Recipient Outcomes of Salvage Liver
Transplantation Versus Primary Liver
Transplantation: A Systematic Review
Zhenhua Hu,1,2,3Wei Wang,1,2,3Zhiwei Li,1,2,3Sunyi Ye,1,2,3and Shu-Sen Zheng1,2,3
1Department of Hepatobiliary and Pancreatic Surgery, First Affiliated Hospital, School of Medicine, Zhejiang
University, Hangzhou, China;2Key Laboratory of Combined Multi-Organ Transplantation, Ministry of Public
Health, First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China and3Key
Laboratory of Organ Transplantation, First Affiliated Hospital, School of Medicine, Zhejiang University,
Salvage liver transplantation (SLT), or liver transplantation after liver resection (LR), has been performed after primary LR for
many years. However, the true outcomes and risks of SLT versus primary liver transplantation (PLT) remain unclear. We per-
formed a systematic review and meta-analysis to evaluate the survival rate of SLT recipients and the incidence of postopera-
tive complications. Among 2799 screened references, 7 eligible studies were identified. The results of the meta-analysis
indicated no statistically significant differences in the overall survival rates of SLT and PLT: the pooled relative risk (RR) was
0.99 [95% confidence interval (CI) ¼ 0.90-1.09, P ¼ 0.87] at 1 year, 0.97 (95% CI ¼ 0.83-1.13, P ¼ 0.68) at 3 years, and
0.96 (95% CI ¼ 0.81-1.13, P ¼ 0.61) at 5 years. As for postoperative complications, there were no statistically significant dif-
ferences in the incidence of sepsis and biliary complications between SLT and PLT, but there was a significantly higher inci-
dence of bleeding with SLT (RR ¼ 2.84, 95% CI ¼ 1.57-5.13, P ¼ 0.001). In conclusion, the overall survival associated with
SLT is similar to that associated with PLT. Because of the limited organ donor pool, SLT might be an acceptable therapy for
patients undergoing primary LR for hepatocellular carcinoma. Liver Transpl 18:1316-1323, 2012. V
C 2012 AASLD.
Received February 13, 2012; accepted July 11, 2012.
Hepatocellular carcinoma (HCC) is the seventh most
common cancer and the third most common cause of
cancer-related deaths worldwide: it accounts for more
than 90% of primary liver neoplasms.1Liver trans-
plantation (LT) is recommended as the best option for
HCC treatment because it resects the tumor, removes
the underlying cirrhotic tissue, and restores well-bal-
anced liver function.2,3However, because of the short-
age of donated organs from both deceased and living
donors and the high incidence of HCC, the applicabil-
ity of LT as the prevailing curative therapy for HCC
worldwide is undoubtedly limited.
Recently, salvage liver transplantation (SLT), which
involves LT after primary liver resection (LR), has been
performed to meet the rising challenge of organ short-
Abbreviations: CI, confidence interval; HCC, hepatocellular carcinoma; LR, liver resection; LT, liver transplantation; PLT, primary
liver transplantation; RR, relative risk; SLT, salvage liver transplantation.
The experiments were conceived and designed by Zhenhua Hu, Wei Wang, and Shu-Sen Zheng. Zhenhua Hu, Wei Wang, Zhiwei
Li, and Sunyi Ye performed the experiments, analyzed the data, and contributed reagents, materials, and analytical tools.
Zhenhua Hu, Wei Wang, and Shu-Sen Zheng wrote the article.
This work was supported by a grant from the National Basic Research Program of China through the 973 Program
Address reprint requests to Shu-Sen Zheng, M.D., Ph.D., F.A.C.S., Key Laboratory of Combined Multi-Organ Transplantation (Ministry of Public
Health), First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China 310003. Telephone: 86-571-87236570; FAX:
86-571-87236884; E-mail: email@example.com
View this article online at wileyonlinelibrary.com.
LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases
LIVER TRANSPLANTATION 18:1316-1323, 2012
C 2012 American Association for the Study of Liver Diseases.
problem of tumor progression during the period of wait-
ing for primary liver transplantation (PLT) and thus
greatly extend the potential waiting time.5,6Neverthe-
less, little is known about SLT and especially about its
outcomes in comparison with PLT, and this is vital in-
formation for the application of this treatment.
