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Long-term Outcomes After Liver Transplantation Among Human Immunodeficiency Virus–Infected Recipients

Locke, Jayme E. MD, MPH1; Durand, Christine MD2; Reed, Rhiannon D. MPH1; MacLennan, Paul A. PhD1; Mehta, Shikha MD1; Massie, Allan PhD3; Nellore, Anoma MD1; DuBay, Derek MD1; Segev, Dorry L. MD PhD3

doi: 10.1097/TP.0000000000000829
Original Clinical Science—Liver
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Background Early outcomes after human immunodeficiency virus (HIV) + liver transplantation (LT) are encouraging, but data are lacking regarding long-term outcomes and comparisons with matched HIV− patients.

Methods We examined outcomes among 180 HIV+ LT, and compared outcomes to matched HIV− counterfactuals (Scientific Registry of Transplant Recipients 2002-2011). Iterative expanding radius matching (1:10) on recipient age, race, body mass index, hepatitis C virus (HCV), model for end-stage liver disease score, and acute rejection; and donor age and race, cold ischemia time, and year of transplant. Patient survival and graft survival were estimated using Kaplan-Meier methodology and compared using log-rank and Cox proportional hazards. Subgroup analyses were performed by transplant era (early: 2002-2007 vs modern: 2008-2011) and HCV infection status.

Results Compared to matched HIV− controls, HIV+ LT recipients had a 1.68-fold increased risk for death (adjusted hazard ratio [aHR], 1.68, 95% confidence interval [95% CI], 1.28-2.20; P < 0.001), and a 1.70-fold increased risk for graft loss (aHR, 1.70; 95% CI, 1.31-2.20; P < 0.001). These differences persisted independent of HCV infection status. However, in the modern transplant era risk for death (aHR, 1.11; 95% CI, 0.52-2.35; P = 0.79) and graft loss (aHR, 0.89; 95% CI, 0.42-1.88; P = 0.77) were similar between monoinfected and uninfected LT recipients. In contrast, independent of transplant era, coinfected LT recipients had increased risk for death (aHR, 2.24; 95% CI, 1.43-3.53; P < 0.001) and graft loss (aHR, 2.07; 95% CI, 1.33-3.22; P = 0.001) compared to HCV+ alone LT recipients.

Conclusions These results suggest that outcomes among monoinfected HIV+ LT recipients have improved over time. However, outcomes among HIV+ LT recipients coinfected with HCV remain concerning and motivate future survival benefit studies.

Risk for death and graft loss were similar between HIV+ monoinfected and uninfected liver transplant recipients. In contrast, independent of transplant era, HIV+/HCV+ coinfected liver transplant recipients had increased risk for death and graft loss compared to HCV+ alone liver transplant recipients.

1 University of Alabama at Birmingham, Birmingham, AL.

2 Department of Medicine, Division of Infectious Diseases, Johns Hopkins School of Medicine, Baltimore, MD.

3 Departments of Surgery and Epidemiology, Johns Hopkins University, Baltimore, MD.

Received 20 December 2014. Revision requested 6 March 2015.

Accepted 24 March 2015.

This research was supported in part by NIH K24DK101828 (PI: Segev).

The authors declare no conflicts of interest.

J.E.L., C.D., and D.L.S. participated in research design, writing of the article, and performance of the research. R.D.R. and P.M. participated in data analysis. A.M. contributed new analytic tool. S.M., A.N., and D.D. participated in writing of the article.

The research was presented in preliminary forms as abstracts at the 2014 American Society of Transplant Surgeons State of the Art Winter Symposium and the 2014 World Transplant Congress. The data reported here have been supplied by the Minneapolis Medical Research Foundation as the contractor for the SRTR. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as an official policy of or interpretation by the SRTR or US government. These analyses were performed by the UAB Comprehensive Transplant Institute Outcomes Research Center analytic team.

Correspondence: Jayme E. Locke, MD, MPH, 701 19th Street South, LHRB 748, Birmingham, AL 35294. (jlocke@uabmc.edu).

