Abstract
Background
Vascular complications commonly cause graft loss and morbidity after liver transplantation (LT). Comparative data on the risk of vascular complications are limited. Hence, the present meta-analysis was conducted to analyze the difference in vascular complications between living-donor LT (LDLT) and deceased-donor LT (DDLT).
Methods
A literature search of three databases was conducted for studies comparing the incidence of vascular complications with LDLT and DDLT. The event rates and odds ratios (OR) with 95% confidence intervals (CI) were calculated using a random-effects model.
Results
A total of 20 studies were included in the final analysis. There was no difference in the incidence of overall vascular complications (9.3%, 95% CI: 6.6–12.0 vs. 8.5%, 95% CI: 5.6–11.4) between LDLT and DDLT with OR 0.94 (95% CI: 0.73–1.21) (15 studies).There was a higher incidence of vascular complications with LDLT in older studies (published before 2013) but not in new studies. When comparing the individual complications, LDLT was associated with a higher incidence of hepatic artery thrombosis (HAT) (3.8%, 95% CI: 2.4–5.2 vs. 1.6%, 95% CI: 1.1–2.2)with OR 2.20 (95% CI: 1.53–3.17) (14 studies)and a significantly lower incidence of intra-abdominal bleeding(4.8%, 95% CI: 3.3–6.2 vs. 7.9%, 95% CI: 5.0–10.7) with OR 0.64 (95% CI: 0.47–0.87) (11 studies). However, there was no difference in the incidence (2.1%, 95% CI: 0.5–3.8 vs. 1.0%, 95% CI: 0.1–1.9) of portal vein thrombosis between LDLT and DDLT with OR 1.85 (95% CI: 0.82–4.18) (6 studies).
Conclusion
Despite a comparable risk of vascular complications between LDLT and DDLT, LDLT was associated with a higher risk of HAT and a lower risk of intraprocedural bleeding. Further studies are required to analyze the effect of donor-recipient characteristics and surgical techniques on the risk of vascular complications.
Keywords: liver cirrhosis, liver transplantation, portal vein thrombosis, hepatic artery thrombosis, bleeding
Liver transplantation (LT) provides a curative option for patients with decompensated cirrhosis of the liver and hepatocellular carcinoma (HCC), along with other rare indications.1 With the increasing number of patients with decompensated cirrhosis and HCC, there is a scarcity of organ availability for deceased donor LT (DDLT).2 After starting living donor LT (LDLT) programs in various countries, there has been a reduction in waitlist mortality as it addresses the growing disparity between organ supply and demand.3 However, LDLT has its own share of disadvantages and has been reported to have a higher risk of biliary complications.4
Vascular complications after LT are associated with significant morbidity in the form of surgical re-exploration, graft failure, re-transplantation, and mortality.5 A recent meta-analysis comparing the outcome of LDLT and DDLT analysed data from 7 studies and reported no difference between the two groups with respect to the risk of hepatic artery thrombosis (HAT) (OR 2.07, 95% CI: 0.84–5.09).6 However, another meta-analysis analysing data from six studies reported a significantly higher rate of vascular complication with LDLT (OR 2.00, 95%CI: 1:31–3.07).7 In both meta-analyses, vascular complications were not the primary outcome and, hence, were limited by the number of studies reporting vascular complications.
Early identification and management of vascular complications may improve the outcome of LT while reducing morbidity. Hence, we aimed to compare the incidence and risk of overall and individual vascular complications associated with LDLT and DDLT and the associated factors.