To our knowledge, no systematic evaluation of the
survival rate of SLT recipients or the incidence of
complications has previously been performed. The
primary aim of this study was, therefore, to conduct a
comprehensive meta-analysis comparing the short-
and long-term survival rates and incidence of compli-
cations for SLT and PLT patients. In addition to aiding
in the assessment of the feasibility of SLT and its indi-
cations, the findings of this study may inform clinical
practice and help in the development of reasonable
guidelines for the management of patients with HCC.
MATERIALS AND METHODS
Data Sources and Search Strategy
To identify relevant studies and reports, we searched
PubMed, Embase, and the Cochrane Library with com-
binations of the following terms: salvage*; secondary*;
transplantation, liver; liver transplantations; transplan-
tations, liver; transplantation, hepatic; grafting, liver;
liver grafting; hepatic grafting; hepatic transplantation;
hepatic transplantations; transplantations, hepatic; and
liver transplantation. Studies were limited to those
involving humans and published in English between
1990 and the first week of June 2011. We checked the
reference lists of identified review articles, meta-analy-
ses, and original studies to obtain further eligible data.
We also searched for clinical trials in the databases of
the National Institutes of Health, the European Liver
Transplant Registry, and the Scientific Registry of
Transplant Recipients. When articles did not report all
the types of data necessary for this analysis, we con-
tacted the authors via e-mail for additional information.
A priori, we established the following inclusion criteria
for eligible trials:
1. Trials should include recipients with HCC who
underwent SLT (ie, LR followed by secondary
2. Trials should include comparisons of PLT and
SLT groups with respect to survival rates or the
incidence of complications with follow-up exceed-
ing 1 year.
3. Recipients must have been selected on clinical
grounds with no restriction on the number of
4. If multiple articles reported the same trial, the
most informative report with respect to the
study’s aims was to be chosen.
We excluded patients with extrahepatic metastases
and major vascular invasion and patients who under-
went SLT or PLT as part of a multiorgan transplant
(eg, liver-kidney transplantation) or whose age was
greater than 70 years at the time of transplantation.
Data Extraction and Quality Assessment
extracted data from all selected articles and stored
them in a customized database. Disagreements were
adjudicated by re-evaluation and consensus. Another
extracted data and was responsible for their accuracy.
Additionally, all extracted data and calculations were
double-checked. For all eligible articles, the following
data were extracted from the original publications: the
first author; the country of origin; the year of publica-
tion; the trial scales; the mean age of the recipients;
the duration of follow-up; the overall 1-, 3-, and
5-year survival rates; and the incidence of postopera-
tive complications (eg, bleeding, sepsis, and biliary
complications). Data that were not directly reported
were calculated or obtained indirectly from the origi-
nal study when they were available.
We assessed the risk of bias in trials according to
the recommendations of the Cochrane Collaboration.7
All selected studies came from the published litera-
ture, and no further ethics approval was required.
Statistical Analysis and Quantitative Data
Our systematic review and meta-analysis were per-
formed according to a recommended protocol that was
consistent with the Meta-Analysis of Observational
Studies in Epidemiology consensus statement and the
Preferred Reporting Items for Systematic Reviews and
Meta-Analyses statement.8,9All analyses were con-
ducted with Stata 10.0 (Stata, College Station, TX).
Heterogeneity across studies was assessed with the I2
statistic, which is the proportion of the total variation
across studies attributable to heterogeneity rather than
sampling error.10,11We chose a fixed effects model (the
Mantel-Haenszel method) to calculate estimates with
low heterogeneity and a random effects model (the
DerSimonian-Laird method) when there was high het-
erogeneity (I2> 50%). Relative risk (RR) was used for
the analysis of dichotomous variables. A sensitivity
analysis was performed to assess the reliability of the
results of both the random effects and fixed effects
models. When it was possible, a meta-regression was
performed to further evaluate heterogeneity between
study results.12Egger’s test (Stata 10.0) was used to
evaluate the potential risk of small study effects (eg,
publication bias).13A 2-tailed P value < 0.05 was con-
sidered to indicate a statistically significant difference.