Improvements in the care of human immunodeficiency virus–infected (HIV+) patients, including potent antiretroviral therapy (ART), development of integrase inhibitors, and once a day ART regimen, have resulted in the decline of HIV-related deaths; as such, the life expectancy of HIV+ individuals has increased.1-3 Chronic diseases, such as end stage liver disease (ESLD), have now surpassed opportunistic infections as the leading causes of death among HIV+ individuals.4,5 Liver transplantation is now offered as an acceptable treatment option for HIV+ ESLD patients and is being offered outside of clinical trials. Although this marks a new era in the care of the HIV+ ESLD patient, experience with HIV+ liver transplantation remains limited.

Recently, the largest prospective United States cohort study reported outcomes among 89 HIV+ liver transplant recipients coinfected with hepatitis C virus (HCV)+: 3-year patient and graft survival (GS) were 60% and 53%, respectively, both significantly lower than survival rates among a cohort of unmatched HCV+ liver transplant recipients.6 Donor age older than 50 years, low recipient body mass index (BMI), need for simultaneous kidney transplant, and the use of HCV+ donor livers were found to be predictors of worse outcomes among coinfected recipients. When these high risk factors were avoided, HIV+/HCV+ liver transplant recipients experienced similar outcomes to an unmatched cohort of elderly (older than 65 years) HIV−/HCV− liver recipients. The median length of follow-up (f/u) among study participants was 1.8 years (interquartile range [IQR], 0.7-3.4), but fewer than 25 patients had 3 years of f/u. Although these findings are encouraging, concerns remain about the high incidence of acute rejection and acceleration of cirrhosis after HIV+ liver transplantation, and the possible impact on long-term outcomes.6-9 Furthermore, both control cohorts (unmatched HCV+ recipients and unmatched elderly HIV−/HCV− recipients) failed to provide an appropriate counterfactual comparison.

To date, no study has examined outcomes among HIV+ monoinfected recipients, quantified long-term outcomes in monoinfected or coinfected recipients, nor compared monoinfected or coinfected recipients to their appropriately matched HIV− counterparts. Furthermore, current practice is based on results from a highly scrutinized clinical protocol used within the prospective NIH trial. The trial was limited to high volume centers, involved only 89 participants, and was limited to HIV+ recipients coinfected with HCV+, representing a highly selected subset of the more than 180 HIV+ liver transplants that have been performed in the United States.6 Going beyond the confines of the NIH trial to study the entire United States experience with HIV+ liver transplantation is necessary to properly assess the generalizability of findings and provides the sample size necessary for risk factor estimation, allowing for comparison to properly matched controls.

To better understand outcomes in this unique population, we conducted a retrospective cohort study to: (1) examine long-term patient survival (PS) and GS among the United States HIV+ liver transplant population in its entirety, including both monoinfected and coinfected HIV+ recipients, and (2) compare these outcomes to those of matched HIV− recipients.

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METHODS

Data Source

This study used data from the Scientific Registry of Transplant Recipients (SRTR). The SRTR data system includes data, submitted by the members of the Organ Procurement and Transplantation Network, on all donors, waitlisted candidates, and transplant recipients in the United States. The Health Services Resources and Services Administration of the US Department of Health and Human Services provides the oversight to the activities of the Organ Procurement and Transplantation Network and SRTR contractors. This study received approval from the University of Alabama at Birmingham Institutional Review Board.

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Study Population

All adult first-time liver transplant patients with known HIV status who were transplanted between January 1, 2002, and December 31, 2011, were identified (HIV+, 180; HIV−, 34,020). Patients were excluded from the adjusted multivariable and matched controlled analyses if they were missing information on cold ischemia time (n = 8), BMI (n = 7), HCV status (n = 10), or a combination of the 3 (n = 3).

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Outcome Ascertainment

The primary outcome measures were GS and PS. Graft survival was defined as the time from transplantation to graft loss or death; PS was defined as the time from transplantation to death. Death indicators were supplemented by linkage to the Social Security Death Master File. Both GS and PS were censored for administrative end of study.

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Statistical Analyses

Exploratory Data Analysis

Donor and recipient variables were analyzed using t tests or Wilcoxon rank-sum tests (based on distribution) and categorical variables were examined using χ2 or Fisher exact tests of independence (based on sample size).