METHODS
Information Sources and Search Strategy
A comprehensive search was conducted using the databases of MEDLINE, EMBASE, and Scopus from inception to August 2023. The keywords used were: (Liver OR Hepat∗ OR HCC OR Cirrhosis) AND (LDLT OR Live donor OR Living donor) AND (DDLT OR Deceased donor OR Cadaveric) AND (Vascular OR Arter∗ OR Venous OR Thrombosis OR Bleed∗). Manual searching of reference lists of the included studies was also undertaken to ensure that all potentially relevant studies were included. The systematic review and meta-analysis was conducted as per the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) guidelines.8
Study Selection
All prospective and retrospective studies fulfilling the following PICO criteria were included: (a) Patients – patients with decompensated cirrhosis of the liver undergoing LT; (b) Intervention – LDLT; (c) Comparison – DDLT; (d) Outcomes – vascular complications. In accordance with the selection criteria above, the titles and abstracts of all studies were independently reviewed by two authors. In the event of any disagreement, the opinion of the third reviewer was taken to resolve the same. Non-comparative studies, conference abstracts, case series, and exclusive pediatric studies were excluded from the analysis.
Definition of Outcomes
Vascular complications included both thrombosis and bleeding. Thrombotic events included the development of HAT or portal vein thrombosis (PVT). Bleeding complications included the development of intraprocedural or early postprocedural bleeding requiring intervention.
Data Extraction and Quality Assessment
Two reviewers independently extracted the data, while a third reviewer arbitrated any conflicts. Each study's title, first author, year of publication, country, the number of patients, age and sex distribution, indication for TIPS, outcome metrics, and follow-up time were all listed on the form. Using a Newcastle–Ottawa scale for cohort studies,9 two independent reviewers evaluated the quality of the included studies. In the event of any disagreement, the opinion of the third reviewer was sought.
Statistical Analysis
Odds ratios (OR) with 95% confidence intervals (CI) were calculated for all the dichotomous outcomes. Regardless of heterogeneity, the Mantel–Haenszel test for random effects was used. A Cochran's Q test and I2 statistics were used to determine the heterogeneity between the studies. A P-value of Q test <0.1 or the I2 value > 30% was significant. Publication bias was assessed by visual inspection of the funnel plot. A leave-one-out meta-analysis was conducted for sensitivity analysis. RevMan software (version 5.4.1, Cochrane Collaboration) and STATA software (version 17, StataCorp., College Station, TX) were used for statistical analysis.
RESULTS
Study Characteristics and Quality Assessment
The above search strategy yielded 2910 records, out of which20 studies were included in the final analysis.10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29 Figure 1 shows the PRISMA flowchart for the study selection and inclusion process. The summary of the baseline characteristics of the patients in individual studies included in the systematic review and meta-analysis has been provided in Table 1. All the studies were retrospective in nature. Thirteen studies were from Asian countries,10,13, 14, 15, 16, 17,19,20,23, 24, 25,27,29 while the rest were from North America.11,12,18,21,22,26,28 Three studies included some pediatric patients,10,13,15 while the rest included adult patients exclusively. Four studies included patients with HCC exclusively.17,19,20,26 Nine studies were of good quality,13,14,16, 17, 18, 19,23,27,29 ten studies were of fair quality,10, 11, 12,15,20, 21, 22,24,26,28 and one was of poor quality.25
Figure 1.
PRISMA flowchart for study identification, screening, and inclusion process.
Table 1.
Baseline Characteristics of the Studies Included in the Meta-analysis.