Flow of the Included Studies
The database searches identified 2779 references for
evaluation, and we obtained 185 references from
LIVER TRANSPLANTATION, Vol. 18, No. 11, 2012HU ET AL. 1317
reference lists for further assessment. Nineteen articles
were included, but 10 were subsequently excluded
because of a lack of available data or information for
analysis. Two of the remaining 9 articles14,15were sub-
sequently excluded because they did not meet the
inclusion criteria. These studies had transplant sur-
vival data only for patients with recurrent HCC and
definitely excluded LT for patients with other indica-
tions such as liver failure. The remaining 7 articles,16–22
which were all observational, retrospective cohort stud-
ies, were included in the meta-analysis (Fig. 1). No
randomized controlled trials were found, and this was
likely a result of ethical limitations; this means that
they are unlikely to be performed.
The baseline characteristics of the 7 eligible studies
(which were published between 2003 and 2009)16–22
are provided in Table 1. Three of these studies were
performed in France, 2 were performed in Korea, 1
was performed in Italy, and 1 was performed in
Spain. The ratio of SLT and PLT patients varied from
0.085 to 0.483.
Overall Survival Outcomes of Recipients
The 1-, 3-, and 5-year overall survival rates were cal-
culated from the transplant data and were compared
for the SLT and PLT recipients. A sensitivity analysis
was conducted to confirm the reliability of the calcu-
lated outcomes, and Egger’s test was used to indicate
any potential publication bias. The results of the
meta-analysis of the overall survival rates are pre-
sented in Table 2 and Fig. 2.
Six studies16,17,19–22compared the 1-year overall
survival rates of SLT and PLT recipients. Homogeneity
tests with a fixed effects model revealed no evidence
of heterogeneity across studies (I2¼ 0.0%, P ¼ 0.75).
The meta-analysis with a fixed effects model showed
Flow diagram of the process for identifying the
TABLE 1. Characteristics of the Eligible Studies Included in This Meta-Analysis
Description of SLT at the Time
Belghiti et al.21
55 6 10
53 6 7
15 for tumor recurrence and 3 for
de principle LT
Margarit et al.17
59.9 6 7.6
5 for tumor recurrence and 1 for liver failure
Hwang et al.20
49.3 6 8.6
51.2 6 7.0
2.6 6 2.2
3.3 6 1.9
15 for tumor recurrence and 2 for liver failure
Del Gaudio et al.22
2.2 6 2.2
3.0 6 2.7
10 for tumor recurrence and 6 for liver failure
Kim et al.16
48.1 6 7.0
51.2 6 6.2
1.5 6 0.7
1.6 6 0.6
13 for tumor recurrence and 2 for liver failure
Scatton et al.19
53.5 6 8.0
14 for tumor recurrence and 6 for
de principle LT
Cherqui et al.18
16 for tumor recurrence and 2 for bridge LT
NOTE: All studies were observational.
1318HU ET AL.LIVER TRANSPLANTATION, November 2012
that the pooled RR was 0.99 [95% confidence interval
(CI) ¼ 0.90-1.09], which was not statistically signifi-
cant (P ¼ 0.87). A low level of sensitivity was revealed
by a sensitivity analysis, which produced the same
result (I2¼ 0.0%, P ¼ 0.75) as the random effects
model. Egger’s test suggested that there was no evi-
dence of publication bias (P ¼ 0.66).
Four studies19–22compared the 3-year overall sur-
vival rates of SLT and PLT recipients. Homogeneity
tests with a fixed effects model showed no evidence of
heterogeneity across studies (I2¼ 0.0%, P ¼ 0.78). A
sensitivity analysis revealed a low level of sensitivity
(I2¼ 0.0%, P ¼ 0.78) with a random effects model. It
was reasonable to perform the meta-analysis with a
fixed effects model, from which a statistically non-
significant pooled RR of 0.97 (95% CI ¼ 0.83-1.13, P
¼ 0.68) was obtained. Egger’s test suggested that
there was no evidence of publication bias (P ¼ 0.61).
