporting practices in place as dictated by the
UNOS guidelines and our own center policies. Therefore,
we estimate that the proportion of patients receiving care
outside our transplant center is very low, and missed
events even less common.
The thrombosis rate in our cohort reflects symptomatic
or clinically relevant clots (revealed in the work up of
symptoms or abnormal lab tests etc.) and therefore may
be an underestimation of the true clot burden. Clinically
insignificant clots, such as those that may be incidentally
discovered on routine imaging were not included, as
these had no clinical impact. The influence of DVT
prophylaxis with heparin products in the peri-operative
period on the subsequent development of post-operative
thrombosis is not well understood. During the study time
frame there was not a consistent DVT prophylaxis
protocol in place. Additionally, we did not have a con-
sistent policy of surveying these patients for known
hypercoagulable conditions such as Factor V Leiden
Mutations, protein C and S deficiencies, hyper-homo-
cysteinemia, etc in pre or post transplant patient nor of
consistently working up patients with PVT for these
disorders. Given the growing interest in hypercoagu-
lability in patients with liver failure and cirrhosis, a
hypercoagulable serologic work-up is appropriate in the
pre-operative setting, in order to gain a better under-
standing of the true presence of a hypercoagulable state
in this patient population. The addition of these labora-
tory tests and the prospective study of any respective
correlation in these patients will strengthen future
Notwithstanding the above limitations, there is limited
published data on this topic and the current study is
strengthened by the relatively large cohort. Additionally,
given the contemporary study time frame, the data
reflects modern day liver transplant and portal vein
thrombosis management practices, which did not exist in
previous reports in the literature. Moreover, all the
patients in the cohort were managed at a single shared
transplant center and are more likely to have had uni-
formity in pre-operative, intra-operative, and post-opera-
tive clinical management. These data suggest that post-
transplant thromboses are not contributing to a subs-
tantial clinical burden in the care of OLT recipients.
Nonetheless, it is critical for surgeons and hepatologists
to recognize the association between warm ischemia time,
DCD liver, donor gender and rejection and post-trans-
plant thromboses to ensure timely recognition and mana-
In summary, pre-transplant portal vein thrombosis was
not associated with post operative thromboses. In
addition, pre-operative portal vein thrombosis should not
preclude liver transplantation in the otherwise appro-
priate candidate. Given the current lack of consensus
opinion or evidence based practices regarding the diag-
nosis and clinical management of portal vein thrombosis,
future prospective studies are warranted to address this
clinical entity.
5. Acknowledgements
Authors’ contributions: Brintha K. Enestvedt: partici-
pated in research design, performance of research, data
analysis and manuscript preparation; C. Kristian Ene-
stvedt: participated in research design, performance of
research, data analysis and manuscript preparation Brian
Diggs: participated in statistical analysis and data
interpretation; Susan L. Orloff: participated in research
design, data analysis and manuscript preparation;
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ESLD: end stage liver disease; HCC: hepatocellular car-
cinoma; HCV: hepatitis C; MELD: model for end stage
liver disease; NASH: non-alcoholic steatohepatitis; OLT:
orthotopic liver transplant; PSC: primary sclerosing cho-
langitis; PVT: portal vein thrombosis.