| Author, year | Country, No. of centers |
Design | Arm | No. of patients | Age, in years | Male sex | MELD score | Patients with HCC | Study quality |
|---|---|---|---|---|---|---|---|---|---|
| Al-Sebayel 200710 | Saudi Arabia, Single |
Retrospective | LDLT | 45 | 47 (1.5–63) | 29 (64.4%) | – | 21 (17%) | Fair |
| DDLT | 77 | 44 (11–63) | 38 (49.3%) | – | |||||
| Freise 200811 | USA, Multicentric |
Retrospective | LDLT | 384 | 49.6 ± 10.7 | 222 (58%) | 15 ± 6 | 63 (16%) | Fair |
| DDLT | 216 | 51.4 ± 9.7 | 128 (59%) | 21 ± 9 | 39 (18%) | ||||
| Lai 200912 | USA, Single |
Retrospective | LDLT | 86 | 50.6 ± 12.2 | 42 (49%) | 20.5 ± 5.1 | 31 (36%) | Fair |
| DDLT | 403 | 53.6 ± 10.8 | 289 (72%) | 23.0 ± 9.8 | 126 (31%) | ||||
| Khalaf 201013 | Saudi Arabia, Single |
Retrospective | LDLT | 69 | 49 (1.5–63) | 48 | – | – | Good |
| DDLT | 155 | 45 (11–73) | 88 | – | – | ||||
| Li 201114 | China, Single |
Retrospective | LDLT | 128 | 42.96 ± 8.57 | 108 | 19.5 ± 10.7 | 0 | Good |
| DDLT | 221 | 44.55 ± 9.71 | 179 | 18.2 ± 9.6 | 0 | ||||
| Saha 201215 | India, Single |
Retrospective | LDLT | 18 | 21.6 (0.5–61) | – | – | 0 | Fair |
| DDLT | 35 | 35.2 (1.2–63) | – | – | 0 | ||||
| Jiang 201316 | China, Single |
Retrospective | LDLT | 70 | 40.2 ± 8.1 | 62 (88.6%) | 23.9 ± 5.6 | 0 | Good |
| DDLT | 191 | 44.1 ± 9.3 | 162 (84.8%) | 21.7 ± 5.7 | 0 | ||||
| Lei 201317 | China, Single |
Retrospective | LDLT | 31 | 44.4 ± 9.7 | 18 (58.1%) | 9.3 ± 6.1 | 31 (100%) | Good |
| DDLT | 52 | 44.0 ± 8.2 | 31 (59.6%) | 9.1 ± 5.8 | 52 (100%) | ||||
| Reichman 201318 | Canada, Single |
Retrospective | LDLT | 145 | 54.2 ± 7.5 | 117 (80.7%) | 14.4 (6–29) | 55 (37.9%) | Good |
| DDLT | 145 | 53.9 ± 7.7 | 117 (80.7%) | 14 (6–33) | 80 (55%) | ||||
| Wan 201419 | China, Single |
Retrospective | LDLT | 40 | 48.6 ± 9.7 | 34 (85%) | 6-19: 87.5% | 40 (100%) | Good |
| DDLT | 80 | 49.5 ± 8.9 | 68 (85%) | 6-19: 88.7% | 80 (100%) | ||||
| Hu 201620 | China, Multicenter |
Retrospective | LDLT | 389 | 48.0 ± 8.6 | 360 (92.5%) | – | 389 (100%) | Fair |
| DDLT | 6471 | 50.1 ± 9.4 | 5817 (89.9%) | – | 6471 (100%) | ||||
| Samstein 201621 | USA, Multicenter |
Retrospective | LDLT | 565 | 51.0 ± 10.9 | 311 (55%) | – | 70 (12%) | Good |
| DDLT | 471 | 52.2 ± 10.4 | 285 (61%) | – | 103 (22%) | ||||
| Barbas 201722 | Canada, Multicenter |
Retrospective | LDLT | 48 | 54.7 ± 9.4 | 35 (72.9%) | 17.8 ± 8.7 | 8 (16.7%) | Fair |
| DDLT | 128 | 56.7 ± 9.3 | 87 (68.0%) | 21.8 ± 10.3 | 42 (32.8%) | ||||
| Chok 201723 | China, Single |
Retrospective | LDLT | 54 | 51 (19–67) | 42 (77.8%) | 40 (35–40) | 3 (5.5%) | Good |
| DDLT | 40 | 51 (23–66) | 34 (85%) | 39 (35–40) | 1 (2.5%) | ||||
| Kim 201724 | South Korea, Single |
Retrospective | LDLT | 109 | 52.0 ± 8.5 | 81 (74.3%) | 12.5 ± 8.3 | 68 (62.4%) | Fair |
| DDLT | 76 | 53.1 ± 11.0 | 50 (65.8%) | 24.9 ± 11.7 | 16 (21.1%) | ||||
| Miyagi 201725 | Japan, Single |
Retrospective | LDLT | 168 | – | – | – | – | Poor |