Six studies17–22compared the 5-year overall survival
rates of SLT and PLT recipients. Homogeneity tests
with a fixed effects model showed no evidence of heter-
ogeneity across studies (I2¼ 0.0%, P ¼ 0.45). We also
recalculated the meta-analysis with a random effects
model and obtained the same result (I2¼ 0.0%, P ¼
0.45), and we thus concluded that the sensitivity was
low. It was reasonable to perform the meta-analysis
with a fixed effects model, from which a pooled RR of
0.96 (95% CI ¼ 0.81-1.13, P ¼ 0.61) was calculated.
Egger’s test suggested no evidence of publication bias
(P ¼ 0.99). However, because of the insufficient
amount of data and number of studies, it was not pos-
sible to perform a meta-regression analysis.23
We also performed a meta-analysis of the overall
survival rates with all 9 articles (ie, we included those
articles that were excluded because of the inclusion
criteria as mentioned previously). The results of this
analysis (data not shown) were similar to the results
of the analysis of the 7 included studies.
Incidence of Postoperative Complications in
We collected reports regarding several primary compli-
cations after LT for the meta-analysis. Bleeding,
sepsis, and biliary complications were chosen as pa-
rameters for the subgroup analysis because sufficient
data were available for them. Homogeneity testing of
the bleeding, sepsis, and biliary complication sub-
groups showed coherent results (see Table 2 and Fig.
3 for more details). All subgroup analyses were per-
formed with a fixed effects model.
The incidenceof bleeding
articles,16,20,21for which the pooled RR was 2.84
(95% CI ¼ 1.57-5.13); it was statistically significant (P
¼ 0.001). Two studies20,21reported the incidence of
sepsis (pooled RR ¼ 0.98, 95% CI ¼ 0.53-1.81), and 4
studies16,20–22reported biliary complications (pooled
RR ¼ 1.28, 95% CI ¼ 0.77-2.13). The pooled RR val-
ues for the sepsis and biliary complication subgroups
were not statistically significant (P > 0.05; Table 2).
The sensitivity analysis for all complication subgroups
revealed a low level of sensitivity.
LR and LT are now widely considered to be comple-
mentary treatments (rather than competitive ones) for
HCC in patients with cirrhosis and well-preserved
liver function.24–26Salvage transplantation after pri-
mary LR is regarded as a reasonable strategy for
patients with HCC.6As a result of the uncertainty
about the outcomes of SLT and PLT recipients, there
is a debate concerning the optimal treatment of HCC
patients with cirrhosis. This is the first meta-analysis
to comprehensively review the relevant literature in
order to specifically compare the survival rates and
postoperative complications of SLT and PLT recipi-
ents. We have found that SLT is feasible and safe in
terms of overall survival rates after transplantation,
and the rates of postoperative complications are com-
parable to those associated with PLT, except that the
bleeding rate is higher with SLT.
The first consideration regarding SLT is its impact
on the posttransplant survival rate in comparison with
PLT. Since SLT was first proposed by Majno et al.27
with encouraging results, series of trials have been
performed to explore the validity of this approach. Two
early series of clinical case studies by Adam et al.14
TABLE 2. Summary of the Meta-Analysis Results
RR (95% CI)
*Included biliary strictures or fistulas that required intervention or reoperation.
LIVER TRANSPLANTATION, Vol. 18, No. 11, 2012 HU ET AL.1319
and Belghiti et al.21reported conflicting results. The
first study showed that the rates of survival after SLT
were inferior to those after PLT, whereas the latter
study indicated that the survival rates of SLT and PLT
group,14the poor outcomes after SLT were primarily
due to high operative mortality rates and intraoperative
bleeding, which may have been related to technical
similar.In the report by thePaul-Brousse
survival rates in the individual
studies and the pooled population
(fixed effects model): (A) 1-, (B) 3-,
and (C) 5-year overall survival
rates. The percentages presented
for the weights in parts A and B
do not add up to exactly 100
because of rounding.
