Abstract
Background
Elderly patients are evaluated for liver transplantation (LT) with increasing frequency, but outcomes in this group have not been well defined.
Methods
A linkage of the Scientific Registry of Transplant Recipients (SRTR) and the University HealthSystem Consortium (UHC) databases identified 12 445 patients who underwent LT during 2007–2011. Two cohorts were created consisting of, respectively, elderly recipients aged ≥70 years (n = 323) and recipients aged 18–69 years (n = 12 122). A 1:1 case-matched analysis was performed based on propensity scores.
Results
Elderly recipients had lower Model for End-stage Liver Disease (MELD) scores at LT (median 15 versus 19; P < 0.0001), more often underwent transplantation at high-volume centres (46% versus 33%; P < 0.0001) and more often received grafts from donors aged >60 years (24% versus 15%; P < 0.0001). The two cohorts had similar hospital lengths of stay, in-hospital mortality, hospital costs and 30-day readmission rates. There were no differences in graft survival between the two cohorts (P = 0.10), but elderly recipients had worse longterm overall survival (P = 0.009). However, a case-controlled analysis confirmed similar perioperative hospital outcomes, graft survival and longterm patient survival in the two matched cohorts.
Conclusions
Elderly LT recipients accounted for <3% of all LTs performed during 2007–2011. Selected elderly recipients have perioperative outcomes and survival similar to those in younger adults.
Introduction
An increasing number of older patients with end-stage liver disease (ESLD) are evaluated for liver transplantation (LT). In fact, patients aged ≥65 years represent one of the fastest-growing patient populations in LT.1 The most extreme of these patients, those aged ≥70 years, are associated with several difficult clinical dilemmas. Firstly, advanced patient age is associated with higher risk and poorer outcomes after complex surgical procedures.2 Specific to the field of transplantation, advanced recipient age is associated with increased risk for infection3 and cardiovascular disease, increased resource utilization4 and lower patient survival.5 As the number of adult candidates on the waiting list continues to rise and organ availability remains unable to fully meet this demand, proper organ allocation and utilization are critically important. Unfortunately, national data that might guide the addressing of these issues for an expanding older LT recipient population are scarce in the USA.
The goal of the present study was to evaluate the safety and efficacy of LT in patients aged ≥70 years. A novel database created by linking two resources was used to evaluate perioperative hospital outcomes, graft survival and patient survival in the elderly patient population and to compare these findings with those in a younger cohort. This evaluation should contribute to the establishment of baseline outcomes for elderly subjects and provide benchmark data for future studies on the role of LT in these patients.
Materials and methods
Database creation and patient selection
The Scientific Registry of Transplant Recipients (SRTR) is administered by the Chronic Disease Research Group of the Minneapolis Medical Research Foundation and maintains scientific data on solid organ transplantation. The SRTR Analysis File was queried to identify all patients (n = 28 880) who underwent LT from 1 January 2007 to 31 December 2011.
The University HealthSystem Consortium (UHC) consists of 118 academic medical centres and 298 affiliated hospitals and represents >90% of non-profit academic medical centres in the USA.6 The UHC Clinical Database/Resource Manager is an administrative database that maintains patient and hospital stay data so that an organization's clinical outcome performance and resource utilization can be assessed. Complete data files were available for the period from 1 January 2007 to 31 December 2011. Patients undergoing LT were identified using International Classification of Diseases Version 9 (ICD-9) procedural codes. Over the same 2007–2011 period, 19 382 patients underwent LT at 67 centres.
The SRTR and UHC databases were linked in a manner that has been previously described.7,8 Common database variables were used to match patients across each dataset and included: recipient age at time of LT; date of LT; recipient gender, and transplantation centre. Recipients aged <18 years and recipients undergoing repeat transplantation were excluded from the study database. This SRTR–UHC linked database contained 12 445 patients submitted to LT during 2007–2011 and represented 43% of all LT procedures performed in the USA over this 5-year period. This cohort was verified as representing donor, recipient and centre characteristics similar to those of the entire SRTR LT database population during the period under study.
Two patient cohorts were created from the linked SRTR–UHC database using recipient age at the time of LT. The elderly cohort consisted of all patients in the linked database who were aged ≥70 years at the time of LT (n = 323, 2.6%). The remaining patients aged 18–69 years (n = 12 122) were used for comparison. Recipient, donor and transplant centre characteristics were compared between the cohorts. The primary purpose of this study was the evaluation of outcomes in the elderly patient cohort, which included graft survival, patient survival, and hospitalization details such as length of stay (LoS) and hospital costs, and rates of 30-day hospital readmission and perioperative mortality.