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Survival Analyses

The GS and PS were estimated among HIV+ recipients and compared between HIV+ recipients and HIV− recipients from the general population using Kaplan-Meier methods, log rank tests, and Cox proportional hazards models. Risk factors for graft loss and death within the HIV+ cohort were identified using univariate Cox proportional hazards with statistical significance set at 0.1. The GS and PS were also estimated among the entire cohort of HIV+ recipients matched to appropriate HIV− controls (1:10) using expanded radius matching. The HIV+ and HIV− liver transplant recipients were matched on recipient age, race, BMI, HCV infection, model for end-stage liver disease (MELD) score, and acute rejection; and donor age and race, cold ischemia time, and year of transplant. Subgroup analyses by transplant era (early: 2002-2007 vs modern: 2008-2011) and HCV infection status were also performed.

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Sensitivity Analyses

The same covariates used to create the matched cohort were used to build the full multivariate models. Results from these models confirmed inferences reported from the matched (1:10) analyses. Matched control analyses must balance introduction of bias with reduction in variability (ie, with increasing numbers of controls per patient, more bias is potentially introduced, yet variability is theoretically reduced). Given this, the analyses were performed among 4 distinct matched cohorts (1:1; 1:3; 1:5; and 1:10); inferences did not change. For the purposes of simplicity, results comparing outcomes among HIV+ and HIV− liver transplant recipients are from the 1:10 matched cohort.

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RESULTS

Study Population

Between 2002 and 2011, there were 180 first-time liver transplants performed among HIV+ adult recipients (median f/u, 3.1 years; IQR, 1.6-6.0) and 34,020 performed among HIV− recipients (median f/u, 4.5 years; IQR, 2.5-6.9). Since 2002, there has been a 4-fold increase in the number of transplant performed in HIV+ recipients (Figure 1). Compared to HIV− recipients, HIV+ recipients were younger (≥50 years old: 55% vs 72.7%; P < 0.001), more often men (77.8% vs 67.5%; P = 0.003), and more likely to be African American (25% vs 9.4%; P < 0.001). Additionally, they were more often underweight (4.1% vs 1.9%; P < 0.001), and more likely to be infected with HCV (64.9% vs 45.8%; P < 0.001) and hepatitis B virus (64.1% vs 45.8%; P < 0.001) (Table 1).

FIGURE 1

FIGURE 1

TABLE 1

TABLE 1

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Long-Term PS

Among all HIV+ recipients, 5-year PS was 55.8%, and 10-year PS was 41.0% (Table 2). The PS was not statistically different among monoinfected (HIV+/HCV−) compared to coinfected (HIV+/HCV+) recipients at 5 years (64.8% (HIV+/HCV−) versus 51.8% (HIV+/HCV+), P = 0.15) or 10 years (43.9% [HIV+/HCV−] vs 44.1% [HIV+/HCV+]; P = 0.2) after transplantation. Among HIV+ recipients, the risk of death was greater in the presence of a pretransplant glomerular filtration rate less than 30 mL/min (hazard ratios, 2.44; 95% CI, 1.12-5.31; P = 0.03) (Table 3).

TABLE 2

TABLE 2

TABLE 3

TABLE 3

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PS Compared to HIV− Population

Compared to the general HIV− population, 5- and 10-year survival were significantly worse among HIV+ recipients (5 years: 55.8% vs 73.4%; P < 0.001; 10 years: 41.0% vs 60.9%; P < 0.001). Although PS was higher among monoinfected recipients (5 years, 64.8%; 10 years, 43.9%), it remained statistically lower than the uninfected (HIV−/HCV−) general transplant population (P = 0.05). Moreover, coinfected patients (HIV+/HCV+) had significantly lower PS (5 years, 51.8%; 10 years, 44.1%) compared to HCV+ recipients from the general transplant population (5 years, 69.1%; 10 years, 55.9%; P < 0.001) (Table 2). These differences persisted even when compared to appropriately matched HIV− controls (5 years: 55.8% vs 72.1%; P < 0.001; 10 years: 39.3% vs 57.1%; P < 0.001; adjusted hazard ratio [aHR], 1.68; 95% CI, 1.28-2.20; P < 0.001) (Figure 2), and across transplant era (early era: aHR, 1.66; 95% CI, 1.11-2.50; P < 0.001; modern era: aHR, 1.88; 95% CI, 1.26-2.82; P < 0.001) (Table 4).