| DDLT | 441 | – | – | – | – | ||||
| Humar 201926 | USA, Single |
Retrospective | LDLT | 245 | 56 | 144 (59%) | 16 | 54 (22%) | Fair |
| DDLT | 592 | 56 | 414 (70%) | 22 | 213 (36%) | ||||
| Wong 201927 | China, Single |
Retrospective | LDLT | 188 | 55 (30–73) | 152 (80.8%) | 11.4 (6–45) | 188 (100%) | Good |
| DDLT | 187 | 56 (31–68) | 158 (84.5%) | 12.4 (6–27) | 187 (100%) | ||||
| Amara 202228 | USA, Multicenter |
Retrospective | LDLT | 109 | – | 57 (52.3%) | – | 17 (15.6%) | Fair |
| DDLT | 1684 | – | 1135 (67.4%) | – | 561 (33.3%) | ||||
| Lapisatepun 202329 | Thailand, Multicenter |
Retrospective | LDLT | 20 | 54.7 ± 11.7 | 14 (70%) | 14.5(12–23.5) | 11 (55.0%) | Good |
| DDLT | 20 | 48.8 ± 14.3 | 14 (70%) | 14.5(7.5–22.5) | 14(70.0%) |
DDLT, Deceased-donor liver transplantation; HCC, Hepatocellular carcinoma; LDLT, living-donor liver transplantation.
Overall Vascular Complications
A total of 15 studies with 12,251 patients compared the risk of vascular complications between LDLT and DDLT.10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20,25, 26, 27, 28 The pooled incidence of vascular complications with LDLT and DDLT was 9.3% (95% CI: 6.6–12.0; I2 = 87.3%) vs. 8.5% (95% CI: 5.6–11.4; I2 = 97.6%), respectively. There was no difference in the odds of vascular complications between LDLT and DDLT with OR 0.94 (95% CI: 0.73–1.21; I2 = 0%). On subgroup analysis based on the year of publication, the pooled analysis of studies published before 2013 showed a higher risk of vascular complications with LDLT with OR 1.57 (95% CI: 1.08–2.27; I2 = 1%) but not with studies after 2013 (OR 0.95, 95% CI: 0.75–1.19; I2 = 0%) (Figure 2).
Figure 2.
Forest plot comparing the risk of vascular complications between live-donor and deceased-donor liver transplantation, with subgroup analysis based on the year of publication (before 2013 vs. in or after 2013).
Hepatic Artery Thrombosis
Overall, 14 studies (n = 4728) compared the risk of HAT between LDLT and DDLT.11,13, 14, 15, 16, 17, 18, 19,21,24, 25, 26,29 The pooled incidence of HAT with LDLT and DDLT was 3.8% (95% CI: 2.4–5.2; I2 = 55.9%) vs. 1.6% (95% CI: 1.1–2.2; I2 = 24.0%), respectively. LDLT was associated with significantly higher odds of HAT with OR 2.20 (95% CI: 1.53–3.17; I2 = 0%), without any heterogeneity. A subgroup analysis based on the year of publication also reported a higher risk of HAT with LDLT (Figure 3A).
Figure 3.
Forest plot comparing the risk of (A) hepatic artery thrombosis with subgroup analysis and (B) portal vein thrombosis between live-donor and deceased-donor liver transplantation.
Portal Vein Thrombosis
Only 6 studies (n = 2353) reported the risk of PVT with LDLT and DDLT.11,13, 14, 15,18,25 The pooled incidence of PVT with LDLT and DDLT was 2.1% (95% CI: 0.5–3.8; I2 = 89.1%) vs. 1.0% (95% CI: 0.1–1.9; I2 = 86.3%), respectively. There was no difference in the odds of PVT between LDLT and DDLT with OR 1.85 (95% CI: 0.82–4.18; I2 = 18%) (Figure 3B).