A case-matched cohort for each group (n = 312) was created using propensity scores and a matching algorithm.9 The propensity scores were created based on the following variables: recipient sex; recipient race; recipient Model for End-stage Liver Disease (MELD) score at the time of transplant; donor age; donor type; donor risk index (DRI) score, and transplant centre volume. These variables were utilized to create a propensity score because they differed significantly between recipients aged 18–69 years and those aged ≥70 years on unadjusted analysis. Hospitalization outcomes, graft survival and patient survival were then compared between the matched cohorts.
Study variables
Recipient and donor race were categorized into four groups: White; Black; Hispanic, and other. Pre-transplant MELD score was calculated for each recipient as previously described10 and recipients were stratified into four groups with MELD scores of 6–13, 14–19, 20–27 and 28–40, respectively. Donor type was categorized according to whether the organ was sourced from a standard criteria donor (SCD), an expanded criteria donor (ECD), or represented a donation after cardiac death (DCD). Expanded criteria donation was based on the United Network for Organ Sharing kidney definition, which included a donor age of ≥60 years or a donor age of 50–59 years with at least two of history of hypertension, cerebrovascular accident as the cause of death and serum creatinine of >132.6 μmol/l. The DRI was calculated as previously described.11 Centres were ranked according to annual case volumes and stratified into tertiles, representing low-volume centres [the third of centres with the lowest annual case volume, ranging from five to a mean ± standard deviation (SD) of 56 ± 4 transplantations per year], medium-volume centres (middle third of centres based on a mean ± SD case volume of 62 ± 6 to 99 ± 10 transplantations per year), and high-volume centres (upper third of centres based on a mean ± SD case volume of 102 ± 9 to 172 transplantations per year).12 Centre volume was recalculated for each year analysed in the study and rankings were based on the number of procedures performed per year, not on cumulative totals. Centres performing fewer than five procedures per year were excluded from the centre volume analysis.
Statistical analysis
Statistical analysis was performed using sas Version 9.3 (SAS Institute, Inc., Cary, NC, USA). A P-value of <0.05 was considered to indicate statistical significance. Study variables were compared between the two cohorts using chi-squared analysis for categorical variables and Wilcoxon rank-sum tests for continuous variables. Graft and patient survival were estimated using Kaplan–Meier survival curves. The log-rank test was used to determine any statistical difference (P < 0.05) in survival between the study cohorts. The median follow-up for the entire study population was 2 years.
This study was approved by and conducted in accordance with the criteria of the University of Cincinnati Institutional Review Board.
Results
Baseline comparison of recipient, donor and centre characteristics
Over the 5-year period of 2007–2011, LT was performed in 323 elderly patients who accounted for only 2.6% of all LTs identified in this study. Recipient characteristics for the elderly (≥70 years of age) and non-elderly (18–69 years) cohorts are listed in Table 1. Although older recipients had medical comorbidities similar to those of the younger cohort, there were several notable differences between the study groups. Elderly recipients were more likely to have received a MELD exception (52% versus 29%), and had lower MELD scores at the time of LT (median score: 15 versus 19).
Table 1.