FIGURE 2

FIGURE 2

TABLE 4

TABLE 4

Stratification by HCV status within each era demonstrated improved outcomes over time among monoinfected patients, such that in the modern transplant era, there was no longer a difference in risk for death between monoinfected and uninfected recipients (aHR, 1.11; 95% CI, 0.52-2.35; P = 0.79). In contrast, survival did not improve over time among coinfected patients, such that, compared to HCV+ alone recipients, increased risk for death persisted over time (aHR, 2.24; 95% CI, 1.43-3.53; P < 0.001) (Table 4).

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Long-Term GS

Among all HIV+ recipients, 5-year GS was 50.7%, and 10-year GS was 35.4% (Table 2). There was no statistically significant difference in GS among monoinfected (HIV+/HCV−) compared to coinfected (HIV+/HCV+) recipients at 5 years (59.3% [HIV+/HCV−] vs 46.4% [HIV+/HCV+]; P = 0.19) and 10 years (35.1% [HIV+/HCV−] vs 41.1% [HIV+/HCV+]; P = 0.28) after transplantation. Among HIV+ recipients, the risk for graft loss was greater with the use of liver grafts from donors over the age of 50 years (hazard ratios, 1.70; 95% CI, 1.11-2.60; P = 0.01) (Table 3).

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GS Compared to HIV− Population

Compared to the general HIV− population, 5- and 10-year survivals were significantly worse among HIV+ recipients (5 years: 50.7% vs 70.1%; P < 0.001; 10 years: 35.4% vs 57.8%; P < 0.001). Moreover, monoinfected recipients had significantly lower GS (5 years, 59.3%; 10 years, 35.1%) compared to the uninfected transplant population (5 years, 73.8%; 10 years, 62.2%; P = 0.05). Further, compared to HCV+ recipients (5 years, 66.0%; 10 years, 53.0%), coinfected patients (HIV+/HCV+) had significantly lower GS (5 years, 46.4%; 10 years, 41.1%; P < 0.001) (Table 2). These differences in GS remained even when comparing HIV+ recipients with appropriately matched HIV− controls (5 years: 51.3% vs 68.4%; P < 0.001; 10 years: 34.2% vs 53.7%; P < 0.001; aHR, 1.70; 95% CI, 1.31-2.20; P < 0.001) (Figure 3), and across transplant era (early era aHR, 1.86; 95% CI, 1.23-2.70; P = 0.001; modern era aHR, 1.58; 95% CI, 1.06-2.34; P = 0.02) (Table 4).

FIGURE 3

FIGURE 3

Stratification by HCV status within each era demonstrated improved outcomes over time among monoinfected patients, such that in the modern transplant era, there was no longer a difference in risk for graft loss between monoinfected and uninfected recipients (aHR, 0.89; 95% CI, 0.42-1.88; P = 0.77). Differences in risk for graft loss persisted in the modern era among coinfected patients when compared to recipients with HCV alone (aHR, 2.07; 95% CI, 1.33-3.22; P = 0.001) (Table 4).

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DISCUSSION

In this national study of long-term outcomes among HIV+ liver transplant recipients, we found that, compared to the general HIV− liver recipient population, long-term GS and PS were significantly lower among HIV+ recipients, particularly among those recipients coinfected with HCV. In fact, at 10 years after transplantation, only 35.4% of HIV+ recipients had functioning grafts, and 41.0% were still living compared to 57.8% and 60.9%, respectively, among the general population of HIV− recipients. Significant differences in baseline characteristics of HIV+ recipients compared to the general population of HIV− recipients were identified, including factors known to be associated with increased risk of graft loss and death, such as coinfection with HCV and hepatitis B and African American race. Interestingly, however, even after adjusting for these potential confounders, HIV+ liver recipients continued to have lower GS and PS at 5 and 10 years after transplantation compared to their appropriately matched HIV− counterparts.