Intra-abdominal Bleeding
Overall, 11 studies (n = 11,452) compared the risk of intra-abdominal bleeding between LDLT and DDLT.11,16, 17, 18, 19, 20, 21,23,24,27,29 The pooled incidence of intra-abdominal bleeding with LDLT and DDLT was 4.8% (95% CI: 3.3–6.2; I2 = 75.4%) vs. 7.9% (95% CI: 5.0–10.7; I2 = 97.6%), respectively. LDLT was associated with significantly lower odds of intra-abdominal bleeding with OR 0.63 (95% CI: 0.49–0.81; I2 = 0%), without any heterogeneity (Figure 4). On subgroup analysis, the risk of bleeding was lower with LDLT in studies that included mixed patients OR 0.59 (95% CI: 0.44–0.79; I2 = 0%) but comparable in studies that included only HCC patients OR 0.77 (95% CI: 0.42–1.41; I2 = 7%).
Figure 4.
Forest plot comparing the risk of intra-abdominal bleeding between live-donor and deceased-donor liver transplantation with subgroup analysis based on the indication (exclusively patients with hepatocellular carcinoma vs. mixed patients).
Publication Bias and Sensitivity Analysis
Visual inspection of the funnel plot did not show any evidence of publication bias for any of the outcomes.On sensitivity analysis of studies exclusively in adult patients, there was no significant change in the overall effect size.
DISCUSSION
Vascular complications are a common cause of morbidity and mortality in patients after LT. Our study included a total of 19 studies with 14,596 patients and compared vascular complications, including HAT, PVT, and intra-abdominal bleeding between LDLT and DDLT. Overall, there was no difference in vascular complications irrespective of type of LT, being 9.3% in the LDLT group and 8.5% in the DDLT group. However, on sub-group analysis, a striking difference in vascular complications was noted between the studies published before 2013, as compared to the studies after 2013, with a higher incidence of vascular complications with LDLT in studies before 2013. Though not mentioned specifically, the lower rate of overall vascular complications in the later studies may result from improvement in the surgical techniques.28,29
Thrombosis of the hepatic artery is a devastating complication following LT. It can be early HAT (diagnosed <7 days after LT) or late HAT (7–28 days after LT). While early HAT leads to graft dysfunction necessitating surgical/radiological intervention or rarely re-transplantation, late HAT is usually less devastating and associated with biliary complications.30 A previous meta-analysis of retrospective studies by Barbetta et al. comparing survival between DDLT vs. LDLT reported no difference in the odds of HAT (OR 2.07, 95% CI: 0.84–5.09). However, the current meta-analysis reported a higher incidence of HAT in patients following LDLT. This difference may be due to the fact that Barbetta et al. had HAT as a secondary outcome and, thus, included only seven studies for the assessment of HAT. The higher incidence of hepatic arterial complications in LDLT is probably due to the smaller hepatic artery of the graft (necessitating extensive dissection of the recipient hepatic artery) as compared to the hepatic artery of the whole liver in DDLT.5 Moreover, the recipient hepatic artery in an individual with portal hypertension with HCC may be already dilated or compromised due to various intervention radiology procedures (e.g., chemoembolization/radioembolization).In such a scenario, extensive dissection of these arteries may further increase the risk of HAT in the LDLT scenario.
Concerning the surgical techniques and patient characteristics that can predict HAT, Oh et al. reported that arterial anastomosis to an old conduit, recipient/donor weight ratio >1.25, and cytomegalovirus mismatch (seropositive donor liver in seronegative recipient) were the independent predictors of early HAT.30 A subsequent systematic review of risk factors associated with early HAT reported cytomegalovirus mismatch, prior transplantation, arterial conduits, prolonged operation time, low recipient weight, variant arterial anatomy, and low-volume transplantation centers as predictors.31 Yang et al. showed that recipient/donor weight ratio ≥1.15, duration of hepatic artery anastomosis more than 80 min, ≥7 units of intraoperative blood transfusion, and postoperative blood transfusions were independent predictors of early HAT, while an operation time >10 h independently predicted late HAT.32 Mourad et al. reported that a higher number of arterial anastomoses was associated with early HAT, the recipient age <50 years was associated with late HAT, and a low donor weight was an independent predictor of both early as well as late HAT.33 Lastly, MELD score and warm ischemia time independently predicted HAT as per Pinto et al.34 In the present analysis patients in the LDLT group had a higher risk of HAT despite a lower MELD score compared to the DDLT group. However, the effect of other factors could not be performed in the present analysis due to the unavailability of data regarding the same.