Unadjusted characteristics of liver transplant patients aged 18–69 years (n = 12 122) and ≥70 years (n = 323)
| Recipients aged 18–69 years | Recipients aged ≥70 years | P-value | |||
|---|---|---|---|---|---|
| Male, n (%) | 8184 | 68% | 200 | 62% | 0.03 |
| Race, n (%) | <0.001 | ||||
| White | 8785 | 72% | 230 | 71% | |
| Black | 1230 | 10% | 18 | 6% | |
| Hispanic | 1343 | 11% | 31 | 10% | |
| Other | 764 | 6% | 44 | 14% | |
| Insurance, n (%) | <0.001 | ||||
| Private | 7432 | 61% | 61 | 19% | |
| Government | 4494 | 37% | 260 | 81% | |
| Other | 196 | 2% | 2 | 0.6% | |
| BMI, kg/m2, median (IQR) | 27.48 | (24.12–31.75) | 26.08 | (23.30–28.90) | <0.001 |
| Recipient medical history, n (%) | |||||
| Diabetes | 2882 | 24% | 89 | 28% | 0.12 |
| Angina | 287 | 3% | 21 | 7% | <0.001 |
| Haemodialysis | 919 | 8% | 15 | 5% | 0.05 |
| Ventilator | 462 | 4% | 10 | 3% | 0.51 |
| Bacterial peritonitis | 641 | 6% | 13 | 4% | 0.28 |
| Portal vein thrombosis | 362 | 3% | 15 | 5% | 0.10 |
| TIPS | 720 | 6% | 18 | 6% | 0.73 |
| MELD exception | 3522 | 29% | 169 | 52% | <0.001 |
| MELD score | <0.001 | ||||
| 6–13 | 3325 | 27% | 127 | 39% | |
| 14–19 | 3081 | 25% | 92 | 28% | |
| 20–27 | 2996 | 25% | 63 | 20% | |
| 28–40 | 2720 | 22% | 43 | 13% | |
| Transplant centre volume | <0.001 | ||||
| Lower third | 4039 | 33% | 95 | 29% | |
| Middle third | 4104 | 34% | 80 | 25% | |
| Upper third | 3963 | 33% | 148 | 46% | |
| Aetiology of liver disease | <0.001 | ||||
| Viral | 4663 | 38% | 82 | 25% | |
| HCC | 1355 | 11% | 63 | 20% | |
| Alcohol | 1560 | 13% | 39 | 12% | |
| NASH | 1515 | 13% | 70 | 22% | |
| Other | 3028 | 25% | 69 | 21% | |
BMI, body mass index; IQR, interquartile range; HCC, hepatocellular carcinoma; MELD, Model for End-stage Liver Disease; NASH, non-alcoholic steatohepatitis; TIPS, transjugular intrahepatic portosystemic shunt.
Donor characteristics for the two cohorts are listed in Table 2. Donor race, donor cause of death, and organ allocation were similar between the two cohorts. However, elderly patients were more likely to be recipients of allografts from donors aged >60 years (24% versus 15%) and received allografts with higher DRI scores compared with the younger cohort (DRI score >1.8: 28% versus 22%). Additionally, elderly recipients were more frequently transplanted at high-volume centres (46% versus 33%) compared with recipients aged 18–69 years (Table 1).
Table 2.
Unadjusted characteristics of donors of liver grafts to liver transplant patients aged 18–69 years (n = 12 122) and ≥70 years (n = 323)
| Recipients aged 18–69 years | Recipients aged ≥70 years | P-value | |||
|---|---|---|---|---|---|
| Male, n (%) | 7204 | 59% | 196 | 61% | 0.65 |
| Age of donor, n (%) | <0.001 | ||||
| <40 years | 5425 | 45% | 139 | 43% | |
| 40–49 years | 2466 | 20% | 55 | 17% | |
| 50–59 years | 2337 | 19% | 51 | 16% | |
| 60–69 years | 1386 | 11% | 46 | 14% | |
| ≥70 years | 508 | 4% | 32 | 10% | |
| Race, n (%) | 0.97 | ||||
| White | 8097 | 67% | 220 | 68% | |
| Black | 2213 | 18% | 56 | 17% | |
| Hispanic | 1394 | 12% | 36 | 11% | |
| Other | 418 | 3% | 11 | 3% | |
| Donor type, n (%) | 0.02 | ||||
| SCD | 7895 | 68% | 193 | 61% | |
| ECD | 3058 | 27% | 97 | 31% | |
| DCD | 589 | 5% | 24 | 8% | |
| Split graft, n (%) | 730 | 6% | 15 | 5% | 0.30 |
| BMI, kg/m2, median (IQR) | 26.23 | (23.02–30.24) | 25.77 | (22.60–29.80) | 0.16 |
| Cause of death, n (%) | 0.45 | ||||
| Trauma | 4003 | 33% | 110 | 34% | |
| Anoxia | 2523 | 21% | 74 | 23% | |
| Cerebrovascular accident | 4714 | 39% | 122 | 38% | |
| Other | 882 | 7% | 17 | 5% | |
| Organ allocation, n (%) | 0.80 | ||||
| Local | 8600 | 71% | 225 | 70% | |
| Regional | 2265 | 19% | 61 | 19% | |
| National | 1257 | 10% | 37 | 11% | |
| Donor risk index, n (%) | 0.05 | ||||
| <1.2 | 3737 | 31% | 96 | 30% | |
| 1.2–1.49 | 3179 | 26% | 78 | 24% | |
| 1.5–1.79 | 2551 | 21% | 58 | 18% | |
| >1.8 | 2655 | 22% | 91 | 28% | |
| Cold ischaemia time, h, median (IQR) | 6.5 | (5–8) | 6 | (5–8) | 0.15 |
| Warm ischaemia time, min, median (IQR) | 40 | (30–50) | 38 | (30–48) | 0.26 |
BMI, body mass index; DCD, donation after cardiac death; ECD, expanded criteria donor; IQR, interquartile range; SCD, standard criteria donor.