1320HU ET AL.LIVER TRANSPLANTATION, November 2012
difficulties during LT. Furthermore, all patients in
Adam et al.’s study underwent LT because of HCC re-
currence, whereas only 61% of the 18 patients in the
study by Belghiti et al. had morphological evidence of
recurrence. This may have also resulted in the different
comparative results. According to the combined results
of the 7 studies selected for our meta-analysis, primary
LR before LT did not impair overall survival rates in
comparison with PLT alone at 1, 3, and 5 years after
In addition, these outcomes should be reconsidered
on the basis of the Milan criteria for the threshold of
resection; the Milan criteria state that transplantation
is indicated if there is a single lesion < 5 cm in size or
there are no more than 3 lesions with the largest ? 3
cm in size.24Traditionally, it has been accepted that
SLT (including PLT) should be proposed for recipients
who meet the Milan criteria.28Recently, some promis-
ing results after PLT and SLT have been reported for
HCC patients who exceed the Milan criteria.19,29–32
of postoperative complications in
the individual studies and the
pooled population (fixed effects
model): (A) bleeding, (B) sepsis,
and (C) biliary complications. The
weights in part A do not add up to
exactly 100 because of rounding.
RRs for the incidence
LIVER TRANSPLANTATION, Vol. 18, No. 11, 2012 HU ET AL. 1321
Kaido et al.5claimed that the Kyoto criteria (?10
tumors with all ? 5 cm in diameter and serum des-
gamma-carboxy prothrombin levels ? 400 mAU/mL)
were also effective for the selection of patients for SLT
because the same results were found for SLT and PLT
recipients in terms of overall survival rates. This
might indicate that the criteria for the selection of
patients for SLT require redefinition. Indeed, the Mi-
lan criteria, which appear to be the first-line selection
standard advocated and validated by many transplant
centers,33are inevitably restricted by the low sensitiv-
ity and accuracy of morphological assessments.
However, some patients dropped from the waiting
list because their tumors progressed during this time.
For example, recipients with HCC that met the Milan
criteria had a decreased 3-year survival rate (from
80% to 60%) as a result of this dropout. It has been
advanced HCC beyond the Milan criteria who are
waiting for PLT will drop out.34Our analysis suggests
that whatever the HCC stage is, the overall survival
rates of SLT and PLT patients are similar. It is unrea-
sonable to exclude such patients from the waiting list
on the basis of the Milan criteria at present. Further-
more, some authors have reported that LR can help to
downgrade HCC, and this could reduce the existing
waiting-list time and provide more opportunities for
increasing the number of patients on the waiting list.
Therefore, patients who have undergone LR and
patients who have not undergone LR should have an
equal right to organ allocation. Besides the question
of organ allocation, SLT may offer a potential advant-
age as an alternative approach by enabling the better
selection of patients who will benefit more from LT.15
The second concern regarding SLT is the rate of
postoperative complications. Adhesions between the
cut surface from a previous LR and the omentum or
intestine are the main technical difficulties encoun-
tered. However, a recent study suggested that sharp
dissection and meticulous hemostatic control would
reduce the difficulty of repeated surgery and decrease
the incidence of postoperative complications.16Our
meta-analysis shows that the risks of sepsis and bili-
arycomplications are similar
patients, but there is an increased risk of bleeding
with SLT. One explanation for this finding is that
transplantation procedures after previous upper ab-
because of vascular adhesions and a degree of portal
hypertension. Another possible reason is a publica-
tion bias: authors might be more willing to share their
successful experiences than their experiences with
high levels of complications. Laurent et al.35showed
that adhesions are reduced if the initial LR is per-
formed laparoscopically, and this suggests a new way
to decrease the incidence of complications in SLT.
Several limitations of our meta-analysis should be
considered. The first limitation is the lack of randomized
controlled trials; this could not be avoided because of
limited resources and ethical restrictions. Second, the
number of high-quality studies was insufficient for more
detailed subgroup analyses. For example, only 1 article
included information on disease-free survival. Finally,
fewer than 10 trials were involved in our meta-analysis,
and thus we failed in our intention to investigate meth-
odological differences as a source of heterogeneity.
In conclusion, our analysis demonstrates that SLT
after primary LR is a safe procedure with overall sur-
vival rates similar to those associated with PLT.
Because of the shortage of donor organs, SLT might
be accepted as a good alternative for the treatment of
patients with HCC.
The authors gratefully acknowledge Mrs. Mingjuan Jin
(Department of Statistics, Zhejiang University) for her
assistance with the statistical analysis and Dr. Jie Zhou
(Department of Hepatobiliary and Pancreatic Surgery,
First Affiliated Hospital, Zhejiang University School of
Medicine) for his help with the data collection.
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