The current meta-analysis also analyzed the risk of PVT in LDLT as compared to DDLT. Only six studies analysed the difference in risk. Historically, LDLT, split LT, and pediatric LT have been associated with a higher risk of PVT.35,36 The common causes of PVT following LT include venous redundancy and kinking and/or stenosis of anastomosis.37 Other risk factors include prior surgery on portal and splanchnic venous system,pre-transplant PVT, hypoplasia of PV, and use of venous conduits for PV reconstruction.37,38 However, in this meta-analysis, no significant difference in incidence of PVT was noted between DDLT and LDLT. This paradoxical finding can be explained by the significant improvement in surgical techniques over the last decades.
Finally, the incidence of post-LT intra-abdominal bleeding was found to be higher following DDLT as compared to LDLT. The risk factors associated with post-LT intra-abdominal bleeding include prolonged cold ischemia time (as seen in DDLT) and sicker patients (e.g., patients with higher Child-Pugh scores in DDLT).39 In agreement with our study, another meta-analysis by Tang et al. also compared post-operative outcomes between DDLT and LDLT. They included six studies that compared the risk of post-LT intra-abdominal bleeding. In this study, pooled results with a fixed effect model revealed that the intra-abdominal bleeding rate was significantly lower in LDLT as compared to DDLT (OR = 0.64, 95%CI: 0.46–0.88).7 On subgroup analysis, the risk of bleeding with LDLT was in studies that included mixed patients OR 0.59 (95% CI: 0.44–0.79) but comparable in studies that included only HCC patients OR 0.77 (95% CI: 0.42–1.41). This difference may be due to the fact that HCC patients undergoing LT had a lower MELD score compared to those undergoing LT for advanced cirrhosis.
Our study, nevertheless, had few limitations. First, most of the studies included in this meta-analysis were retrospective. However, none of the previous meta-analyses have specifically looked into vascular complications following LT. Also, we included a higher number of studies to mitigate some of these limitations. Future prospective studies or individual patient data meta-analyses are required to reduce the limitations of retrospective analyses and analyze the independent risk factors for vascular complications. Second, we did not analyze other vascular complications following LT (e.g., hepatic vein thrombosis, hepatic artery stenosis).However, these are relatively uncommon complications following LT, and available literature is also scarce. Finally, patients with HAT and PVT were not sub-classified and analyzed separately in our study. This limitation is particularly important, e.g., patients with early HAT may have a fulminant clinical course compared to late HAT. Early identification and prompt treatment of early HAT are essential to salvage the patient.
To conclude, ours is the first meta-analysis that specifically compared vascular complications following LT. With improvement in surgical techniques, most vascular complications (PVT and abdominal bleeding) have been significantly reduced following LDLT as compared to DDLT. However, HAT (the most life-threatening vascular complication) still remains higher following LDLT as compared to DDLT, while the incidence of periprocedural bleeding was significantly lower with LDLT. These factors should be considered while following up with patients after LT, and patients should be closely monitored so that early intervention can be planned in case of complications.
Credit authorship contribution statement
Conceptualization: SG, VM, DLP; Data curation: SG, PN, SKS, BM, DLP; Formal analysis: SG, DLP; Funding acquisition: N/A; Investigation: SG, DLP; Methodology: SG, PN, SKS, BM, DLP; Project administration: VM, SCP, ACA; Resources: SG, PN, SKS, BM, DLP; Software: SG; Supervision; VM, SCP, ACA; Validation: VM, SCP, ACA; Visualization: SG; Roles/Writing - original draft: SG, DLP; Writing - review & editing: SG, SCP, VM, PN, SKS, BM, DLP, and ACA.
Funding
None.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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