Unadjusted perioperative outcomes were compared between the two cohorts. Although elderly recipients were less likely to be discharged to home after LT, both groups had similar hospital LoS, intensive care unit LoS, direct costs, and rates of perioperative mortality and 30-day readmission. Graft and patient survival are depicted in Fig. 1. Elderly patients had similar graft survival (P = 0.10) (Fig. 1a), but worse overall survival (P = 0.009) (Fig. 1b). Rates of 1-, 3- and 5-year overall survival in elderly recipients were 84.9% [95% confidence interval (CI) 80.3–88.4], 74.0% (95% CI 67.9–79.1) and 64.1% (95% CI 54.6–72.1), respectively. Rates of 1-, 3- and 5-year overall survival in the younger cohort were 89.4% (95% CI 88.9–90.0), 79.7% (95% CI 78.9–80.6) and 72.3 (95% CI 71.0–73.6), respectively.
Figure 1.
(a) Unadjusted graft survival and (b) patient survival in elderly liver transplant recipients (aged ≥70 years) and recipients aged 18–69 years
Adjusted outcomes with case-matched analysis
A case-matched analysis of outcomes was performed using matched cohorts created from propensity scores. The 1:1 matching algorithm identified two matched cohorts (n = 312 in each) in which all differences between donor and recipient characteristics were eliminated. This allowed for the direct comparison of outcomes between the study cohorts, which again demonstrated similar perioperative outcomes (Table 3). There was no detectable difference in graft survival at 1 year between the elderly cohort and those aged 18–69 years (93% versus 89%). Graft and patient survival were evaluated in the matched cohorts and are displayed in Fig. 2. There were no differences in overall graft survival (P = 0.35) (Fig. 2a) or patient survival (P = 0.13) (Fig. 2b).
Table 3.
Perioperative outcomes in case-matched liver transplant patients aged 18–69 years (n = 312) and ≥70 years (n = 312)
| Recipients aged 18–69 years | Recipients aged ≥70 years | P-value | |||
|---|---|---|---|---|---|
| Hospital LoS, days, median (IQR) | 10 | (7–15) | 10 | (7–16) | 0.97 |
| ICU LoS, days, median (IQR) | 3 | (1–5) | 3 | (2–6) | 0.70 |
| Mortality, n (%) | 12 | 4% | 10 | 3% | 0.67 |
| Routine discharge home, n (%) | 264 | 85% | 239 | 77% | 0.01 |
| Direct cost, US$, median (IQR) | 111 000 | (87 000–145 000) | 108 000 | (80 000–155 000) | 0.90 |
| 30-day readmission, n (%) | 108 | 35% | 102 | 33% | 0.59 |
| 1-year graft failure, n (%) | 35 | 11% | 23 | 7% | 0.10 |
ICU, intensive care unit; IQR, interquartile range; LoS, length of stay.
Figure 2.
(a) Adjusted graft survival and (b) patient survival in case-matched elderly liver transplant recipients (aged ≥70 years) and recipients aged 18–69 years
Discussion
This study utilized a linkage between the SRTR and UHC clinical databases to evaluate the current status of LT in elderly patients. Elderly patients represent <3% of LT recipients operated during 2007–2011. An unadjusted analysis of outcomes in this cohort and in patients aged 18–69 years demonstrated similar perioperative outcomes and graft survival. However, in the unadjusted analysis elderly patients were found to have worse overall survival. Several differences existed at baseline between the study groups including in recipient demographics, pre-transplant MELD scores, donor age and type, DRI score, and transplant centre. In order to account for these differences, propensity scores were used to create matched cohorts for comparison. In this matched analysis, there were no differences in patient or graft survival. This matched analysis suggests that equivalent outcomes can be achieved in elderly recipientsand that advanced recipient age should not be used as a barrier to LT.