Although these findings likely reflect the natural history of HIV, it is also possible that residual confounding exists. In particular, cumulative viremia among HIV+ individuals has been identified as an important predictor of progression to liver fibrosis. A recent cohort study of 288 HIV/HCV coinfected participants demonstrated a 1.2-fold increased risk of fibrosis progression for each additional 1 log10 copies/mL HIV RNA cumulative exposure.10 Although an undetectable plasma HIV viral load is generally required for transplant candidacy, SRTR data lack granularity with regard to viral load at the time of transplant, time of suppressed viral load, and HIV suppression after transplantation. Moreover, similar effects of cumulative viremia have been observed among HCV+ individuals. Although most HCV+ patients are viremic at the time of transplant, SRTR data do not quantify HCV viral load or document changes over time.11 Not surprisingly, multiple studies have demonstrated accelerated fibrosis before and after transplantation in the setting of HIV/HCV coinfection, as the individual viral effects appear to be additive in the setting of coinfection.7,8

Since their introduction in 2008, integrase-strand transfer inhibitors have become the recommended ART regimen in the transplant setting, as they do not interact with standard maintenance immunosuppressants, such as calcineurin inhibitors.12-14 We further explored the matched cohort by transplant era (before and after introduction of integrase-strand transfer inhibitors), and observed that among monoinfected patients, there was no longer a significant difference in GS or PS in the modern era, suggesting that outcomes among monoinfected patients have improved over time. In contrast, independent of transplant era, HIV+ recipients coinfected with HCV continued to have worse outcomes when compared to HIV−/HCV+ recipients, suggesting that HCV coinfection was an effect modifier for outcomes among HIV+ recipients.

Although our findings among coinfected patients are worrisome, data suggest that HIV+ recipients do derive a significant survival benefit from transplant, as accelerated cirrhosis and high mortality rates among HIV+ ESLD patients have been well documented.15-17 A study of HIV+ liver transplant waitlist candidates demonstrated that each unit increase in MELD score was associated with a 20% increase in the risk of pretransplantation death.17 Moreover, the study found that detectable HIV RNA at baseline was associated with a 3.2-fold increased risk for death and a 2.79-fold increased risk for liver disease progression as measured by MELD. It is important to note that in the current ART era, liver disease is now the most frequent cause of death among HIV+ individuals, likely related to complications of HCV coinfection as well as hepatotoxicity secondary to ART. As such, the need for liver transplantation among this unique population is on the rise.18,19 Therefore, the ability to assess the potential survival benefit of liver transplantation among HIV+ ESLD patients is of paramount importance. Given the small number of HIV+ liver transplants performed to date, pooled national data are needed to properly address this concern. Currently, HIV serostatus of waitlist registrants/candidates is not reported to United Network for Organ Sharing. This has hampered efforts to study survival benefit among this unique population on a national scale.

Although our study did not identify potentially modifiable recipient factors, we did find a significant increase in risk for graft loss among HIV+ recipients of liver grafts from older donors (≥50 years). Our findings parallel results from studies within the general HCV+/HIV− transplant population that have demonstrated an association between older donor age and increased risk of graft loss and patient death.20,21 Results from our study and others suggest that the effect of older donor age on outcomes after liver transplantation is more pronounced among HIV+ recipients compared to their HIV− counterparts.6,15 These findings motivate a focus in clinical practice to avoid grafts from donors over the age of 50 years among HIV+ recipients, which may serve to improve outcomes among this vulnerable population.

Inferences based on our findings must take into account a number of important limitations. The SRTR data lack granularity with regard to CD4 count, viral loads, infections, and malignancies—factors that are known to influence long-term outcomes among HIV+ patients. However, the NIH protocol used relatively restricted criteria for HIV+ ESLD patients to be considered candidates for transplantation, requiring CD4 counts greater than 100. It is unlikely that there would be major deviations from this protocol in the national data. Moreover, immunosuppressant levels and antiviral regimen are not captured by SRTR data, and as such, it is impossible to determine whether drug interactions between HAART therapy and immunosuppressants led to subtherapeutic drug levels and higher rates of acute rejection and graft loss. Although understanding these interactions would help inform the mechanism of our long-term findings, the absence of these data does not bias our findings. Finally, the sample size available for our subgroup analyses were relatively small and may impact the accuracy of our estimates. However, these data represent the HIV+ liver transplant population in the United States in its totality, and therefore, contribute new and important information about long-term outcomes after liver transplantation in this unique population.

This is the first national study to examine long-term outcomes among the entire United States cohort of HIV+ liver transplant recipients and to compare these outcomes to appropriately matched HIV− counterfactuals. We found long-term GS and PS to have improved among monoinfected patients in the modern transplant era and were similar to matched HIV−/HCV− controls. In contrast, independent of transplant era, outcomes among HIV+ patients coinfected with HCV continue to be worrisome. These results motivate future studies of survival benefit in this vulnerable population.

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