Recent data for waitlist registrants on the SRTR registry suggest that <12% of waitlisted patients are aged ≥65 years, but this proportion has steadily increased over the past decade. Continued improvements in care in pre- and post-transplant medicine and surgery suggest that this age group will continue to grow on the waiting list. With this demographic shift in the ESLD and national populations, more elderly patients will be considered for LT and the use of scarce donor livers will need to be addressed because these recipients have a shortened lifespan compared with younger recipients. Despite the shortened lifespan, single-centre reports have shown equivalent post-transplant survival in selected patients.13 Studies in support of LT in geriatric recipients document 5-year survival rates of close to 70%.14,15 Schwartz and colleagues reported similar survival in hepatocellular carcinoma (HCC) patients aged ≥70 years compared with younger recipients.16 Another recent report attempted to define five prognostic factors for outcome in recipients aged >60 years and included ventilator status, diabetes mellitus, hepatitis C virus, creatinine levels of ≥1.6 mg/dl, and a combined recipient and donor age of ≥120 years.17 The present review of the literature focused on recent studies in the context of recent improvements in the care of LT recipients because many studies conducted in previous decades reported inferior outcomes in older recipients.18 The present report confirms previous findings with short-term follow-up of equivalent survival, but is the first to report a multicentre review of peritransplant hospital utilization and outcomes in these patients. Discharge disposition was the only perioperative outcome for which the two groups differed significantly. Further research is needed to determine the impact of this variable on outcomes and cost-effectiveness after LT.
Growing concern regarding post-LT outcomes has led to an increased focus on selection among both donors and candidate recipients. The evaluation of potential recipients requires some complex clinical decision making with regard to their general health, the severity of their ESLD and their potential survival after LT. The MELD allocation system is based on the risk for mortality without LT and therefore does not take into account survival-associated risk after LT. This is dependent on the practitioner at the transplant centre. It is a crucial issue in the context of elderly patients because their overall survival is already limited and documenting a longterm survival benefit with LT may be difficult, as it is with kidney transplant.19,20 The present data attempt to address this issue by incorporating all factors in the transplant process (donor, recipient and centre characteristics) and using propensity scores to control for patient selection and bias. This study was able to eliminate all differences in demographic characteristics between the two groups and subsequently show that, at a median follow-up of 2 years, patient survival does not differ between them. This study is important because the elderly population is growing and is expected to impose an increasing burden of disease. Although this population accounted for only 2.6% of all LTs performed over the 5-year period surveyed in the current study, this proportion is likely to increase over time.
The data presented here were sourced from the SRTR and UHC databases in combination in order to provide insight into transplant-specific variables and to facilitate an examination of perioperative and postoperative metrics from the hospital perspective. Patient selection must be optimal and the timing of orthotopic LT (OLT) critical if it is to achieve maximal utility in ESLD patients. Key factors for success include the provision of lifelong medical follow-up and medications, access to care when ill, and the provision of appropriate education and resources to manage any complications. Increasing insurance regulation, restrictions in the use of medications and centre-based restrictions for listing and transplant may make these differences larger in the future. Despite these unknowns, the present study nonetheless demonstrates differences in recipients at the time of OLT (MELD score, independent status, not hospitalized), but does not support any conclusion on whether these factors played a role in the worse outcome in the elderly group. The utilization of hospital resources was similar in both groups, except in terms of discharge disposition, which suggests that elderly recipients are appropriately selected. Whether current selection protocols are too restrictive cannot be ascertained from these data because the elderly patient group represented only 2.6% of LTs in the study population.
This study has several potential limitations. It used a large retrospective database cohort derived from two administrative databases. Although this linkage of the UHC and SRTR databases represents >40% of all OLTs performed in adults in the USA over the 5-year period, it is possible that the database is skewed toward areas of higher competition and organ availability. It is also possible that the data would differ if all LTs were accounted for; however, the demographic data used in the present study were examined and compared with data in the entire SRTR file and were found to be similar in donor, recipient and centre characteristics. The present data do not include non-transplant-related comorbidities or provide the ability to address longterm factors related to survival, including understanding of adherence to immunosuppression and compliance. This is an important constraint because elderly recipients were found to have a higher rate of mortality within a 2-year follow-up, but this does not appear to be associated with graft-related issues because graft survival was similar across the groups. Linkage with the UHC database provides additional insight into the perioperative outcomes and resource utilization of these patients; however, patient data are available only for the study time period evaluated. This limitation in the availability of data accounts for the relatively short median follow-up time reported in this study.
In summary, elderly patients represent <3% of LT recipients operated during 2007–2011. These patients have perioperative outcomes and graft survival similar to those in younger adults. After adjusting for patient differences with a case-controlled analysis, patient survival was found to be similar among elderly patients and those aged 18–69 years. Survival differences in the present unadjusted analysis suggest the importance of patient selection and the maintenance of postoperative health after LT. Based on this analysis, elderly patients may represent an underserved patient population that would benefit from LT. Future studies should focus on evaluating risk factors for poor outcomes in the elderly patient population to help guide patient selection.
Conflicts of interest
None declared.
References
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